Abstract
Protected areas are often designed with conservation focus on rare species. However, provision of essential areas for other species is crucial for maintenance of overall biodiversity. The brown bear (Ursus arctos), throughout most of its present distribution area, helps to maintain diverse ecosystems through trophic effects. As with other hibernating mammals, undisturbed wintering areas are a highly important resource for bears. In lowland areas containing intensively managed forests, undisturbed winter dens might largely be confined to protected areas. Here, we assess the importance of protected areas for bear winter denning in a forested landscape. We employed maximum entropy modelling and data of 80 bear winter den locations in a 39,000 km2 area of mainland Estonia to evaluate areas suitable for winter denning. We compared the amount of highly suitable wintering areas (suitability index > 0.6) in 22 protected areas with two ring buffers around these areas to assess the relative importance of adjoining areas for bear wintering. The proportion of highly suitable wintering area was significantly lower in protected areas than in nearby ring buffers. Therefore, our results demonstrate that protected areas do not provide much conservation support for denning brown bears, and we recommend focussing attention on managed forests to meet conservation objectives. The results reveal the importance of larger forest areas for brown bear wintering in lowland to avoid constant disturbance.
Similar content being viewed by others
References
Albrecht J, Bartoń KA, Selva N, Sommer RS, Swenson JE, Bischof R (2017) Humans and climate change drove the Holocene decline of the brown bear. Sci Reports7:10399. https://doi.org/10.1038/s41598-017-10772-6
Baldwin RA (2009) Use of maximum entropy modelling in wildlife research. Entropy 11:854–866. https://doi.org/10.3390/e11040854
Boitani L, Alvarez F, Anders O, Andren H, Avanzinelli E, Balys V, Blanco JC, Breitenmoser U, Chapron G, Ciucci P, Dutsov A, Groff C, Huber D, Ionescu O, Knauer F, Kojola I, Kubala J, Kutal M, Linnell J, Majic A, Mannil P, Manz R, Marucco F, Melovski D, Molinari A, Norberg H, Nowak S, Ozolins J, Palazon S, Potocnik H, Quenette P-Y, Reinhardt I, Rigg R, Selva N, Sergiel A, Shkvyria M, Swenson J, Trajce A, Von Arx M, Wolfl M, Wotschikowsky U, Zlatanova D (2015) Key actions for large carnivore populations in Europe. Institute of Applied Ecology (Rome, Italy). Report to DG Environment, European Commission, Bruxelles. Contract no. 07.0307/2013/654446/SER/B3
Bojarska K, Selva N (2012) Spatial patterns in brown bear Ursus arctos diet: the role of geographical and environmental factors. Mammal Rev 42:120–143. https://doi.org/10.1111/j.1365-2907.2011.00192.x
Boyles JG, Brack V Jr (2009) Modeling survival rates of hibernating mammals with individual-based models of energy expenditure. J Mammal 90:9–16. https://doi.org/10.1644/08-MAMM-A-205.1
Ciarniello LM, Boyce MS, Heard HD, Seip DP (2005) Denning behaviour and den site selection of grizzly bears along the Parsnip River, British Columbia, Canada. Ursus 16:47–58
Ciarniello LM, Heard DC, Seip DR (2014) Grizzly bear behaviour in forested, clearcut and non-forested areas in sub-boreal British Columbia. Can Wildl Biol Manag 3:82–92
Davison J, Ho SYW, Bray SC, Korsten M, Tammeleht E, Hindrikson M, Østbye K, Østbye E, Lauritzen S-E, Austin J, Cooper A, Saarma U (2011) Late-Quaternary biogeographic scenarios for the brown bear (Ursus arctos), a wild mammal model species. Quat Sci Rev 30:418–430
Delgado MM, Tikhonov G, Meyke E, Babushkin M, Bespalova T, Bondarchuk S, Esengeldenova A, Fedchenko I, Kalinkin Y, Knorre A, Kosenkov G, Kozsheechkin V, Kuznetsov A, Larin E, Mirsaitov D, Prokosheva I, Rozhkov Y, Rykov A, Seryodkin IV, Shubin S, Sibgatullin R, Sikkila N, Sitnikova E, Sultangareeva L, Vasin A, Yarushina L, Kurhinen J, Penteriani V (2018) The seasonal sensitivity of brown bear denning phenology in response to climatic variability. Front Zool 15:41. https://doi.org/10.1186/s12983-018-0286-5
QGIS Development Team (2016) QGIS geographic information system. Open Source Geospatial Foundation. URL http://qgis.osgeo.org
Diserens TA, Borowik T, Nowak S, Szewczyk M, Niedźwiecka N, Mysƚajek RW (2017) Deficiencies in Natura 2000 for protecting recovering large carnivores: a spotlight on the wolf Canis lupus in Poland. PLoS One 12:e0184144. https://doi.org/10.1371/journal.pone.0184144
Durant SM, Mitchell N, Groom R, Pettorelli N, Ipavec A, Jacobson AP, Woodroffe R, Böhm M, Hunter LTB, Becker MS, Broekhuis F, Bashir S, Andresen L, Aschenborn O, Beddiaf M, Belbachir F, Belbachir-Bazi A, Berbash A, Brandao de Matos Machado I, Breitenmoser C, Chege M, Cilliers D, Davies-Mostert H, Dickman AJ, Ezekiel F, Farhadinia MS, Funston P, Henschel P, Horgan J, de Iongh HH, Jowkar H, Klein R, Lindsey PA, Marker L, Marnewick K, Melzheimer J, Merkle J, M’soka J, Msuha M, O’Neill H, Parker M, Purchase G, Sahailou S, Saidu Y, Samna A, Schmidt-Küntzel A, Selebatso E, Sogbohossou EA, Soultan A, Stone E, van der Meer E, van Vuuren R, Wykstra M, Young-Overton K (2017) The global decline of cheetah Acinonyx jubatus and what it means for conservation. PNAS 114:528–533. https://doi.org/10.1073/pnas.1611122114
Elfström M, Swenson JE (2009) Effects of sex and age on den site use by Scandinavian brown bears. Ursus 20:85–93
Elfström M, Swenson JE, Ball JP (2008) Selection of denning habitats by Scandinavian brown bears Ursus arctos. Wildl Biol 14:176–187. https://doi.org/10.2981/0909-6396(2008)14[176:SODHBS]2.0.CO;2
Eriksen A, Wabakken P, Maartmann E, Zimmermann B (2018) Den site selection by male brown bears at the population’s expansion front. PLoS One 13:e0202653. https://doi.org/10.1371/journal.pone.0202653
Estes JA, Tinker MT, Williams TM, Doak DF (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473–476
Evans AL, Sahlén V, Støen O-G, Fahlman Å, Brunberg S, Madslien K, Fröbert O, Swenson JE, Arnemo JM (2012) Capture, anesthesia, and disturbance of free-ranging brown bears (Ursus arctos) during hibernation. PLoS One 7:e40520. https://doi.org/10.1371/journal.pone.0040520
Fernández N, Selva N, Yuste CS, Okarma H, Jakubiec Z (2012) Brown bears at the edge: modeling habitat constrains at the periphery of the Carpathian population. Biol Conserv 153:134–142. https://doi.org/10.1016/j.biocon.2012.04.013
Frank SC, Steyaert SMJG, Swenson JE, Stroch I, Kindberg J, Barck H, Zedrosser A (2015) A “clearcut” case? Brown bear selection of coarse woody debris and carpenter ants on clearcuts. Forest Ecol Managem 348:164–173. https://doi.org/10.1016/j.foreco.2015.03.051
García P, Lastra J, Marquínez J, Nores C (2007) Detailed model of shelter areas for the Cantabrian brown bear. Ecol Inform 2:297–307. https://doi.org/10.1016/j.ecoinf.2007.08.003
Gilroy JJ, Ordiz A, Bischof R (2015) Carnivore coexistence: value the wilderness. Science 347:382. https://doi.org/10.1126/science.347.6220.382-a
Gompper ME, Belant JL, Kays R (2015) Carnivore coexistence: America’s recovery. Science 347:382–383. https://doi.org/10.1126/science.347.6220.382-b
Güthlin D, Knauer F, Kneib T, Küchenhoff H, Kaczensky P, Rauer G, Jonozovič M, Mustoni A, Jerina K (2011) Estimating habitat suitability and potential population size for brown bears in the Eastern Alps. Biol Conserv 144:1733–1741. https://doi.org/10.1016/j.biocon.2011.03.010
Hagen SB, Kopatz A, Aspi J, Kojola I, Eiken HG (2015) Evidence of rapid change in genetic structure and diversity during range expansion in a recovering large terrestrial carnivore. Proc R Soc B 282:20150092. https://doi.org/10.1098/rspb.2015.0092
Hindrikson M, Remm J, Pilot M, Godinho R, Stronen AV, Baltrūnaité L, Czarnomska SD, Leonard JA, Randi E, Nowak C, Åkesson M, López-Bao JV, Álvares F, Llaneza L, Echegaray J, Vilá C, Ozolins J, Rungis D, Aspi J, Paule L, Skrbinšek T, Saarma U (2017) Wolf population genetics in Europe: a systematic review, meta-analysis and suggestions for conservation and management. Biol Rev 92:1601–1629. https://doi.org/10.1111/brv.12298
Hodder DP, Johnson CJ, Rea RV, Zedrosser A (2014) Application of a species distribution model to identify and manage bear den habitat in Central British Columbia, Canada. Wildl Biol 20:238–245. https://doi.org/10.2981/wlb.00037
Johnson HE, Lewis DL, Verzuh TL, Wallace CF, Much RM, Willmarth LK, Breck SW (2017) Human development and climate affect hibernation in a large carnivore with implications for human-carnivore conflicts. J Appl Ecol 55:663–672. https://doi.org/10.1111/1365-2664.13021
Jung M (2016) LecoS — a python plugin for automated landscape ecology analysis. Ecol Inform 31:18–21. https://doi.org/10.1016/j.ecoinf.2015.11.006
Kaal M (1980) Pruunkaru. Tallinn, Valgus
Kaczensky P, Chapron G, von Arx M, Huber D, Andrén H, Linnell J (2013) Status, management and distribution of large carnivores – bear, lynx, wolf & wolverine – in Europe. Part 1 – Europe summaries. Report: 1-72. A large carnivore initiative for Europe report prepared for the European Commission
Kharuk VI, Im ST, Petrov IA, Golyukov AS, Ranson KJ, Yagunov MN (2017) Climate-induced mortality of Siberian pine and fir in the Lake Baikal Watershed, Siberia. Forest Ecol Manag 384:191–199
Kolenosky GB, Strathearn SM (1987) Winter denning of black bears in east-central Ontario. Int Conf Bear Res and Manag 7:305–316
Kuraś PK, Alila Y, Weiler M (2012) Forest harvesting effects on the magnitude and frequency of peak flows can increase with return period. Water Resour Res 48:W01544. https://doi.org/10.1029/2011WR010705
Libal NS, Belant JL, Leopold BD, Wang G, Owen PA (2011) Despotism and risk of infanticide influence grizzly bear den-site selection. PLoS One 6:e24133. https://doi.org/10.1371/journal.pone.0024133
Libal NS, Belant JL, Maraj R, Leopold BD, Wang G, Marshall S (2012) Microscale den-site selection of grizzly bears in southwestern Yukon. Ursus 23:226–230. https://doi.org/10.2192/URSUS-D-12-00002.1
Linnell JDC, Swenson JE, Andresen R, Barnes B (2000) How vulnerable are denning bears to disturbance? Wildl Soc Bull 28:400–413
Lõhmus A (2016) Eesti rangelt kaitstavate metsade tüpoloogiline analüüs. https://www.envir.ee/sites/default/files/metsade_range_kaitse_2016_alohmus.pdf
Loskutov AV, Pavlov MP, Puchkovskiy SV (1993) Brown bear: the Volga-Kama region. In: Vaisfeld MA, Chestin IE (eds) Bears: brown bear, polar bear, Asian black bear. Nauka, Moscow, pp 91–135
Luvsamjamba A, Reynolds H, Yansanjav A, Tserenbataa T, Amgalan B, Tumendemberel O (2016) Review of Gobi bear research (Ursus arctos gobiensis, Sokolov and Orlov, 1992). Arid Ecosyst 6:206–212. https://doi.org/10.1134/S2079096116030021
Malanson GP, Heumann BW (2016) Models and data in biogeography and landscape ecology. In: Clifford N, Cope M, Gillespie T, French S (eds) Key methods in geography, 3rd edn. SAGE Publications, Thousand Oaks
Marcinkowski P, Piniewski M, Kardel I, Szcześniak M, Benestad R, Srinivasan R, Ignar S, Okruszko (2017) Effect of climate change on hydrology, sediment and nutrient losses in two lowland catchments in Poland. Water 9:156. https://doi.org/10.3390/w9030156
Martin J, Revilla E, Quenette P-Y, Naves J, Dominique A, Swenson JE (2012) Brown bear habitat suitability in the Pyrenees: transferability across sites and linking scales to make the most of scarce data. J Appl Ecol 49:621–631. https://doi.org/10.1111/j.1365-2664.2012.02139.x
Mateo-Tomás P, Olea PP, Moleón M, Selva N, Sánchez-Zapata JA (2017) Both rare and common species support ecosystem services in scavenger communities. Glob Ecol Biogeogr 26:1459–1470. https://doi.org/10.1111/geb.12673
McLellan BN, Proctor MF, Huber D, Michel S (2017) Ursus arctos (amended version of 2017 assessment). The IUCN red list of threatened species 2017: e.T41688A121229971. 10.2305/IUCN.UK.2017-3.RLTS.T41688A121229971.en
McLoughlin PD, Case RL, Gau RJ, Cluff DH, Mulders R, Messier F (2002) Hierarchical habitat selection by barren-ground grizzly bears in the central Canadian Arctic. Oecol 132:102–108. https://doi.org/10.1007/s00442-002-0941-5
Milanesi P, Breiner FT, Puopolo F, Holderegger R (2017) European human-dominated landscapes provide space for the recolonization of large carnivore populations under future land change scenarios. Ecography 40:1359–1368. https://doi.org/10.1111/ecog.02223
Moe TF, Kindberg J, Jansson I, Swenson JE (2007) Importance of diel behaviour when studying habitat selection: examples from female Scandinavian brown bears (Ursus arctos). Can J Zool 85:518–525. https://doi.org/10.1139/Z07-034
Moskvitina NS, Tyutenkov OY, Shpansky AV, Pugachyova AV, Kurbatsky DV (2017) The history and modern condition of the brown bear (Ursus arctos L., 1758) of the West Siberian plain. Int J Environ Stud 74:891–902. https://doi.org/10.1080/00207233.2017.1294417
Mueller T, Selva N, Pugacewicz E, Prins E (2009) Scale-sensitive landscape complementation determines habitat suitability for a territorial generalist. Ecography 32:345–353. https://doi.org/10.1111/j.1600-0587.2008.05694.x
Ordiz A, Støen OG, Delibes M, Swenson JE (2011) Predators or prey? Spatio-temporal discrimination of human-derived risk by brown bears. Oecol 166:59–67. https://doi.org/10.1007/s00442-011-1920-5
Pazhetnov VS (1993) Brown bear: the centre of European Russia. In: Vaisfeld MA, Chestin IE (eds) Bears: brown bear, polar bear, Asian black bear. Nauka, Moscow, pp 51–60
Petram W, Knauer F, Kaczensky P (2004) Human influence on the choice of winter dens by European brown bears in Slovenia. Biol Conserv 119(1):129–136
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Phillips SJ, Anderson RP, Dudík M, Schapire RE, Blair ME (2017) Opening the black box: an open-source release of Maxent. Ecography 40:887–893. https://doi.org/10.1111/ecog.03049
Pigeon KE, Nielsen SE, Stenhouse GB, Côté SD (2014) Den selection by grizzly bears on a managed landscape. J Mammal 95:559–571. https://doi.org/10.1644/13-MAMM-A-137
Pop MI, Iosif R, Miu IV, Rozylowicz L, Popescu VD (2018) Combining resource selection functions and home-range data to identify habitat conservation priorities for brown bears. Anim Conserv 21:352–362. https://doi.org/10.1111/acv.12399
Raudsaar M, Sims A, Timmusk T, Pärt E, Nikopensius M (2017) Forest resources. In Raudsaar M, Siimon K-L, Valgepea M (eds) Yearbook Forest 2016, Estonian Environment Agency, pp. 18-81
Raukas A, Teedumäe A (1997) Geology and mineral resources of Estonia. Estonian Academy Publishers, Tallinn
Richmond-Coggan L (2014) Comparative abundance and ranging behaviour of brown hyaena (Parahyaena brunnea) inside and outside protected areas in South Africa. Ph.D. Thesis. Nottingham Trent University, Nottingham, UK
Ripple WJ, Beschta RL (2007) Hardwood tree decline following large carnivore loss on the Great Plains, USA. Front Ecol Environ 5:241–246. https://doi.org/10.1890/1540-9295(2007)5[241:HTDFLC]2.0.CO;2
Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach AD, Wirsing AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484. https://doi.org/10.1126/science.1241484
Sahlén E, Støen O-G, Swenson JE (2011) Brown bear den site concealment in relation to human activity in Sweden. Ursus 22:152-158. https://doi.org/10.2192/URSUS-D-10-00007.1
Santini L, Boitani L, Maiorano L, Rondinini C (2016) Effectiveness of protected areas in conserving large carnivores in Europe. In: Joppa L, Baillie J, Robinson J (eds) Protected areas: are they safeguarding biodiversity? 1st edn. Wiley, Hoboken
Saupe EE, Barve V, Myers CE, Soberón J, Barve N, Hensz CM, Peterson AT, Owens HL, Lira-Noreiga A (2012) Variation in niche and distribution model performance: the need for a priori assessment of key causal factors. Ecol Model 237-238:11–22. https://doi.org/10.1016/j.ecolmodel.2012.04.001
Scharf AK, Fernández N (2018) Up-scaling local-habitat models for large-scale conservation: Assessing suitable areas for the brown bear comeback in Europe. Divers Distrib 24(11):1573–1582
Shubin NG (1993) Brown bear: the Western Siberia. In: Vaisfeld MA, Chestin IE (eds) Bears: brown bear, polar bear, Asian black bear. Nauka, Moscow, pp 206–214
Smerdon BD, Redding TE, Beckers J (2009) An overview of the effects of forest management on groundwater hydrology. BC J Ecosyst Manag 10:22–44
Sobanskiy GG, Zavatzkiy BP (1993) Brown bear: the Altai and Sayans. In: Vaisfeld MA, Chestin IE (eds) Bears: brown bear, polar bear, Asian black bear. Moscow, Nauka, pp 214–249
Sokolov VA, Vtyurina OP, Sokolova NV, Lapin EA (2017) Forecast for the dynamics of forests in Krasnoyarsk Krai. Sib J Forest Sci 4:91–100
StatSoft Inc. (2005) STATISTICA (data analysis software system), version 7.1. www.statsoft.com
Swenson JE, Sandegren F, Brunberg S, Wabakken P (1997) Winter den abandonment by brown bears Ursus arctos: causes and consequences. Wildl Biol 3:35–38
Tammeleht E, Kuuspu M (2018) Effect of competition and landscape characteristics on mesocarnivore cohabitation in badger setts. J Zool 305:8–16. https://doi.org/10.1111/jzo.12529
Tammeleht E, Remm J, Korsten M, Davison J, Tumanov I, Saveljev A, Männil P, Kojola I, Saarma U (2010) Genetic structure in large, continuous mammal populations: the example of the brown bears in northwestern Eurasia. Mol Ecol 19:5359–5370. https://doi.org/10.1111/j.1365-294X.2010.04885.x
Thodsen H, Baarup-Pedersen A, Andersen HE, Jensen KMB, Andersen PM, Bolding K, Ovesen N (2016) Climate change effects on lowland stream flood regimes and riparian rich fen vegetation communities in Denmark. Hydrol Sci J 61:344–358. https://doi.org/10.1080/02626667.2014.990965
Vaisfeld MA (1993) Brown bear: the north-east of European Russia. In: Vaisfeld MA, Chestin IE (eds) Bears: brown bear, polar bear, Asian black bear. Nauka, Moscow, pp 37–51
Valgepea M, Sims A, Raudsaar M (2017) Fellings. In Raudsaar M, Siimon K-L, Valgepea M (eds) Yearbook Forest 2016, Estonian Environment Agency, pp. 106-137
van Gils H, Westinga E, Carafa M, Antonucci A, Ciaschetti G (2014) Where the bears roam in Majella National Park, Italy. J Nat Conserv 22:23–34. https://doi.org/10.1016/j.jnc.2013.08.001
Vulla E, Hobson KA, Korsten M, Leht M, Marin A-J, Lind A, Männil P, Valdmann H, Saarma U (2009) Carnivory is positively correlated with latitude among omnivorous mammals: evidence from brown bears, badgers and pine martens. Ann Zool Fenn 46:395–415. https://doi.org/10.5735/086.046.0601
Whiteman A, Passoni G, Rowcliffe JM, Ugarković D, Kusak J, Reljić S, Huber D (2017) Identifying key denning habitat to conserve brown bear (Ursus arctos) in Croatia. Wildl Res 44:309–315. https://doi.org/10.1071/WR16164
Wolf C, Ripple WJ (2017) Range contractions of the world’s large carnivores. R Soc Open Sci 4:170052. https://doi.org/10.1098/rsos.170052
Yudin VG (1993) Brown bear: the south of the far east. In: Vaisfeld MA, Chestin IE (eds) Bears: brown bear, polar bear, Asian black bear. Nauka, Moscow, pp 348–380
Маrtynyuk АА, Sidorenkov VM, Doroshchenkova EV, Sidorenkova ЕМ, Zakharov YG (2016) Zoning of the Russian Federation territory based on forest management and forest use intensity. Sib J For Sci 3:3–12
Acknowledgements
We would like to thank Peep Männil from the Department of Game Monitoring, Estonian Environmental Agency, Ahto Täpsi and Vahur Sepp, for kindly sharing the data on brown bear wintering sites and Riinu Rannap, Ann Kraut, John Davison, Urmas Saarma, Marju Keis and Peeter Anijalg and anonymous reviewers for their generous help and comments on earlier versions of the manuscript.
Funding
The study was funded by European Union through the European Regional Development Fund by the program 3.2.0802.11-0043 and the Estonian Ministry of Education and Research by institutional research funding (IUT-2032).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Jan M. Wójcik
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Tammeleht, E., Kull, A. & Pärna, K. Assessing the importance of protected areas in human-dominated lowland for brown bear (Ursus arctos) winter denning. Mamm Res 65, 105–115 (2020). https://doi.org/10.1007/s13364-019-00447-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13364-019-00447-0