Long-term snow-track indices of a Finnish native mesopredator declined while those of an invasive one increased.
Nyctereutes procyonoides
Vulpes vulpes
Climate change
Invasive animals
Invasive species
Mesopredators
Snow-tracks
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
31 10 2024
31 10 2024
Historique:
received:
06
03
2024
accepted:
25
10
2024
medline:
31
10
2024
pubmed:
31
10
2024
entrez:
31
10
2024
Statut:
epublish
Résumé
Monitoring both native and invasive species is crucial for understanding their ecological impacts. However, obtaining reliable data can be challenging, especially for elusive species like mesopredators. This study utilized snow-track surveys in Finland (1989-2022) to examine population trends of the invasive raccoon dog and the native red fox. While raccoon dogs are known to reduce activity during cold weather, we demonstrated that accounting for temperature and snowfall allows for effective population trend estimation using snow-track data. Track accumulation decreased in cold and snowy weather more clearly for raccoon dogs than for red foxes. We also found that the track accumulation of the raccoon dog had significantly increased, while those of the red fox population had declined, particularly in southern parts of the country. Notably, raccoon dog snow-track numbers increased in northern regions, suggesting a potential for further range expansion under a warming climate. These findings reveal a concerning shift in Finland's mesopredators abundance due to the invasive species' success and the decline of the native species. Thus, the invasive raccoon dog is likely to have an increasing role in those northern ecosystems where it interacts with the native fauna.
Identifiants
pubmed: 39478129
doi: 10.1038/s41598-024-77777-w
pii: 10.1038/s41598-024-77777-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
26190Subventions
Organisme : Research Council of Finland
ID : 357199 and 357200
Organisme : Research Council of Finland
ID : 357199 and 357200
Informations de copyright
© 2024. The Author(s).
Références
Thompson, W. L., White, G. C. & Gowan, C. Monitoring Vertebrate Populations (Academic Press Inc., 1998).
Santini, G. et al. Population assessment without individual identification using camera-traps: A comparison of four methods. Basic. Appl. Ecol. 61, 68–81 (2022).
doi: 10.1016/j.baae.2022.03.007
Directorate-General for Environment. European Commision - Nature and Biodiversity. Retrieved March 2022, from Invasive Alien Species. https://ec.europa.eu/environment/nature/invasivealien (2022).
Sadlier, L. M. J., Webbon, C. C., Baker, P. J. & Harris, S. Methods of monitoring red foxes Vulpes vulpes and badgers Meles meles: are field signs the answer? Mamm. Rev. 34, 75–98 (2004).
doi: 10.1046/j.0305-1838.2003.00029.x
Podgórski, T. et al. Guidance on estimation of abundance and density of wild carnivore population: methods, challenges, possibilities, EFSA Supporting Publications. https://doi.org/10.2903/sp.efsa.2020.EN- 1947, 17, 11. (2020).
Kauhala, K. & Kowalczyk, R. Invasion of the raccoon dog Nyctereutes procyonoides in Europe: history of colonization, features behind its success, and threats to native fauna. Curr. Zool. 57, 584–598 (2011).
pubmed: 32288758
doi: 10.1093/czoolo/57.5.584
Holopainen, S., Väänänen, V-M., Vehkaoja, M. & Fox, A. Do alien predators pose a particular risk to duck nests in Northern Europe? Results from an artificial nest experiment. Biol. Invasions 23, 3795–3807 (2021).
doi: 10.1007/s10530-021-02608-2
Jaatinen, K., Hermansson, I., Mohring, B., Steele, B. B. & Öst, M. Mitigating impacts of invasive alien predators on an endangered sea duck amidst high native predation pressure. Oecologia 198, 543–552 (2022).
pubmed: 35028754
doi: 10.1007/s00442-021-05101-8
Tuomikoski, E., Selonen, V., Merimaa, K. & Laaksonen, T. Diet of the raccoon dog, an invasive mesopredator, during the breeding season of declining waterbird populations. Glob Ecol. Cons 51, e02917 (2024).
Mustonen, A. M. & Nieminen, P. A review of the physiology of a survival expert of big freeze, deep snow, and an empty stomach: the boreal raccoon dog (Nyctereutes procyonoides). J. Comp. Physiol. B 188, 15–25 (2018).
pubmed: 28674771
doi: 10.1007/s00360-017-1114-5
Melis, C. et al. Raccoon dogs in Norway - Potential expansion rate, distribution area and management implications. NTNUVitenskapsmuseet Rapp Zool. Ser. 3, 1–49 (2007).
Drygala, F., Werner, U. & Zoller, H. Diet composition of the invasive raccoon dog (Nyctereutes procyonoides) and the native red fox (Vulpes vulpes) in north-east Germany. Hystrix 24, 190–194 (2013).
Thompson, I. D., Davidson, I. J., O’Donnell, S. & Brazeau, F. Use of track transects to measure the relative occurrence of some boreal mammals in uncut forest and regeneration stands. Can. J. Zool. 67, 1816–1823 (1989).
doi: 10.1139/z89-258
Kojola, I. et al. Tracks in snow and population size estimation: The wolf Canis lupus in Finland. Wildl. Biol. 20, 279–284 (2014).
doi: 10.2981/wlb.00042
Krauze-Gryz, D., Jackowiak, M., Klich, D., Gryz, J. & Jasińska, K. D. Following urban predators – long-term snow-tracking data reveals changes in their abundance and habitat use. J. Zool. 323, 213–224 (2024).
doi: 10.1111/jzo.13170
Linnell, J. D. C. et al. An evaluation of structured snow-track surveys to monitor Eurasian lynx Lynx lynx populations. Wildl. Biol. 13, 456–466 (2007a).
doi: 10.2981/0909-6396(2007)13[456:AEOSSS]2.0.CO;2
Kurki, S., Nikula, A., Helle, P. & Lindén, H. Abundances of red fox and pine marten in relation to the composition of boreal forest landscapes. J. Anim. Ecol. 67, 874–886 (1998).
pubmed: 26412368
doi: 10.1046/j.1365-2656.1998.6760874.x
Kawaguchi, T., Desrochers, A. & Bastien, H. Snow tracking and trapping harvest as reliable sources for inferring abundance: a 9-year comparison. Northeast Nat. 22, 798–811 (2015).
doi: 10.1656/045.022.0413
Lindén, H., Helle, E., Helle, P. & Wikman, M. Wildlife triangle scheme in Finland. Methods and aims for monitoring wildlife populations. Finn Game Res. 49, 4–11 (1996).
Lindström, E. The role of medium-sized carnivores in the Nordic boreal forest. Finnish Game Res. 46, 53–63 (1989a).
Mustonen, A-M. et al. Application of change-point analysis to determine winter sleep patterns of the raccoon dog (Nyctereutes procyonoides) from body temperature recordings and a multi-faceted dietary and behavioral study of wintering. BMC Ecol. 12, 27 (2012).
pubmed: 23237274
doi: 10.1186/1472-6785-12-27
Selonen, V., Toivonen, P. & Tuomikoski, E. Invasion in cold: weather effects on winter activity of an alien mesopredator at its northern range. Eur. J. Wildl. Res. 70, 74 (2024).
doi: 10.1007/s10344-024-01824-0
Selonen, V., Brommer, J. E., Klangwald, C. & Laaksonen, T. Successful invasion: camera trap distance sampling reveals higher density for invasive raccoon dog compared to native mesopredators. Biol. Invasions 26, 1–10 (2024).
doi: 10.1007/s10530-024-03323-4
Dahl, F., Åhlén, P. A. & Granström, Å. The management of raccoon dogs (Nyctereutes procyonoides) in Scandinavia. Aliens 30, 59–63 (2010).
Turkia, T. et al. Red squirrels decline in abundance in the boreal forests of Finland and NW Russia. Ecography 41, 1370–1379 (2018).
doi: 10.1111/ecog.03093
Lindström, E. R. et al. Disease reveals the predator: sarcoptic mange, red fox predation, and prey populations. Ecology 75, 1042–1049 (1994).
doi: 10.2307/1939428
Kjellander, P. & Nordström, J. Cyclic voles, prey switching in red fox, and roe deer dynamics – a test of the alternative prey hypothesis. Oikos 101, 338–344 (2003).
doi: 10.1034/j.1600-0706.2003.11986.x
Brommer, J. E. et al. The return of the vole cycle in southern Finland refutes the generality of the loss of cycles through ‘climatic forcing’. Global Change Biol. 16, 577–586 (2010).
doi: 10.1111/j.1365-2486.2009.02012.x
Selonen, V. et al. Invasive species control with apex predators: increasing presence of wolves is associated with reduced occurrence of the alien raccoon dog. Biol. Invasions 24, 3461–3474 (2022).
doi: 10.1007/s10530-022-02850-2
Wikenros, C. et al. Fear or food – abundance of red fox in relation to occurrence of lynx and wolf. Sci. Rep. 7, 9059 (2017).
pubmed: 28831079
doi: 10.1038/s41598-017-08927-6
Selås, V. & Vik, J. O. Possible impact of snow depth and ungulate carcasses on red fox (Vulpes vulpes) populations in Norway, 1897–1976. J. Zool. 269, 299–308 (2006).
doi: 10.1111/j.1469-7998.2006.00048.x
Elmhagen, B. et al. Homage to Hersteinsson and Macdonald: climate warming and resource subsidies cause red fox range expansion and Arctic fox decline. Polar Res. 36, supl1 (2017).
doi: 10.1080/17518369.2017.1319109
Panek, M. & Bresiński, W. Red fox Vulpes vulpes density and habitat use in a rural area of western Poland in the end of 1990s, compared with the turn of 1970s. Acta Theriol. 47, 433–442 (2002).
doi: 10.1007/BF03192468
Delcourt, J., Brochier, B., Delvaux, D., Vangeluwe, D. & Poncin, P. Fox Vulpes vulpes population trends in Western Europe during and after the eradication of rabies. Mam Rev. 52, 343–359 (2022).
doi: 10.1111/mam.12289
Krauze-Gryz, D. & Gryz, J. Den-Dwelling Carnivores in Central Poland: Long-Term Trends in Abundance and Productivity. Diversity 15, 1 (2022).
doi: 10.3390/d15010032
Carricondo-Sanchez, D. et al. Spatial and temporal variation in the distribution and abundance of red foxes in the tundra and taiga of northern Sweden. Eur. J. Wildl. Res. 62, 211–218 (2016).
doi: 10.1007/s10344-016-0995-z
Drygala, F. & Zoller, H. Spatial use and interaction of the invasive raccoon dog and the native red fox in Central Europe: competition or coexistence? Eur. J. Wildl. Res. 59, 683–691 (2013).
doi: 10.1007/s10344-013-0722-y
Kauhala, K., Laukkanen, P. & von Rege, I. Summer food composition and food niche overlap of the raccoon dog, red fox and badger in Finland. Ecography 21, 457–463 (1998).
doi: 10.1111/j.1600-0587.1998.tb00436.x
Kowalczyk, R. & Zalewski, A. Adaptation to cold and predation—shelter use by invasive raccoon dogs Nyctereutes procyonoides in Białowieża Primeval Forest (Poland). Eur. J. Wildl. Res. 57, 133–142 (2011).
doi: 10.1007/s10344-010-0406-9
Willebrand, T., Samelius, G., Walton, Z., Odden, M. & Englund, J. Declining survival rates of red foxes Vulpes vulpes during the first outbreak of sarcoptic mange in Sweden. Wildl Biol 2022: e01014 (2022).
Singer, A., Kauhala, K., Holmala, K. & Smith, G. C. Rabies in northeastern Europe: the threat from invasive raccoon dogs. J. Wildl. Dis. 45, 1121–1137 (2009).
pubmed: 19901385
doi: 10.7589/0090-3558-45.4.1121
Kauhala, K. Removal of medium-sized predators and the breeding success of ducks in Finland. Folia Zool. 53, 367–378 (2004).
Kauhala, K. & Auttila, M. Habitat preferences of the native badger and the invasive raccoon dog in southern Finland. Acta Theriol. 55, 231–240 (2010).
doi: 10.4098/j.at.0001-7051.040.2009
Gompper, M. E. et al. A comparison of noninvasive techniques to survey carnivore communities in northeastern North America. Wildl. Soc. Bull. 34, 1142–1151 (2006).
doi: 10.2193/0091-7648(2006)34[1142:ACONTT]2.0.CO;2
Fløjgaard, C., Morueta-Holme, N., Skov, F., Madsen, A. B. & Svenning, J. C. Potential 21st century changes to the mammal fauna of Denmark – implications of climate change, land-use, and invasive species. IOP Conf. Ser: Earth Environ. Sci. 8, 012016 (2009).
doi: 10.1088/1755-1315/8/1/012016
Kauhala, K., Holmala, K. & Schregel, J. Seasonal activity patterns and movements of the raccoon dog, a vector of diseases and parasites, in southern Finland. Mamm. Biol. 72, 342–353 (2007).
doi: 10.1016/j.mambio.2006.10.006
Jasiulionis, M., Stirkė, V. & Balčiauskas, L. The Distribution and Activity of the Invasive Raccoon Dog in Lithuania as Found with Country-Wide Camera Trapping. Forests 14, 1328 (2023).
doi: 10.3390/f14071328
Willebrand, T. et al. Snow tracking reveals different foraging patterns of red foxes and pine martens. Mamm. Res. 62, 331–340 (2017).
doi: 10.1007/s13364-017-0332-2
Ruosteenoja, K., Jylhä, K. & Kämäräinen, M. Climate projections for Finland under the RCP forcing scenarios. Geophysica 51, 17–50 (2016).
Sala, O. E. et al. Global biodiversity scenarios for the year 2100. Science 287, 1770–1774 (2000).
pubmed: 10710299
doi: 10.1126/science.287.5459.1770
Post, E. et al. Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355–1358 (2009).
pubmed: 19745143
doi: 10.1126/science.1173113
Legagneux, P. et al. Arctic ecosystem structure and functioning shaped by climate and herbivore body size. Nat. Clim. Change 4, 379–383 (2014).
doi: 10.1038/nclimate2168
Stoessel, M., Elmhagen, B., Vinka, M., Hellström, P. & Angerbjörn, A. The fluctuating world of a tundra predator guild: bottom-up constraints overrule top-down species interactions in winter. Ecography 42, 488–499 (2019).
doi: 10.1111/ecog.03984
Kauhala, K. Growth, size, and fat reserves of the raccoon dog in Finland. Acta Theriol. 38, 139–150 (1993).
doi: 10.4098/AT.arch.93-12
Lindström, E. Food limitation and social regulation in a red fox population. Ecography 12, 70–79 (1989b).
doi: 10.1111/j.1600-0587.1989.tb00824.x
Dell’Arte, G. A., Laaksonen, T., Norrdahl, K. & Korpimäki, E. Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey. Acta Oecol. 31, 276–281 (2007).
doi: 10.1016/j.actao.2006.12.007
Pellikka, J., Rita, H. & Lindén, H. Monitoring wildlife richness—Finnish applications based on wildlife triangle censuses. Ann. Zool. Fenn 42, 123–134 (2005).
Pierce, D. _ncdf4: Interface to Unidata netCDF (Version 4 or Earlier) Format Data Files_. R package version 1.21. https://CRAN.R-project.org/package=ncdf4 (2023).
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2022).
Bivand, R. R Packages for Analyzing Spatial Data: A Comparative Case Study with Areal Data. Geographical Anal. 54, 488–518 (2022).
doi: 10.1111/gean.12319
Brooks, B. E. et al. glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling. R J. 9, 378–400 (2017).
doi: 10.32614/RJ-2017-066