Abstract
Age-related deterioration of physiological functions is one of the most evident manifestations of ageing. In wild populations of some species, including murid rodents, lifespans are substantially modified by environmental signals that affect an individual’s response to such challenges as unfavourable climatic conditions, parasitic load etc. But the real impact of ageing on natural mortality of most species remains obscure. To clarify how age affects the responsiveness of organisms to environmental challenges, we performed longitudinal laboratory observations of wild-derived northern red-backed voles (Myodes rutilus). We fixed individual longevity and measured metabolic indexes (basal and maximal metabolic rates), ability to maintain body temperature under acute cooling, plasma corticosterone, indexes of acquired and innate immunity in the same individuals of 3–4, 6–7 and 9–10 months old. The maximum estimated lifespan was about 2 years 8 months, which is considerably older than in nature, but less than 30% of individuals passed the one-year milestone. Regardless of the intense mortality, in the first year of life, animals did not demonstrate any age-related deterioration in physiological functions, except leucocyte number. No consistency in any individual physiological index was found. As the individual longevity of red-backed voles varied between years of captivity, we suggest that the welfare and lifespan of wild animals in captivity may be affected by the environmental conditions in the period preceding removal of the animal from the wild.
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References
Austad SN (2009) Comparative biology of aging. J Gerontol Ser A Biol Sci Med Sci 64(2):199–201
Bashenina NV, Aristov AA, Bernshtein AD (1981) Evropeyskaya ryzhaya polevka. Nauka, Moscow
Boonstra R (1994) Population cycles in microtines: the senescence hypothesis. Evol Ecol 8:196–219. https://doi.org/10.1007/BF01238250
Boonstra R, Boag PT (1992) Spring declines in Microtus pennsylvanicus and the role of steroid hormones. J Anim Ecol 61:339–352
Boonstra R, Krebs CJ (2012) Population dynamics of red-backed voles (Myodes) in North America. Oecologia 168(3):601–620
Breuner CW, Delehanty B, Boonstra R (2013) Evaluating stress in natural populations of vertebrates: total CORT is not good enough. Funct Ecol 27:24–36. https://doi.org/10.1111/1365-2435.12016
Buffenstein R (2008) Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J. Comp Physiol B Biochem Syst Environ Physiol 178:439–445
Cohen AA (2018) Aging across the tree of life: the importance of a comparative perspective for the use of animal models in aging. Biochim Biophys Acta Mol Basis Dis 1864:2680–2689
Dammann P, Burda H (2007) Senescence patterns in African Mole-rats (Bathyergidae, Rodentia). In: Begall S, Burda H, Schleich CE (eds) Subterranean rodents: news from underground. Springer, Berlin, pp 251–263
Dammann P, Šumbera R, Maßmann C et al (2011) Extended longevity of reproductives appears to be common in Fukomys mole-rats (Rodentia, Bathyergidae). PLoS ONE 6:2–8. https://doi.org/10.1371/journal.pone.0018757
De Magalhães JP, Costa J (2009) A database of vertebrate longevity records and their relation to other life-history traits. J Evol Biol 22:1770–1774. https://doi.org/10.1111/j.1420-9101.2009.01783.x
Finch CE (1990) Longevity, senescence, and the genome. The University of Chicago Press, Chicago
Fletcher QE, Dantzer B, Boonstra R (2015) The impact of reproduction on the stress axis of free-living male northern red backed voles (Myodes rutilus). Gen Comp Endocrinol 224:136–147. https://doi.org/10.1016/j.ygcen.2015.07.004
Hansson L, Henttonen H (1985) Gradients in density variations of small rodents: the importance of latitude and snow cover. Oecologia 67:394–402. https://doi.org/10.1007/BF00384946
Hansson L, Henttonen H (1988) Rodent dynamics as community processes. Trends Ecol Evol 3:195–200. https://doi.org/10.1016/0169-5347(88)90006-7
Harman D (1956) Aging: a theory on free radical radiation chemistry. J. Gerontol. 11:298–300. https://doi.org/10.1093/geronj/11.3.298
Hayssen V, Lacy RC (1985) Basal metabolic rates in mammals: taxonomic differences in the allometry of BMR and body mass. Comp Biochem Physiol Part A Physiol 81:741–754. https://doi.org/10.1016/0300-9629(85)90904-1
Jimenez AG (2018) “The same thing that makes you live can kill you in the end”: exploring the effects of growth rates and longevity on cellular metabolic rates and oxidative stress in mammals and birds. Integr Comp Biol 58:544–558. https://doi.org/10.1093/icb/icy090
Kalela O (1957) Regulation of reproduction rate in subarctic populations of the vole, Clethrionomys rufocanus (Sund.). Ann Acad Sci Fenn Ser A IV Biol 34:1–60
Kenyon CJ (2010) The genetics of ageing. Nature 464:504–512. https://doi.org/10.1038/nature09047
Kirkwood TB, Rose MR (1991) Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc Lond B Biol Sci 332:15–24. https://doi.org/10.1098/rstb.1991.0028
Koshkina TV, Korotkov YS (1975) Regulative adaptations in populations of the red vole (Clethrionomys rutilus) under optimum conditions of its range. Fauna Ecol Rodents 12:5–61
Krebs CJ, Myers JH (1974) Population cycles in small mammals. In: MacFadyen A (ed) Advances in ecological research. Academic Press, London, pp 267–399
Kugler J, Lange KW, Kalveram KT (1988) Influence of bleeding order on plasma corticosterone concentration in the mouse. Exp Clin Endocrinol 91:241–243. https://doi.org/10.1055/s-0029-1210754
McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15. https://doi.org/10.1016/S0018-506X(02)00024-7
Mihok S, Boonstra R (1992) Breeding performance in captivity of meadow voles (Microtus pennsylvanicus) from decline-and increase-phase populations. Can J Zool 70:1561–1566
Møller AP, Saino N (2004) Immune response and survival. Oikos 104:299–304. https://doi.org/10.1111/j.0030-1299.2004.12844.x
Moshkin MP, Dobrotvorsky AK, Mak V et al (1998) Variability of immune response to heterologous erythrocytes during population cycles of red (Clethrionomys rutilus) and bank (C. glareolus) Voles. Oikos 82:131–138. https://doi.org/10.2307/3546923
Novikov E, Moshkin M (1998) Sexual maturation, adrenocortical function and population density of red-backed vole, Clethrionomys rutilus (Pall.). Mammalia 62:529–540
Novikov EA, Panov VV, Moshkin MP (2012) Density-dependent regulation in populations of northern red-backed voles (Myodes rutilus) in optimal and suboptimal habitats of southwest Siberia. Biol Bull Rev 2:431–438. https://doi.org/10.1134/S2079086412050052
Novikov EA, Kondratyuk EY, Burda H (2015a) Age-related increase of urine cortisol in non-breeding individuals of Fukomys Anselli (Rodentia, Bathyergidae) from a laboratory colony. Zool Zh 94:119–124. https://doi.org/10.7868/S0044513415010092
Novikov E, Kondratyuk E, Petrovski D et al (2015b) Reproduction, aging and mortality rate in social subterranean mole voles (Ellobius talpinus Pall.). Biogerontology 16:723–732. https://doi.org/10.1007/s10522-015-9592-x
Novikov E, Kondratyuk E, Petrovski D et al (2015c) Effects of parasites and antigenic challenge on metabolic rates and thermoregulation in northern red-backed voles (Myodes rutilus). Parasitol Res 114:4479–4486. https://doi.org/10.1007/s00436-015-4691-9
Novikov EA, Kondratyuk EY, Petrovskii DV (2015d) Effect of the life history pattern on bioenergetic parameters of northern red-backed voles (Myodes rutilus Pall.) in a mountain taiga population from the south of Western Siberia. Russ J Ecol 46:476–480. https://doi.org/10.1134/S106741361505015X
Novikov E, Kondratuk E, Titova T et al (2019) Reproduction and mortality rates in ecologically distinct species of murid rodents. Biogerontology 20:149–157. https://doi.org/10.1007/s10522-018-9783-3
Nussey DH, Froy H, Lemaitre JF et al (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225. https://doi.org/10.1016/j.arr.2012.07.004
Olenev GV (2002) Alternative types of ontogeny in cyclomorphic rodents and their role in population dynamics: an ecological analysis. Russ J Ecol 33:321–330. https://doi.org/10.1023/A:1020213709830
Panov VV (2001) Winter in the life of small mammals in Ob pine forests of northern forest-steppe of Western Siberia. Sib Ekol Zh 8:777–784
Pokrovsky A, Bolshakov V (1979) Experimental ecology of voles. Nauka, Moscow
Polikarpov IA, Kondratyuk EY, Petrovsky DV, Novikov EA (2017) Interpopulation variability of endocrine-metabolic reaction to cold stress in northern red-backed vole (Myodes rutilus). Biol Bull Rev 7:56–63. https://doi.org/10.1134/S2079086417010030
Polikarpov IA, Titova TV, Kondratyuk EY, Novikov EA (2018) Adrenocortical and bioenergetic responses to cold in laboratory-born northern red-backed voles (Myodes rutilus) from two populations in south Siberia, Russia. Can J Zool 96:660–666. https://doi.org/10.1139/cjz-2016-0314
Romero LM, Meister CJ, Cyr NE, Kenagy GJ, Wingfield JC (2008) Seasonal glucocorticoid responses to capture in wild free-living mammals. Am J Physiol-Regul Integr Comp Physiol 294:R614–R622
Rosner W (1990) The functions of corticosteroid-binding globulin and sex hormone-binding globulin: recent advances. Endocr Rev 11:80–91
Seluanov A, Hine C, Azpurua J et al (2009) Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat. Proc Natl Acad Sci USA 106:19352–19357. https://doi.org/10.1073/pnas.0905252106
Sheldon BC, Verhulst S (1996) Ecological immunology—costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321. https://doi.org/10.1016/0169-5347(96)10039-2
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. https://doi.org/10.1086/516403
Sipari S, Haapakoski M, Klemme I, Palme R, Sundell J, Ylönen H (2016) Population sex-ratio affecting behavior and physiology of overwintering bank voles (Myodes glareolus). Physiol Behav 159:45–51. https://doi.org/10.1016/j.physbeh.2016.03.008
Speakman JR, Selman C, McLaren JS, Harper EJ (2002) Living fast, dying when? The link between aging and energetics. J Nutr 132:1583S–1597S
Tkadlec E, Zejda J (1998) Density-dependent life histories in female bank voles from fluctuating populations. J Anim Ecol 67:863–873
Acknowledgements
The study was supported by the Federal Program of Fundamental Scientific Studies 2013–2020 (VI.51.1.8) AAAA-A16-116121410118-7 and by the Russian Foundation for Basic Research, grants 13-04-01045, 16-04-00888 and 19-04-00929.
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Keeping conditions were adjusted to the biology of the species to minimise the harmful and stressful effects of caging. Climatic regime in laboratory room was comfortable for the animals; conventional diet was balanced and included all the nutrients essential for the normal grows and development. The room was periodically sterilised by quartz lamp. We did not disturb the animals without the reason. If deceased, individuals were carefully removed from the cages. All manipulations with the animals were performed with care and according to local and national legal requirements. The Experimental protocol conforms to the provisions of the Declaration of Helsinki.
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Novikov, E.A., Kondratyuk, E.Y. & Polikarpov, I.A. Age-related differences in physiology and survival of northern red-backed voles (Myodes rutilus) in captivity. Biogerontology 21, 133–142 (2020). https://doi.org/10.1007/s10522-019-09847-w
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DOI: https://doi.org/10.1007/s10522-019-09847-w