Article

Article name HEMATOLOGICAL ANALYSIS AS A METHOD OF MONITORING PHYSIOLOGICAL STATUS OF MEDIUM CARNIVOROUS MAMMALS IN THE RUSSIAN FAR EAST
Authors

Galina S. Alekseeva, PhD, Senior Researcher of A.N. Severtsov Institute of Ecology and Evolution of the RAS (119071, Russia, Moscow, Leninsky Prospekt, 33); iD ORCID: https://orcid.org/0000-0002-1996-2387; e-mail: gal.ser.alekseeva@gmail.com
Mariya N. Erofeeva, PhD, Senior Researcher of A.N. Severtsov Institute of Ecology and Evolution of the RAS (119071, Russia, Moscow, Leninsky Prospekt, 33); iD ORCID: https://orcid.org/0000-0002-4672-6160; e-mail: erofeevamariya@yandex.ru
Jose A. Hernandez-Blanco, PhD, Senior Researcher of A.N. Severtsov Institute of Ecology and Evolution of the RAS (119071, Russia, Moscow, Leninsky Prospekt, 33); iD ORCID: https://orcid.org/0000-0002-1072-2483; e-mail: j.a.hernandez.blanco@gmail.com
Mikhail N. Litvinov, PhD, Principal Engineer of A.N. Severtsov Institute of Ecology and Evolution of the RAS (119071, Russia, Moscow, Leninsky Prospekt, 33); iD ORCID: https://orcid.org/0000-0003-3493-199X; e-mail: mnlitvinov@rambler.ru
Mariya D. Chistopolova, Junior Researcher of A.N. Severtsov Institute of Ecology and Evolution of the RAS (119071, Russia, Moscow, Leninsky Prospekt, 33); iD ORCID: https://orcid.org/0000-0003-1605-6247; e-mail: chistopolova_m@mail.ru
Mariya D. Kim, Engineer of A.N. Severtsov Institute of Ecology and Evolution of the RAS (119071, Russia, Moscow, Leninsky Prospekt, 33); iD ORCID: https://orcid.org/0009-0007-4778-5078; e-mail: marykim1069@yandex.ru
Viatcheslav V. Rozhnov, Dr.Sc, Academician of A.N. Severtsov Institute of Ecology and Evolution of the RAS (119071, Russia, Moscow, Leninsky Prospekt, 33); iD ORCID: https://orcid.org/0000-0002-2142-0763; e-mail: rozhnov-v-2015@yandex.ru
Sergey V. Naidenko, Dr.Sc, Corresponding Member of the Russian Academy of Sciences, Head Researcher of A.N. Severtsov Institute of Ecology and Evolution of the RAS (119071, Russia, Moscow, Leninsky Prospekt, 33); iD ORCID: https://orcid.org/0000-0001-6400-5108; e-mail: snaidenko@mail.ru

Reference to article

Alekseeva G.S., Erofeeva M.N., Hernandez-Blanco J.A., Litvinov M.N., Chistopolova M.D., Kim M.D., Rozhnov V.V., Naidenko S.V. 2024. Hematological analysis as a method of monitoring physiological status of medium carnivorous mammals in the Russian Far East. Nature Conservation Research 9(4): 93–104. https://dx.doi.org/10.24189/ncr.2024.034

Section Research articles
DOI https://dx.doi.org/10.24189/ncr.2024.034
Abstract

Clinical blood analysis is considered not only a method of assessing the health status of individuals, but also their fitness and welfare, although the interpretation of the obtained data is complicated by the combined influence of various factors. For most wild carnivore species, there is insufficient information about the effect of environmental factors on hematological parameters. Mammals in the Far East are exposed to hard seasonal climate changes, and therefore have physiological adaptations that enable them to survive the cold season. The aim of this study was to estimate the hematological parameters of three widespread species of medium carnivorous mammals in this region, namely Meles leucurus amurensis, Prionailurus bengalensis euptilura, and Nyctereutes procyonoides ussuriensis, taking into account such factors as sex, age and season in the Ussuriisky State Nature Reserve (Russia), as well as to identify the most informative blood indicators of the animal physiological status. In spring and autumn of 2014–2023, blood samples were collected from 103 individuals of the studied carnivores. The animals were captured, immobilised, blood-sampled and released in the wild at the capture site. The number of leucocytes was counted in the field, and their ratio was detected on the blood smears in the lab. The absence of sex differences and the presence of age differences in the studied species were revealed, which corresponds to the already known data on the parameters of mammalian blood. In spring, Nyctereutes procyonoides ussuriensis had higher leucocyte count (14.77 ± 1.76 mln/ml and 12.33 ± 1.08 mln/ml (hereinafter, in spring vs. autumn, respectively)), the ratio of neutrophils to lymphocytes (4.87 ± 0.47 and 3.02 ± 0.28), and the percentage of segmented neutrophils (73.12 ± 1.77% and 62.95 ± 2.29%), and the lower percentage of lymphocytes (20.35 ± 1.45% and 25.64 ± 1.49%) compared to autumn. Similar blood patterns were observed in two other species. This may be the result of a decrease in body mass and poor condition of animals, i.e. physiological stress after a long winter period and a lack of food resources. In addition, Nyctereutes procyonoides ussuriensis had higher percentages of eosinophils, basophils, and band neutrophils (7.85 ± 1.61%, 3.69 ± 1.26%, 2.15 ± 0.34%, respectively) than Meles leucurus amurensis (2.55 ± 1.09%, 0.45 ± 0.17%, 0.55 ± 0.18%, respectively) and Prionailurus bengalensis euptilura (1.48 ± 0.59%, 0.30 ± 0.16%, 1.74 ± 0.47%, respectively). These differences are probably determined by the biological characteristics of Nyctereutes procyonoides ussuriensis, since this species is an ideal host and carrier of various diseases, and it also has specific morphological features of blood cells. Thus, our results demonstrate the importance of systematic blood tests and the necessity of considering both species-specific characteristics and environmental factors for assessing animal health.

Keywords

Amur leopard cat, Asian badger, immune system, leucogram, raccoon dog, red blood cells, white blood cells

Artice information

Received: 11.04.2024. Revised: 03.10.2024. Accepted: 14.10.2024.

The full text of the article
References

Barnes T.S., Goldizen A.W., Coleman G.T. 2008. Hematology and serum biochemistry of the brush-tailed rock-wallaby (Petrogale penicillata). Journal of Wildlife Diseases 44(2): 295–303. DOI: 10.7589/0090-3558-44.2.295
Becker D.J., Nachtmann C., Argibay H.D., Botto G., Escalera-Zamudio M., Carrera J.E., Tello C., Winiarski E., Greenwood A.D., Méndez-Ojeda M.L., Loza-Rubio E., Lavergne A., de Thoisy B., Czirják G.Á., Plowright R.K., Altizer S., Streicker D.G. 2019. Leukocyte profiles reflect geographic range limits in a widespread Neotropical bat. Integrative and Comparative Biology 59(5): 1176–1189. DOI: 10.1093/icb/icz007
Becker D.J., Albery G.F., Kessler M.K., Lunn T.J., Falvo C.A., Czirják G.Á., Martin L.B., Plowright R.K. 2020. Macroimmunology: the drivers and consequences of spatial patterns in wildlife immune defence. Journal of Animal Ecology 89(4): 972–995. DOI: 10.1111/1365-2656.13166
Castellanos A., Arias L., Jackson D., Castellanos R. 2010. Hematological and serum biochemical values of Andean bears in Ecuador. Ursus 21(1): 115–120. DOI: 10.2192/09GR002.1
Chang G.R., Mao F.C., Yang C.C., Chan F.T. 2006. Hematological profiles of the Formosan black bear (Ursus thibetanus formosanus). Zoological Studies 45(1): 93–97.
Davis A.K., Maney D.L. 2018. The use of glucocorticoid hormones or leucocyte profiles to measure stress in vertebrates: what's the difference?. Methods in Ecology and Evolution 9(6): 1556–1568. DOI: 10.1111/2041-210X.13020
Davis A.K., Maney D.L., Maerz J.C. 2008. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Functional Ecology 22(5): 760–772. DOI: 10.1111/j.1365-2435.2008.01467.x
Demas G.E. 2004. The energetics of immunity: a neuroendocrine link between energy balance and immune function. Hormones and Behavior 45(3): 173–180. DOI: 10.1016/j.yhbeh.2003.11.002
Demas G.E., Nelson R.J. 2012. Ecoimmunology. Oxford: Oxford University Press. 636 p.
Deveci D., Stone P.C.W., Egginton S. 2001. Differential effect of cold acclimation on blood composition in rats and hamsters. Journal of Comparative Physiology B 171(2): 135–143. DOI: 10.1007/s003600000156
Dhabhar F.S., Miller A.H., McEwen B.S., Spencer R.L. 1996. Stress-induced changes in blood leukocyte distribution. Role of adrenal steroid hormones. Journal of Immunology 157(4): 1638–1644. DOI: 10.4049/jimmunol.157.4.1638
Dillon W.R., Goldstein M. 1984. Multivariate analysis: methods and applications. New York: Wiley. 587 p.
Downs C.J., Dochtermann N.A., Ball R., Klasing K.C., Martin L.B. 2020. The effects of body mass on immune cell concentrations of mammals. American Naturalist 195(1): 107–114. DOI: 10.1086/706235
Ellwanger J.H., Chies J.A.B. 2021. Zoonotic spillover: understanding basic aspects for better prevention. Genetics and Molecular Biology 44(1): e20200355. DOI: 10.1590/1678-4685-GMB-2020-0355
Erofeeva M.N., Naidenko S.V. 2020. Interspecific variation in the relationships of mating partners in felids. Biology Bulletin 47(1): 63–70. DOI: 10.1134/S1062359019060062
Erofeeva M.N., Vasilieva N.A., Ananyeva M.S., Klyuchnikova P.S., Naidenko S.V. 2023. Meeting with a male can lead to stress: female reaction to a pairing with a partner in Felidae. Behavioural Processes 208: 104876. DOI: 10.1016/j.beproc.2023.104876
Fancourt B.A., Nicol S.C. 2019. Hematologic and serum biochemical reference intervals for wild eastern quolls (Dasyurus viverrinus): variation by age, sex, and season. Veterinary Clinical Pathology 48(1): 114–124. DOI: 10.1111/vcp.12703
Gaspar‐López E., Landete‐Castillejos T., Estevez J.A., Ceacero F., Gallego L., García A.J. 2011. Seasonal variations in red deer (Cervus elaphus) hematology related to antler growth and biometrics measurements. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 315(4): 242–249. DOI: 10.1002/jez.670
Gelli D., Gerardi G., Lai O., Stefani A., Contiero B., Segato S. 2024. Hematology and biochemistry reference intervals for rehabilitated European badgers (Meles meles). Journal of Zoo and Wildlife Medicine 54(4): 801–804. DOI: 10.1638/2023-0035
Gilbert M., Sulikhan N., Uphyrkina O., Goncharuk M., Kerley L., Castro E.H., Reeve R., Seimon T., McAloose D., Seryodkin I.V., Naidenko S.V., Davis C.A., Wilkie G.S., Vattipally S.B., Adamson W.E., Hinds C., Thomson E.C., Willett B.J., Hosie M.J., Logan N., McDonald M., Ossiboff R.J., Shevtsova E.I., Belyakin S., Yurlova A.A., Osofsky S.A., Miquelle D.G., Matthews L., Cleaveland S. 2020. Distemper, extinction, and vaccination of the Amur tiger. Proceedings of the National Academy of Sciences of the United States of America 117(50): 31954–31962. DOI: 10.1073/pnas.2000153117
Goncharuk M.S., Kerley L.L., Naidenko S.V., Rozhnov V.V. 2012. Prevalence of seropositivity to pathogens in small carnivores in adjacent areas of Lazovskii Reserve. Biology Bulletin 39(8): 708–713. DOI: 10.1134/S1062359012080067
Græsli A.R., Fahlman Å., Evans A.L., Bertelsen M.F., Arnemo J.M., Nielsen S.S. 2014. Haematological and biochemical reference intervals for free-ranging brown bears (Ursus arctos) in Sweden. BMC Veterinary Research 10(1): 183. DOI: 10.1186/s12917-014-0183-x
Harvey J.W. 2012. Veterinary hematology: a diagnostic guide and color atlas. Amsterdam: Elsevier Health Sciences. 368 p.
Heim R.J., Hölzel N., Heinken T., Kamp J., Thomas A., Darman G.F., Smirenski S.M., Heim W. 2019. Post-burn and long-term fire effects on plants and birds in floodplain wetlands of the Russian Far East. Biodiversity and Conservation 28: 1611–1628. DOI: 10.1007/s10531-019-01746-3
Herrera J., Nunn C.L. 2019. Behavioural ecology and infectious disease: implications for conservation of biodiversity. Philosophical Transactions of the Royal Society B: Biological Sciences 374(1781): 20180054. DOI: 10.1098/rstb.2018.0054
Hufschmid J., Beveridge I., Handasyde K.A. 2014. Haematology and serum biochemistry of adult free-ranging mountain brushtail possums (Trichosurus cunninghami), including correlations with season, sex, age, habitat type and disease status. Australian Journal of Zoology 61(6): 430–445. DOI: 10.1071/ZO12097
Johnstone C.P., Reina R.D., Lill A. 2012. Interpreting indices of physiological stress in free-living vertebrates. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 182(7): 861–879. DOI: 10.1007/s00360-012-0656-9
Johnstone C.P., Lill A., Reina R.D. 2017. Use of erythrocyte indicators of health and condition in vertebrate ecophysiology: a review and appraisal. Biological Reviews 92(1): 150–168. DOI: 10.1111/brv.12219
Kalinina S.N., Kizhina A.G., Ilyukha V.A. 2023. Morphological features and morphometric parameters of eosinophils in peripheral blood of the raccoon dog Nyctereutes procyonoides (Grey, 1834). Cell and Tissue Biology 17(6): 706–712. DOI: 10.1134/S1990519X23060081
Kido N., Kamegaya C., Omiya T., Wada Y., Takahashi M., Yamamoto Y. 2011. Hematology and serum biochemistry in debilitated, free-ranging raccoon dogs (Nyctereutes procyonoides) infested with sarcoptic mange. Parasitology International 60(4): 425–428. DOI: 10.1016/j.parint.2011.06.023
Kirk C.M., Amstrup S., Swor R., Holcomb D., O'Hara T.M. 2010a. Hematology of southern Beaufort Sea polar bears (2005–2007): biomarker for an Arctic ecosystem health sentinel. EcoHealth 7(3): 307–320. DOI: 10.1007/s10393-010-0322-1
Kirk C.M., Amstrup S., Swor R., Holcomb D., O'Hara T.M. 2010b. Morbillivirus and Toxoplasma exposure and association with hematological parameters for Southern Beaufort Sea polar bears: potential response to infectious agents in a sentinel species. EcoHealth 7: 321–331. DOI: 10.1007/s10393-010-0323-0
Korenberg E.I. 2000. Seasonal population dynamics of Ixodes ticks and tick-borne encephalitis virus. Experimental and Applied Acarology 24(9): 665–681. DOI: 10.1023/A:1010798518261
Korytny L.M., Kichigina N.V., Gartsman B.I., Gubareva T.S. 2007. Rain floods of the Far East and East Siberia. In: O. Vasiliev, P. van Gelder, E. Plate, M. Bolgov (Eds.): Extreme Hydrological Events: New Concepts for Security. NATO Science Series 78. Dordrecht, Netherlands: Springer. P. 125–135. DOI: 10.1007/978-1-4020-5741-0_10
Kovalzon V.M., Komarova A.D., Alekseeva G.S., Erofeeva M.N., Naidenko S.V. 2022. Motor activity dynamics and body temperature in Far Eastern forest and domestic cats in the fall–winter period. Journal of Evolutionary Biochemistry and Physiology 58(5): 1381–1388. DOI: 10.1134/S002209302205009X
Kusak J., Rafaj R.B., Žvorc Z., Huber D., Foršek J., Bedrica L., Mrljak V. 2005. Effects of sex, age, body mass, and capturing method on hematologic values of brown bears in Croatia. Journal of Wildlife Diseases 41(4): 843–847. DOI: 10.7589/0090-3558-41.4.843
Lindenfors P., Nunn C.L., Jones K.E., Cunningham A.A., Sechrest W., Gittleman J.L. 2007. Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Global Ecology and Biogeography 16(4): 496–509. DOI: 10.1111/j.1466-8238.2006.00301.x
Macdonald D.W., Yamaguchi N., Passanisi W.C. 1998. The health, haematology and blood biochemistry of free-ranging farm cats in relation to social status. Animal Welfare 7(3): 243–256. DOI: 10.1017/S0962728600020686
Maceda-Veiga A., Figuerola J., Martínez-Silvestre A., Viscor G., Ferrari N., Pacheco M. 2015. Inside the Redbox: applications of haematology in wildlife monitoring and ecosystem health assessment. Science of the Total Environment 514: 322–332. DOI: 10.1016/j.scitotenv.2015.02.004
Manjerovic M.B., Waterman J.M. 2012. Immunological sex differences in socially promiscuous African ground squirrels. PLoS ONE 7(6): e38524. DOI: 10.1371/journal.pone.0038524
Martin L.B., Weil Z.M., Nelson R.J. 2008. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society B: Biological Sciences 363(1490): 321–339. DOI: 10.1098/rstb.2007.2142
Mbizah M.M., Steenkamp G., Groom R.J. 2016. Evaluation of the applicability of different age determination methods for estimating age of the endangered African wild dog (Lycaon pictus). PLoS ONE 11(10): e0164676. DOI: 10.1371/journal.pone.0164676
Morera D., MacKenzie S.A. 2011. Is there a direct role for erythrocytes in the immune response?. Veterinary Research 42: 89. DOI: 10.1186/1297-9716-42-89
Mulder J.L. 2012. A review of the ecology of the raccoon dog (Nyctereutes procyonoides) in Europe. Lutra 55(2): 101–127.
Mustonen A.M., Nieminen P. 2018. A review of the physiology of a survival expert of big freeze, deep snow, and an empty stomach: the boreal raccoon dog (Nyctereutes procyonoides). Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 188(1): 15–25. DOI: 10.1007/s00360-017-1114-5
Myśliwy I., Perec-Matysiak A., Hildebrand J. 2022. Invasive raccoon (Procyon lotor) and raccoon dog (Nyctereutes procyonoides) as potential reservoirs of tick-borne pathogens: data review from native and introduced areas. Parasites & Vectors 15(1): 126. DOI: 10.1186/s13071-022-05245-3
Naidenko S.V., Alshinetskiy M.V. 2020. Size matters: zoo data analysis shows that the white blood cell ratio differs between large and small felids. Animals 10(6): 940. DOI: 10.3390/ani10060940
Naidenko S.V., Pavlova E.V., Kirilyuk V.E. 2014. Detection of seasonal weight loss and a serologic survey of potential pathogens in wild Pallas' cats (Felis [Otocolobus] manul) of the Daurian steppe, Russia. Journal of Wildlife Diseases 50(2): 188–194. DOI: 10.7589/2013-03-068
Naidenko S.V., Hernandez-Blanco J.A., Pavlova E.V., Erofeeva M.N., Sorokin P.A., Litvinov M.N., Kotlyar A.K., Sulikhan N.S., Rozhnov V.V. 2018. Primary study of seroprevalence to virus pathogens in wild felids of South Primorie, Russia. Canadian Journal of Zoology 96(8): 839–846. DOI: 10.1139/cjz-2017-0192
Naidenko S.V., Hernandez-Blanco J.A., Erofeeva M.N., Litvinov M.N., Rozhnov V.V. 2019a. Serum prevalence to non-viral pathogens in wild felids of Southern Primorye, Russia. Nature Conservation Research 4(1): 99–105. DOI: 10.24189/ncr.2019.010
Naidenko S.V., Hernandez-Blanco J.A., Seryodkin I.V., Miquelle D.G., Blidchenko E.Y., Litvinov M.N., Kotlyar A.K., Rozhnov V.V. 2019b. Serum prevalence of bears in the Russian Far East to different pathogens. Biology Bulletin 46(8): 960–965. DOI: 10.1134/S1062359019080089
Nelson R.J. 2004. Seasonal immune function and sickness responses. Trends in immunology 25(4): 187–192. DOI: 10.1016/j.it.2004.02.001
Nunn C.L. 2002. A comparative study of leukocyte counts and disease risk in primates. Evolution 56(1): 177–190. DOI: 10.1111/j.0014-3820.2002.tb00859.x
Nunn C.L., Gittleman J.L., Antonovics J. 2000. Promiscuity and the primate immune system. Science 290(5494): 1168–1170. DOI: 10.1126/science.290.5494.1168
Nunn C.L., Gittleman J.L., Antonovics J. 2003. A comparative study of white blood cell counts and disease risk in carnivores. Proceedings of the Royal Society B: Biological Sciences 270(1513): 347–356. DOI: 10.1098/rspb.2002.2249
Palenske N.M., Saunders D.K. 2002. Comparisons of blood viscosity between amphibians and mammals at 3°C and 38°C. Journal of Thermal Biology 27(6): 479–484. DOI: 10.1016/S0306-4565(02)00020-7
Pastor J., Mach-Raich E., Mesalles M., Gracia I., Martínez F., Vargas A., Cuenca R., Lavín S. 2009. Haematological reference values for the Iberian lynx. In: A. Vargas, C. Breitenmoser-Würsten, U. Breitenmoser (Eds.): Iberian lynx ex situ conservation: an interdisciplinary approach. Madrid: Fundación Biodiversidad. P. 185–196.
Pavlova E.V., Alekseeva G.S., Erofeeva M.N., Vasilieva N.A., Tchabovsky A.V., Naidenko S.V. 2018. The method matters: the effect of handling time on cortisol level and blood parameters in wild cats. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology 329(3): 112–119. DOI: 10.1002/jez.2191
Pérez J.M., Serrano E., Soriguer R.C., González F.J., Sarasa M., Granados J.E., Cano-Manuel F.J., Cuenca R., Fandos P. 2015. Distinguishing disease effects from environmental effects in a mountain ungulate: seasonal variation in body weight, hematology, and serum chemistry among Iberian ibex (Capra pyrenaica) affected by sarcoptic mange. Journal of Wildlife Diseases 51(1): 148–156. DOI: 10.7589/2014-01-008
Prikhodko O.Y., Soboleva E.V., Pretsiniek I.P. 2020. Analyzing of the situation with forest fires in the Primorsky region. IOP Conference Series: Earth and Environmental Science 459(5): 052077. DOI: 10.1088/1755-1315/459/5/052077
Rahman M.T., Sobur M.A., Islam M.S., Ievy S., Hossain M.J., El Zowalaty M.E., Rahman A.M.M.T., Ashour H.M. 2020. Zoonotic diseases: etiology, impact, and control. Microorganisms 8(9): 1405. DOI: 10.3390/microorganisms8091405
Rozhnov V.V., Sidorchuk N.V., Erofeeva M.N., Maslov M.V. 2014. Reproductive behavior of the Asian badger (Meles leucurus amurensis) at the Ussuriisky Reserve. Zoologicheskii Zhurnal 93(6): 778–785. DOI: 10.7868/S0044513414060129 [In Russian]
Rui P., Ma Z.J., Zhang X.Z., Li P.G., Gao G.P., Yang Z.Z., Zhang J.H. 2011. Hematology and serum biochemistry values in adult racoon dogs and foxes in Changli farms of Hebei province, China. African Journal of Microbiology Research 5: 4667–4672. DOI: 10.5897/AJMR11.932
Salakij C., Salakij J., Prihirunkit K., Narkkong N.A., Pitakkingthong D. 2010. Characterization of blood cells in the Leopard cat (Prionailurus bengalensis). Veterinary Clinical Pathology 39(2): 193–198. DOI: 10.1111/j.1939-165X.2010.00215.x
Seryodkin I.V., Odoyevskaya I.M., Konyaev S.V., Spiridonov S.E. 2020. Trichinella infection of wild carnivorans in Primorsky Krai, Russian Far East. Nature Conservation Research 5(Suppl.2): 31–40. DOI: 10.24189/ncr.2020.040
Seryodkin I.V., Kurnosova O.P., Khrustalev A.V., Esaulova N.V., Varlamova A.I., Odoevskaya I.М. 2023. Helminth zoonoses of wild carnivore mammals in the Primorsky Krai of the Russian Far East. Russian Journal of Parasitology 17(4): 443–452. DOI: 10.31016/1998-8435-2023-17-4-443-452
Shvarts E.A., Pushkaryov S.V., Krever V.G., Ostrovsky M.A. 1995. Geography of mammal diversity and searching for ways to predict global changes in biodiversity. Journal of Biogeography 22(4/5): 907–914. DOI: 10.2307/2845991
Soboleva A.S., Alekseeva G.S., Erofeeva M.N., Klyuchnikova P.S., Sorokin P.A., Naidenko S.V. 2021. Leukocytes count and profile during early postnatal ontogenesis in domestic cats: Effect of litter size and multiple paternity. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology 335(8): 637–648. DOI: 10.1002/jez.2508
Stannard H.J., Thompson P., McAllan B.M., Raubenheimer D. 2016. Hematology and serum biochemistry reference ranges of healthy captive Tasmanian devils (Sarcophilus harrisii) and their association with age, gender and seasonal variation. Mammalian Biology 81(4): 393–398. DOI: 10.1016/j.mambio.2016.03.007
Sutor A., Schwarz S., Conraths F.J. 2014. The biological potential of the raccoon dog (Nyctereutes procyonoides, Gray 1834) as an invasive species in Europe – new risks for disease spread?. Acta Theriologica 59(1): 49–59. DOI: 10.1007/s13364-013-0138-9
Tian J., Courtiol A., Schneeberger K., Greenwood A.D., Czirják G.A. 2015. Circulating white blood cell counts in captive and wild rodents are influenced by body mass rather than testes mass, a correlate of mating promiscuity. Functional Ecology 29(6): 823–829. DOI: 10.1111/1365-2435.12394
Tkachenko K.N. 2023. Increase in the abundance of the Amur leopard cat (Prionailurus bengalensis euptilura, Felidae, Carnivora) in the Southern Amur region. Biology Bulletin 50(9): 2425–2438. DOI: 10.1134/S106235902309039X
Uphyrkina O. 1996. Assessment of the influence of forest exploitation on species biodiversity in the Russian Far East. Working Paper 96-147, International Institute for Applied Systems Analysis, Laxenburg, Austria. 70 p.
van Lieshout S.H., Badás E.P., Mason M.W., Newman C., Buesching C.D., Macdonald D.W., Dugdale H.L. 2020. Social effects on age-related and sex-specific immune cell profiles in a wild mammal. Biology Letters 16(7): 20200234. DOI: 10.1098/rsbl.2020.0234
Weiss D.J., Wardrop K.J. 2011. Schalm's Veterinary Hematology, 6th ed. New York: Wiley. 1232 p.
White P.A., Belant J.L. 2016. Individual variation in dental characteristics for estimating age of African lions. Wildlife Biology 22(3): 71–77. DOI: 10.2981/wlb.00180
White R.J., Razgour O. 2020. Emerging zoonotic diseases originating in mammals: a systematic review of effects of anthropogenic land-use change. Mammal Review 50(4): 336–352. DOI: 10.1111/mam.12201
Winnacker H., Walker N.J., Brash M.G.I., MacDonald J.A., Delahay R.J. 2008. Haematological and biochemical measurements in a population of wild Eurasian badgers (Meles meles). Veterinary Record 162(17): 551–555. DOI: 10.1136/vr.162.17.551
Xu D.L., Hu X.K. 2020. Season and sex have different effects on hematology and cytokines in striped hamsters (Cricetulus barabensis). Journal of Comparative Physiology B 190: 87–100. DOI: 10.1007/s00360-019-01246-4
Zhou Y., Newman C., Kaneko Y., Buesching C., Chen W., Zhou Z., Xie Z., Macdonald D. 2017. Asian badgers – the same, only different: how diversity among badger societies informs socio-ecological theory and challenges conservation. In: D.W. Macdonald, C. Newman, L.A. Harrington (Eds.): Biology and Conservation of Musteloids. Oxford: Oxford University Press. P. 304–325. DOI: 10.1093/oso/9780198759805.003.0013
Zhuravlev Y.N. 1997. Sources and Management of Biodiversity in the Russian Far East. In: T. Abe, S.A. Levin, M. Higashi (Eds.): Biodiversity. New York: Springer. P. 231–247. DOI: 10.1007/978-1-4612-1906-4_14