Abstract
The raccoon dog, Nyctereutes procyonoides, is a canid with a passive overwintering strategy in northern Europe. However, the behaviour and physiology of the Japanese subspecies, N. p. albus, which has fewer chromosomes than the other subspecies, remain unknown. We measured body temperature, body composition and blood biochemistry of wild free-ranging and fasted enclosure-housed N. p. albus during boreal winter in Hokkaido, Japan. Body temperature of N. p. albus decreased from 38°C in autumn to 35.9–36.7°C while maintaining a circadian rhythm in late February (n = 3). A transient 18–36% decrease in resting heart rate occurred when body temperature was low (n = 2). Despite a 33–45% decrease in body weight due to winter fasting, circulating glucose, total protein and triglyceride levels were maintained (n = 4). Serum urea nitrogen dropped by 43–45% from autumn to spring, suggesting protein conservation during fasting. The overwintering survival strategy of N. p. albus in central Hokkaido is based upon large changes in seasonal activity patterns, winter denning and communal housing without the large decrease in body temperature that is characteristic of subarctic animals exhibiting hibernation or torpor.
Similar content being viewed by others
References
Arnold W (1988) Social thermoregulation during hibernation in alpine marmots (Marmota marmota). J Comp Physiol [B] 158:151–156. doi:10.1007/BF01075828
Asikainen J, Mustonen AM, Hyvärinen H, Nieminen P (2004) Seasonal physiology of the wild raccoon dog (Nyctereutes procyonoides). Zool Sci 21:385–391. doi:10.2108/zsj.21.385
Craighead JJ, Varney JR, Craighead FC, Sumner JS (1974) Telemetry experiments with a hibernating black bear. Ursus 3:357–371
Dubois C, Armand M, Mekki N, Portugal H, Pauli AM, Bernard PM, Lafont H, Lairon D (1994) Effects of increasing amounts of dietary cholesterol on postprandial lipemia and lipoproteins in human subjects. J Lipid Res 35:1993–2007
Haba C, Oshida T, Sasaki M, Endo H, Ichikawa H, Masuda Y (2008) Morphological variation of the Japanese raccoon dog: implications for geographical isolation and environmental adaptation. J Zool (Lond) 274:239–247. doi:10.1111/j.1469-7998.2007.00376.x
Harlow HJ (1981) Torpor and other physiological adaptations of the badger (Taxidea taxus) to cold environments. Physiol Zool 54:267–275
Heptner VG, Naumov NP, Jürgenson PB, Sludski AA, Cirkova AF, Bannikov AG (1974) Gattung Nyctereutes Temminck 1839, Marderhunde oder Mangute. In: Heptner VG, Naumov NP (eds) Die Säugetiere der Sowjetunion, Band II: Seekühe und Raubtiere. Fischer, Jena, pp 67–97
Hissa R, Siekkinen J, Hohtola E, Saarela S, Hakala A, Pudas J (1994) Seasonal patterns in the physiology of the European brown bear (Ursus arctos arctos) in Finland. Comp Biochem Physiol Physiol 109:781–791. doi:10.1016/0300-9629(94)90222-4
Hwang YT, Larivière S, Messier F (2007) Energetic consequences and ecological significance of heterothermy and social thermoregulation in striped skunks (Mephitis mephitis). Physiol Biochem Zool 80:138–145. doi:10.1086/509211
Ikeda H, Eguchi K, Ono Y (1979) Home range utilization of a raccoon dog, Nyctereutes procyonoides viverrinus, Temminck, in a small islet in western Kyushu. Jpn J Ecol 29:35–48
Julien P, Fong B, Angel A (1984) Cardiac and peripheral lymph lipoproteins in dogs fed cholesterol and saturated fat. Arteriosclerosis 4:435–442
Kauhala K, Saeki M (2004) Raccoon dog, Nycteriutes procyonoides (Gray, 1834). In: Sillero-Zubiri C, Hoffmann M, Macdonald DW (eds) Canids: Foxes, Wolves, Jackals and Dogs. Status Survey and Conservation Action Plan. ICUN/SSC Canid Specialist Group, Gland, Switzerland and Cambridge, UK, pp 136–142
Korhonen H, Mononen J, Harri M (1991) Evolutionary comparison of energy economy between Finnish and Japanese raccoon dogs. Comp Biochem Physiol Physiol 100:293–295. doi:10.1016/0300-9629(91)90472-O
Mäkinen A, Kuokkanen MT, Valtonen M (1986) A chromosome-banding study in the Finnish and the Japanese raccoon dog. Hereditas 105:97–105. doi:10.1111/j.1601-5223.1986.tb00647.x
Masuda R (1994) Nucleotide sequence analysis of mitochondrial DNA in the Carnivora: molecular phylogenetic study using an improved PCR product-direct sequencing technique. Mamm Sci 34:81–89
Mustonen AM, Nieminen P, Puukka M, Asikainen J, Saarela S, Karonen SL, Kukkonen JV, Hyvärinen H (2004) Physiological adaptations of the raccoon dog (Nyctereutes procyonoides) to seasonal fasting-fat and nitrogen metabolism and influence of continuous melatonin treatment. J Comp Physiol [B] 174:1–12. doi:10.1007/s00360-003-0400-6
Mustonen AM, Asikainen J, Aho J, Nieminen P (2007a) Selective seasonal fatty acid accumulation and mobilization in the wild raccoon dog (Nyctereutes procyonoides). Lipids 42:1155–1167. doi:10.1007/s11745-007-3118-5
Mustonen AM, Asikainen J, Kauhala K, Paakkonen T, Nieminen P (2007b) Seasonal rhythms of body temperature in the free-ranging raccoon dog (Nyctereutes procyonoides) with special emphasis on winter sleep. Chronobiol Int 24:1095–1107. doi:10.1080/07420520701797999
Mustonen AM, Käkelä R, Käkelä A, Pyykönen T, Aho J, Nieminen P (2007c) Lipid metabolism in the adipose tissues of a carnivore, the raccoon dog, during prolonged fasting. Exp Biol Med (Maywood) 232:58–69
Nelson RA, Beck TD, Steiger DL (1984) Ratio of serum urea to serum creatinine in wild black bears. Science 226:841–842. doi:10.1126/science.6494914
Nieminen P, Hohtola E, Pyykönen T, Paakkonen T, Aho J, Cittová-Kontu M, Asikainen J, Mononen J, Mustonen AM (2005) Thermoregulatory adaptations of the overwintering captive raccoon dog (Nyctereutes procyonoides) in boreal climate. J Exp Zoolog A Comp Exp Biol 303:776–784. doi:10.1002/jez.a.208
Tanaka H (2006) Winter hibernation and body temperature fluctuation in the Japanese badger, Meles meles anakuma. Zoolog Sci 23:991–997. doi:10.2108/zsj.23.991
Ward OG, Wurster-Hill DH (1989) Ecological studies of Japanese raccoon dogs, Nyctereutes procyonoides viverrinus. J Mammal 70:330–334. doi:10.2307/1381515
Ward OG, Wurster-Hill DH (1990) Nyctereutes procyonoides. Mamm Species 358:1–5. doi:10.2307/3504213
Ward OG, Wurster-Hill DH, Ratty FJ, Song Y (1987) Comparative cytogenetics of Chinese and Japanese raccoon dogs, Nyctereutes procyonoides. Cytogenet Cell Genet 45:177–186. doi:10.1159/000132451
Acknowledgements
The authors would like to thank Masao Kosuge and Gen Bando for providing access to the Asahiyama Zoological Park facilities. We thank the staff at Asahiyama Zoological Park for skilled technical assistance. This study was funded by grants from the Wild Animal Fund of the Japanese Association of Zoos and Aquariums to D.F., JSPS Fellows (#20-10270) to N.K., and JSPS Grant-in-Aid for Exploratory Research (#18650226) to M.H.
Author information
Authors and Affiliations
Corresponding author
Additional information
Naoya Kitao, Daisuke Fukui and Peter G. Osborne contributed equally to this work
Rights and permissions
About this article
Cite this article
Kitao, N., Fukui, D., Hashimoto, M. et al. Overwintering strategy of wild free-ranging and enclosure-housed Japanese raccoon dogs (Nyctereutes procyonoides albus). Int J Biometeorol 53, 159–165 (2009). https://doi.org/10.1007/s00484-008-0199-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-008-0199-7