Skip to main content

Advertisement

SpringerLink
Log in

The importance of fine-scale breeding site selection patterns under a landscape-sharing approach for wolf conservation

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

For large carnivores persisting in human-dominated landscapes, conservation planning is often hindered by the large spatial requirements of these species, availability of protected areas, and human land uses. Protected areas are usually too small to support viable populations, and scattered across a human land-use matrix. Therefore, large carnivore conservation should be planned at large spatial scales under a land-sharing approach (allowing the coexistence between large carnivores and people in the same landscape), which means increasing the focus on the human-dominated matrix. Most of the critical factors determining large carnivore persistence (i.e., those related to food availability and vulnerability to humans) interact synergistically in space and time during the breeding season. Here, using as a case study a wolf population in NW Iberia, we studied fine-scale breeding site selection patterns (1 and 9 km2) in relation to human pressure, and the availability of food and refuge. The selection of wolf breeding sites in this human-dominated landscape was not determined by potential availability of prey biomass in the immediate vicinity (1 km2). However, wolves selected breeding sites with high availability of refuge (concealing vegetation), and low human accessibility and activity levels. Paved roads showed the highest proportion of independent contribution to explaining breeding site selection patterns (negative influence), being followed by refuge availability (positive influence) and the remoteness of breeding sites in relation to the surrounding spatial context (positive influence). Refuge availability, even at very small spatial scales taking into account the spatial requirements of wolves, may compensate for moderate levels of human activities in the vicinity of breeding sites. The strength of breeding selection patterns varied along a hierarchical process at different spatial scales. Under a landscape-sharing approach, integrating key processes observed in the human-dominated matrix, such as breeding site selection patterns, into landscape planning is of paramount importance for carnivore conservation. By temporally restricting human use on breeding sites and small portions of surrounding lands (~ 1 km2), and by maintaining several small refuge areas interspersed within the human-dominated matrix, we could favor wolf persistence without reducing land availability for other uses, improving the conditions for coexistence between wolves and humans.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmadi M, López-Bao JV, Kaboli M (2014) Spatial heterogeneity in human activities favors the persistence of wolves in agroecosystems. PLoS ONE 9:e108080

    Article  PubMed  PubMed Central  Google Scholar 

  • Alexander JS, Gopalaswamy AM, Shi K, Hughes J, Riordan P (2016) Patterns of Snow Leopard site use in an increasingly human-dominated landscape. PLoS ONE 11:e0155309

    Article  PubMed  PubMed Central  Google Scholar 

  • Athreya V, Odden M, Linnell JD, Krishnaswamy J, Karanth U (2013) Big cats in our backyards: persistence of large carnivores in a human dominated landscape in India. PLoS ONE 8:e57872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Athreya V, Linnell JD, Ghosal S, Odden M (2016) Case study 5 large carnivores in human-dominated landscapes of India. Tropical conservation: perspectives on local and global priorities. Oxford University Press, Oxford, p 132

    Google Scholar 

  • Barton K (2013) MuMIn: multi-model inference. R package version 1.9.5. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Blackburn S, Hopcraft JGC, Ogutu JO, Matthiopoulos J, Frank L (2016) Human–wildlife conflict, benefit sharing and the survival of lions in pastoralist community-based conservancies. J Appl Ecol 53:1195–1205

    Article  Google Scholar 

  • Boron V, Tzanopoulos J, Gallo J, Barragan J, Jaimes-Rodriguez L, Schaller G, Payán E (2016) Jaguar densities across human-dominated landscapes in Colombia: the contribution of unprotected areas to long term conservation. PLoS ONE 11:e0153973

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouyer Y, Gervasi V, Poncin P, Beudels-Jamar RC, Odden J, Linnell JDC (2015) Tolerance to anthropogenic disturbance by a large carnivore: the case of Eurasian lynx in south-eastern Norway. Anim Conserv 18:271–278

    Article  Google Scholar 

  • Brodie JF, Giordano AJ, Dickson B, Hebblewhite M, Bernard H, Mohd-Azlan J, Anderson J, Ambu L (2015) Evaluating multispecies landscape connectivity in a threatened tropical mammal community. Conserv Biol 29:122–132

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2010) Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Capitani C, Mattioli L, Avanzinelli E, Gazzola A, Lamberti P, Mauri L, Scandura M, Viviani A, Apollonio M (2006) Selection of rendezvous sites and reuse of pup raising areas among wolves Canis lupus of north-eastern Apennines, Italy. Acta Theriol 51:395–404

    Article  Google Scholar 

  • Carter NH, Shrestha BK, Karki JB, Pradhan NMB, Liu J (2012) Coexistence between wildlife and humans at fine spatial scales. PNAS 109:15360–15365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chanchani P, Noon BR, Bailey LL, Warrier RA (2016) Conserving tigers in working landscapes. Conserv Biol 30:649–660

    Article  PubMed  Google Scholar 

  • Chapman A, Buck WJ (1910) Unexplored Spain. Edward Arnold, London

    Book  Google Scholar 

  • Chapron G et al (2014) Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346:1517–1519

    Article  CAS  PubMed  Google Scholar 

  • Chevan A, Sutherland M (1991) Hierarchical partitioning. Am Stat 45:90–96

    Google Scholar 

  • Chundawat RS, Sharma K, Gogate N, Malik PK, Vanak AT (2016) Size matters: scale mismatch between space use patterns of tigers and protected area size in a Tropical Dry Forest. Biol Conserv 197:146–153

    Article  Google Scholar 

  • Collinge SK (1996) Ecological consequences of habitat fragmentation: implications for landscape architecture and planning. Landsc Urban Plan 36:59–77

    Article  Google Scholar 

  • Crooks KR, Sanjayan M (eds) (2006) Connectivity conservation, vol 14. Cambridge University Press, Cambridge

    Google Scholar 

  • Cuesta L, Bárcena F, Palacios F, Reig S (1991) The trophic ecology of the Iberian wolf (Canis lupus signatus, Cabrera, 1907): a new analysis of stomach’s data. Mammalia 55:239–254

    Article  Google Scholar 

  • Dellinger JA, Proctor C, Steuryc TD, Kelly MJ, Vaughan MR (2013) Habitat selection of a large carnivore, the red wolf, in a human-altered landscape. Biol Conserv 157:324–330

    Article  Google Scholar 

  • DGCN (2000) Tercer Inventario Forestal Nacional, 1997–2006: Galicia. Ministerio de Medio Ambiente, Dirección General de Conservacion de la Naturaleza, Madrid

  • Elbroch LM, Lendrum PE, Alexander P, Quigley H (2015) Cougar den site selection in the Southern Yellowstone Ecosystem. Mammal Res 60:89–96

    Article  Google Scholar 

  • Epps CW, Mutayoba BM, Gwin L, Brashares JS (2011) An empirical evaluation of the African elephant as a focal species for connectivity planning in East Africa. Divers Distrib 17:603–612

    Article  Google Scholar 

  • Fernández JM, De Azúa NR (2010) Historical dynamics of a declining wolf population: persecution vs. prey reduction. Eur J Wildl Res 56:169–179

    Article  Google Scholar 

  • Fox J, Weisberg S, Bates D, Fox MJ (2012) Package “car”. https://cran.r-project.org/web/packages/car/car.pdf

  • Fuller TK, Sievert PR (2001) Carnivore demography and the consequences of changes in prey availability. In: Gittleman JL, Funk SM, MacDonald D, Wayne RK (eds) Carnivore conservation. Cambridge University Press, Cambridge, pp 163–178

    Google Scholar 

  • García E, Llaneza L, Palacios V, López-Bao JV, Sazatornil V, Rodríguez A, Rivas O, Cabana M (2012) Primeros datos sobre la ecología espacial del lobo en Galicia. Abstracts of the III Iberian Wolf Congress, Lugo (Spain), pp. 44

  • Ginsberg JR (2017) When protected areas prove insufficient: cheetah and “protection-reliant” species. PNAS 201619817

  • Gubbi S, Mukherjee K, Swaminath MH, Poornesha HC (2016) Providing more protected space for tigers Panthera tigris: a landscape conservation approach in the Western Ghats, Southern India. Oryx 50:336–343

    Article  Google Scholar 

  • Guerrero AM, McAllister RYAN, Corcoran J, Wilson KA (2013) Scale mismatches, conservation planning, and the value of social-network analyses. Conserv Biol 27:35–44

    Article  PubMed  Google Scholar 

  • Habib B, Kumar S (2007) Den shifting by wolves in semi-wild landscapes in the Deccan Plateau, Maharashtra, India. J Zool 272:259–265

    Article  Google Scholar 

  • Houle M, Fortin D, Dussault C, Courtois R, Ouellet JP (2010) Cumulative effects of forestry on habitat use by gray wolf (Canis lupus) in the boreal forest. Landsc Ecol 25:419–433

    Article  Google Scholar 

  • Iliopoulos Y, Youlatos D, Sgardelis S (2014) Wolf pack rendezvous site selection in Greece is mainly affected by anthropogenic landscape features. Eur J Wildl Res 60:23–34

    Article  Google Scholar 

  • INE (2010) Censo de población y vivienda. Instituto Nacional de Estadística de España

  • Jêdrzejewski W, Niedzia£kowska M, Myslajek RW, Nowak S, Jêdrzejewska B (2004) Habitat selection by wolves Canis lupus in the uplands and mountains of southern Poland. Acta Theriol 50:417–428

    Article  Google Scholar 

  • Jêdrzejewski W, Niedzia£kowska M, Myslajek RW, Nowak S, Jêdrzejewska B (2005) Habitat variables associated with wolf (Canis lupus) distribution and abundance in northern Poland. Divers Distrib 10:225–233

    Article  Google Scholar 

  • Johansson Ö, Rauset GR, Samelius G, McCarthy T, Andrén H, Tumursukh L, Mishra C (2016) Land sharing is essential for snow leopard conservation. Biol Conserv 203:1–7

    Article  Google Scholar 

  • Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71

    Article  Google Scholar 

  • Kaartinen S, Luoto M, Kojola I (2010) Selection of den sites by wolves in boreal forests in Finland. J Zool 281:99–104

    Article  Google Scholar 

  • Kleiven J, Bjerke T, Kaltenborn B (2004) Factors influencing the social acceptability of large carnivore behaviours. Biodivers Conserv 13:1647–1658

    Article  Google Scholar 

  • Laliberte AS, Ripple WJ (2004) Range contractions of North American carnivores and ungulates. Bioscience 54:123–138

    Article  Google Scholar 

  • Lázaro A (2014) Ecología trófica del lobo (Canis lupus) en un ambiente humanizado y multipresa: Variación geográfica. MSc thesis. University of Córdoba, Spain

  • Lesmerises F, Dussault C, St-Laurent MH (2012) Wolf habitat selection is shaped by human activities in a highly managed boreal forest. For Ecol Manage 276:125–131

    Article  Google Scholar 

  • Llaneza L, López-Bao JV (2015) Indirect effects of changes in environmental and agricultural policies on the diet of wolves. Eur J Wildl Res 61:895–902

    Article  Google Scholar 

  • Llaneza L, Fernández A, Nores C (1996) Dieta del lobo en dos zonas de Asturias (España) que difieren en carga ganadera. Doñana Acta Vertebrata 23:201–213

    Google Scholar 

  • Llaneza L, Palacios V, Uzal A, Ordiz A, Sazatornil V, Sierra P, Álvares F (2005) Distribución y aspectos poblacionales del lobo ibérico (Canis lupus signatus) en las provincias de Pontevedra y A Coruña. Galemys 17:61–80

    Google Scholar 

  • Llaneza L, López-Bao JV, Sazatornil V (2012) Insights into wolf presence in human-dominated landscapes: the relative role of food availability, humans and landscape attributes. Divers Distrib 18:459–469

    Article  Google Scholar 

  • Llaneza L, García EJ, López-Bao JV (2014) Intensity of territorial marking predicts wolf reproduction: implications for wolf monitoring. PLoS ONE 9:e93015

    Article  PubMed  PubMed Central  Google Scholar 

  • Llaneza L, García EJ, Palacios V, López-Bao JV (2015) Wolf monitoring in Galicia, 2013–2014. Report to the Spanish Ministry of Agriculture, Food and Environment, Spain

  • Llaneza L, García EJ, Palacios V, Sazatornil V, López-Bao JV (2016) Resting in risky environments: the importance of cover for wolves to cope with exposure risk in human-dominated landscapes. Biodivers Conserv 25:1515–1528

    Article  Google Scholar 

  • López-Bao JV, Sazatornil V, Llaneza L, Rodríguez A (2013) Indirect effects on heathland conservation and wolf persistence of contradictory policies that threaten traditional free-ranging horse husbandry. Conserv Lett 6:448–455

    Article  Google Scholar 

  • López-Bao JV, Kaczensky P, Linnell JDC, Boitani L, Chapron G (2015) Carnivore coexistence: wilderness not required. Science 348:871–872

    Article  PubMed  Google Scholar 

  • López-Bao JV, Bruskotter J, Chapron G (2017) What place for large carnivores? Nat Ecol Evol 1:140

    Article  PubMed  Google Scholar 

  • Mac Nally R, Horrocks G (2002) Relative influences of patch, landscape and historical factors on birds in an Australian fragmented landscape. J Biogeogr 29:395–410

    Article  Google Scholar 

  • Mech LD, Boitani L (eds) (2003) Wolves: behaviour, ecology, and conservation. University of Chicago Press, Chicago

    Google Scholar 

  • Mech SG, Hallett JG (2001) Evaluating the effectiveness of corridors: a genetic approach. Conserv Biol 15:467–474

    Article  Google Scholar 

  • Meriggi A, Lovari S (1996) A review of wolf predation in southern Europe: does the wolf prefer wild prey to livestock? J Appl Ecol 33:1561–1571

    Article  Google Scholar 

  • Newsome TM et al (2016) Food habits of the world’s grey wolves. Mammal Rev 46:255–269

    Article  Google Scholar 

  • Norris DR, Theberge MT, Theberge JB (2002) Forest composition around wolf (Canis lupus) dens in eastern Algonquin Provincial Park, Ontario. Can J Zool 80:866–872

    Article  Google Scholar 

  • Noss RF, Quigley HB, Hornocker MG, Merrill T, Paquet PC (1996) Conservation biology and carnivore conservation in the Rocky Mountains. Conserv Biol 10:949–963

    Article  Google Scholar 

  • Oriol-Cotterill A, Valeix M, Frank LG, Riginos C, Macdonald DW (2015) Landscapes of coexistence for terrestrial carnivores: the ecological consequences of being downgraded from ultimate to penultimate predator by humans. Oikos 124:1263–1273

    Article  Google Scholar 

  • Palacios V, López-Bao JV, Llaneza L, Fernández C, Font E, Higgs DM (2016) Decoding group vocalizations: the acoustic energy distribution of chorus howls is useful to determine wolf reproduction. PLoS ONE 11:e0153858

    Article  PubMed  PubMed Central  Google Scholar 

  • Person DK, Russell AL (2009) Reproduction and den site selection by wolves in a disturbed landscape. Northwest Sci 83:211–224

    Article  Google Scholar 

  • Prugh LR, Hodges KE, Sinclair ARE, Brashares JS (2008) Effect of habitat area and isolation on fragmented animal populations. PNAS 105:20770–20775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Rettie WJ, Messier F (2000) Hierarchical habitat selection by woodland caribou: its relationship to limiting factors. Ecography 23:466–478

    Article  Google Scholar 

  • Ripple WJ et al (2016) Saving the world’s terrestrial megafauna. Bioscience 66:807–812

    Article  PubMed  PubMed Central  Google Scholar 

  • Santini L, Di Marco M, Boitani L, Maiorano L, Rondinini C (2014) Incorporating spatial population structure in gap analysis reveals inequitable assessments of species protection. Divers Distrib 20:698–707

    Article  Google Scholar 

  • Santini L, Boitani L, Maiorano L, Rondinini C (2016) Effectiveness of protected areas in conserving large carnivores in Europe. Protected areas. Wiley, Hoboken, pp 122–133

    Google Scholar 

  • Sazatornil V et al (2016) The role of human-related risk in breeding site selection by wolves. Biol Conserv 201:103–110

    Article  Google Scholar 

  • Soga M, Koike S (2013) Mapping the potential extinction debt of butterflies in a modern city: implications for conservation priorities in urban landscapes. Anim Conserv 16:1–11

    Article  Google Scholar 

  • Theuerkauf J, Rouys S, Jêdrzejewski W (2003a) Selection of den, rendezvous, and resting sites by wolves in the Bialowieza Forest, Poland. Can J Zool 81:163–167

    Article  Google Scholar 

  • Theuerkauf J, Jędrzejewski W, Schmidt K, Gula R (2003b) Spatiotemporal segregation of wolves from humans in the Białowieża Forest (Poland). J Wildl Manag 67:706–716

    Article  Google Scholar 

  • Thornton D et al (2016) Assessing the umbrella value of a range-wide conservation network for jaguars (Panthera onca). Ecol Appl 26:1112–1124

    Article  PubMed  Google Scholar 

  • Tischendorf L, Fahrig L (2000) How should we measure landscape connectivity? Landsc Ecol 15:633–641

    Article  Google Scholar 

  • Treves A, Bruskotter J (2014) Tolerance for predatory wildlife. Science 344:475–476

    Article  Google Scholar 

  • Walsh C, Mac Nally R (2008) Hier.part: hierarchical partitioning. R package version 1.0.3. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • White S, Briers RA, Bouyer Y, Odden J, Linnell JDC (2015) Eurasian lynx natal den site and maternal home-range selection in multi-use landscapes of Norway. J Zool 297:87–98

    Article  Google Scholar 

  • Wikramanayake ED, Dinerstein E, Robinson JG, Karanth U, Rabinowitz A, Olson D, Mathew T, Hedao P, Conner M, Hemley T, Bolze D (1998) An ecology based method for defining priorities for large mammal conservation: the tiger as case study. Conserv Biol 12:865–878

    Article  Google Scholar 

  • Wikramanayake E, McKnight M, Dinerstein E, Joshi A, Gurung B, Smith D (2004) Designing a conservation landscape for tigers in human-dominated environments. Conserv Biol 18:839–844

    Article  Google Scholar 

  • Woodroffe R (2000) Predators and people, using human densities to interpret declines of large carnivores. Anim Conserv 3:165–173

    Article  Google Scholar 

  • Woodroffe R, Ginsberg JR (1998) Edge effects and the extinction of populations inside protected areas. Science 280:2126–2128

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are in debt to the staff of the Regional Government of Galicia (Belén Bris, Rogelio Fernández, Carmen Juliani, Mercedes Robles, Emilio Rosa, Jesús Santamarina, Javier Turrillo). Spatial information from wolves in the study area comes from research projects funded by DESA S.L. and GAMESA S.L. We thank Enrique Anchústegui (DESA) and Aitziber Céspedes (GAMESA) for their collaboration and support. J.V.L.B. was supported by a Ramon & Cajal research contract (RYC-2015-18932) from the Spanish Ministry of Economy, Industry and Competitiveness. This is scientific paper no. 19 from the Iberian Wolf Research Team (IWRT).

Author information

Authors and Affiliations

  1. A.RE.NA. Asesores en Recursos Naturales, S.L, 27003, Lugo, Spain

    Luis Llaneza

  2. Departamento de Bioloxía Celular e Ecoloxía, Universidad de Santiago de Compostela, 15782, Santiago de Compostela, Spain

    Luis Llaneza

  3. Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, 08028, Barcelona, Spain

    Víctor Sazatornil

  4. Research Unit of Biodiversity (UO/CSIC/PA), Oviedo University, 33600, Mieres, Spain

    José Vicente López-Bao

Authors
  1. Luis Llaneza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Víctor Sazatornil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Vicente López-Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José Vicente López-Bao.

Additional information

Communicated by Kirsty Park.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 40 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Llaneza, L., Sazatornil, V. & López-Bao, J.V. The importance of fine-scale breeding site selection patterns under a landscape-sharing approach for wolf conservation. Biodivers Conserv 27, 1239–1256 (2018). https://doi.org/10.1007/s10531-017-1491-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-017-1491-9

Keywords

Search

Navigation