Abstract
Urban forests are often modified and fragmented by human land use and the original habitat might exist only in remnant patches. Due to their specific habitat requirements and unwillingness to move through matrix many forest-dwelling mammals are susceptible to changes in landscape structure. It is important to understand how the availability of suitable habitat and landscape fragmentation affect species distributions, and what landscape characteristics are essential to the persistence of a given species to conserve urban wildlife. We investigated the effect of landscape composition and configuration on the occurrence of the Siberian flying squirrel, a small-sized arboreal rodent, in a partly urbanized area of Eastern Finland. All suitable and potential forest patches were searched to determine the presence or absence of species, and the landscape characteristics of occupied sites were compared to those of unoccupied sites. Flying squirrels occurred both at the edges of large suitable forested areas, but also in small forest fragments within residential areas. Surprisingly, urban areas did not have a negative effect on the flying squirrel occurrence. Occurrence probability was not either associated with the proportion of suitable habitat, but occupied sites contained larger amount of movement habitat and had shorter distances to nearest occupied sites than unoccupied sites. Our results show that flying squirrels can exist in urbanized landscape and near residential areas, but more detailed information on habitat use and survival is still needed to determine the long-term persistence and viability of the urban populations.
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References
Ahti T, Hämet-Ahti L, Jalas J (1968) Vegetation zones and their sections in northwestern Europe. Ann Bot Fenn 5:169–211
Andrén H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat - a review. Oikos 71:340–346
Andrén H, Delin A, Seiler A (1997) Population response to landscape changes depends on specialization to different landscape elements. Oikos 80:193–196
Anonymous (1992) Council Directive 92/43/EEC
Bakker VJ, Van Vuren DH (2004) Gap-crossing decisions by the red squirrel, a forest-dependent small mammal. Conserv Biol 18:689–697
Bender D, Contreras T, Fahrig L (1998) Habitat loss and population decline: a meta-analysis of the patch size effect. Ecology 18:689–697
Brearley G, Bradley A, Bell S, McAlpine C (2010) Influence of contrasting urban edges on the abundance of arboreal mammals: A study of squirrel gliders (Petaurus norfolcensis) in southeast Queensland, Australia. Biol Conserv 143:60–71
Brearley G, Bradley A, Bell S, McAlpine C (2011) Change in habitat resources and structure near urban edges and its influence on the squirrel glider (Petaurus norfolcensis) in southeast Queensland, Australia. Austral Ecol 36:425–432
Breuste J, Feldmann H, Uhlmann O (1998) Urban Ecology. Springer, Berlin
Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information–theoretic approach. Springer, New York
Byholm P, Burgas D, Virtanen T, Valkama J (2012) Competitive exclusion within the predator community influences the distribution of a threatened prey species. Ecology 93:1802–1808
Caryl F, Thomson K, van der Ree R (2013) Permeability of the urban matrix on arboreal gliding mammals. Austral Ecology 38:609–616
Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9:5–12
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, Schröder B, Schurr FM, Wilson R (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30:609–628
Dunning J, Danielson B, Pulliam H (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175
Fahrig L (1997) Relative effects of habitat loss and fragmentation on population extinction. J Wildl Manage 61:603–610
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515
Fielding A, Bell J (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49
FitzGibbon SI, Putland DA, Goldizen AW (2007) The importance of functional connectivity in the conservation of a ground-dwelling mammal in an urban Australian landscape. Landsc Ecol 22:1513–1525
Forman RTT (1998) Road ecology: a solution to the giant embracing us. Landsc Ecol 13: III–V.
Gilbert OL (1989) The Ecology of urban habitats. Chapman & Hall, London
Gillies C, Clout M (2003) The prey of domestic cats (Felis catus) in two suburbs of Auckland City, New Zealand. J Zool 259:309–315
Grueber CE, Nagakawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711
Haila Y, Kousis M, Jokinen A, Nygren N, Psarikidou K (2007) Building Trust through Public Participation: Learning from Conflicts over the Implementation of the Habitats Directive. PAGANINI Work-package 4. Participatory Governance and Institutional Innovation. http://www.univie.ac.at/LSG/paganini/finals_pdf/WP4_FinalReport.pdf
Hanski IK (1998) Home ranges and habitat use in the declining flying squirrel Pteromys volans in managed forests. Wildl Biol 4:33–46
Hanski IK, Selonen V (2009) Female-biased natal dispersal in the Siberian flying squirrel. Behav Ecol 20:60–67
Hanski IK, Stevens PC, Ihalempiä P, Selonen V (2000) Home-range size, movements, and nest-site use in the Siberian flying squirrel, Pteromys volans. J Mammal 81:798–809
Harper K, Macdonald S, Burton P, Chen J, Brosofske K, Saunders S, Euskirchen E, Roberts D, Jaiteh M, Esseen P (2005) Edge influence on forest structure and composition in fragmented landscapes. Conserv Biol 19:768–782
Hokkanen H, Törmälä T, Vuorinen H (1982) Decline of the flying squirrel Pteromys volans L. populations in Finland. Biol Conserv 23:273–284
Hurme E, Reunanen P, Mönkkönen M, Nikula A, Nivala V, Oksanen J (2007) Local habitat patch pattern of the Siberian flying squirrel in a managed boreal forest landscape. Ecography 30:277–287
Hurme E, Mönkkönen M, Reunanen P, Nivala V (2008) Temporal patch occupancy dynamics of the Siberian flying squirrel in a boreal forest landscape. Ecography 31:469–476
Ims R, Rolstad J, Wegge P (1993) Predicting space use responses to habitat fragmentation - can voles Microtus oeconomus serve as an experimental model system (Ems) for Capercaillie grouse Tetrao urogallus in boreal forest. Biol Conserv 63:261–268
Jokimäki J, Kaisanlahti-Jokimäki M, Suhonen J, Clergeau P, Pautasso M, Fernandez-Juricic E (2011) Merging wildlife community ecology with animal behavioral ecology for a better urban landscape planning. Landsc Urban Plan 4:383–385
Koprowski J (2005) The response of tree squirrels to fragmentation: a review and synthesis. Anim Conserv 8:369–376
Lampila S, Wistbacka R, Mäkelä A, Orell M (2009) Survival and population growth rate of the threatened Siberian flying squirrel (Pteromys volans) in a fragmented forest landscape. Ecoscience 16:66–74
Lang S, Tiede D (2003) vLATE Extension für ArcGIS - vektorbasiertes Tool zur quantitativen Landschaftsstrukturanalyse, ESRI Anwenderkonferenz 2003 Innsbruck. CDROM
Lidicker WZ (1999) Responses of mammals to habitat edges: an overview. Landsc Ecol 14:333–343
Lobo JM, Jiménez-Valverde A, Hortal J (2010) The uncertain nature of absences and their importance in species distribution modelling. Ecography 33:103–114
MacKenzie DI, Royle AJ (2005) Designing occupancy studies: general advice and allocating survey effort. J Appl Ecol 42:1105–1114
MacKenzie DI, Nichols JD, Lachman GB, Droege S, Royle JA, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248–2255
MacKenzie DI, Nichols JD, Hines JE, Knutson MG, Franklin AB (2003) Estimating site occupancy, colonization, and a local extinction when a species is detected imperfectly. Ecology 84:2200–2207
Marzluff J, Ewing K (2001) Restoration of fragmented landscapes for the conservation of birds: A general framework and specific recommendations for urbanizing landscapes. Restor Ecol 9:280–292
McAlpine CA, Rhodes JR, Callaghan JG, Bowen ME, Lunney D, Mitchell DL, Pullar DV, Possingham HP (2006) The importance of forest area and configuration relative to local habitat factors for conserving forest mammals: a case study of koalas in Queensland, Australia. Biol Conserv 132:153–165
Mönkkönen L, Reunanen P, Nikula A, Inkeroinen J, Forsman J (1997) Landscape characteristics associated with the occurrence of the flying squirrel Pteromys volans in old-growth forests of northern Finland. Ecography 20:634–642
Niemelä J (1999) Ecology and urban planning. Biodivers Conserv 8:119–131
Ognev SI (1966) Mammals of the USSR and adjacent countries. Israel Progr Sci Translations, Jerusalem
Parker TS, Nilon CH (2008) Gray squirrel density, habitat suitability, and behavior in urban parks. Urban Ecosyst 11:243–255
Parker TS, Nilon CH (2012) Urban landscape characteristics correlated with the synurbanization of wildlife. Landsc Urban Plan 106:316–325
Pulliam H (1988) Sources, sinks, and population regulation. Am Nat 132:652–661
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rassi P, Hyvärinen E, Juslén A, Mannerkoski I (2010) The 2010 Red list of Finnish species, Helsinki
Rebele F (1994) Urban ecology and special features of urban ecosystems. Global Ecol Biogeogr Lett 4:173–187
Reunanen P, Mönkkönen M, Nikula A (2002a) Habitat requirements of the Siberian flying squirrel in northern Finland: comparing field survey and remote sensing data. Ann Zool Fenn 39:7–20
Reunanen P, Nikula A, Mönkkönen M, Hurme E, Nivala V (2002b) Predicting occupancy for the Siberian flying squirrel in old-growth forest patches. Ecol Appl 12:1188–1198
Rhodes JR, McAlpine CA, Zuur AF, Smith GM, Ieno EN (2009) GLMM applied on the spatial distribution of koalas in a fragmented landscape. In: Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (eds) Mixed effects models and extensions in ecology with R. Springer Verlag, New York, USA, pp 469–492
Ritchie LE, Betts MG, Forbes G, Vernes K (2009) Effects of landscape composition and configuration on northern flying squirrels in forest mosaic. Forest Ecol Manag 257:1920–1929
Santangeli A, Hanski IK, Mäkelä H (2013a) Integrating multi-source forest inventory and animal survey data to assess nationwide distribution and habitat correlates of the Siberian flying squirrel. Biol Conserv 157:31–38
Santangeli A, Wistbacka R, Hanski IK, Laaksonen T (2013b) Ineffective enforced legislation for nature conservation: a case study with Siberian flying squirrel and forestry in a boreal landscape. Biol Conserv 157:237–244
Selonen V, Hanski IK (2003) Movements of the flying squirrel Pteromys volans in corridors and in matrix habitat. Ecography 26:641–651
Selonen V, Hanski IK (2004) Young flying squirrels (Pteromys volans) dispersing in fragmented forests. Behav Ecol 15:564–571
Selonen V, Hanski IK, Stevens P (2001) Space use of the Siberian flying squirrel Pteromys volans in fragmented forest landscapes. Ecography 24:588–600
Skarén U (1978) The occurrence and winter food of Pteromys volans in North Savo. Luonnon Tutkija 82:139–140 (in Finnish)
Smith WP (2007) Ecology of Glaucomys sabrinus: habitat, demography and community relations. J Mammal 88:862–881
Solonen T (2008) Larger broods in the Northern Goshawk Accipiter gentilis near urban areas in southern Finland. Ornis Fenn 85:118–125
Sorace A, Gustin M (2009) Distribution of generalist and specialist predators along urban gradients. Landsc Urban Plan 90:111–118
Taylor L, Woiwod I, Perry J (1978) Density-dependence of spatial behavior and rarity of randomness. J Anim Ecol 47:383–406
Taylor P, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–573
van der Ree R, Bennett A, Gilmore D (2004) Gap-crossing by gliding marsupials: thresholds for use of isolated woodland patches in an agricultural landscape. Biol Conserv 115:241–249
van der Ree R, Cesarini S, Sunnucks P, Moore JL, Taylor A (2010) Large gaps in canopy reduce road crossing by a gliding mammal. Ecol Soc 15:35 http://www.ecologyandsociety.org/vol15/iss4/art35/
Verbeylen G, De Bruyn L, Adriaensen F, Matthysen E (2003) Does matrix resistance influence Red squirrel (Sciurus vulgaris L. 1758) distribution in an urban landscape? Landsc Ecol 18:791–805
Wiens JA (1995) Landscape mosaics and ecological theory. In: Hansson L et al (eds) Mosaic landscape and ecological processes. Chapman and Hall, London, pp 1–26
Wilson DE, Reeder DM (2005) Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14
Acknowledgments
City of Kuopio is acknowledged for providing the forest stand data and facilities during field work. We also thank Pöyry and Suunnittelukeskus consultancies for access and permission to use their data based on flying squirrel fecal pellet surveys made in 2006–2008. We are grateful to Mari Wikholm for taking part to field work. Heidi Björklund, Otso Ovaskainen, Andrea Santangeli and two anonymous reviewers are thanked for the valuable comments which improved the earlier version of the manuscript. This study was funded by Maj and Tor Nessling Foundation (grant numbers 2012476, 2013150 and 2014367), and Research Foundation of the University of Helsinki for SM.
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Mäkeläinen, S., Schrader, M. & Hanski, I.K. Factors explaining the occurrence of the Siberian flying squirrel in urban forest landscape. Urban Ecosyst 18, 223–238 (2015). https://doi.org/10.1007/s11252-014-0381-0
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DOI: https://doi.org/10.1007/s11252-014-0381-0