Abstract
Most research on the demography of wild animal populations has focused on characterizing the variation in the mortality of organisms as a function of intrinsic and environmental characteristics. However, such variation in mortality is difficult to relate to functional life history components (e.g. reproduction, dispersal, hibernation) due to the difficulty in monitoring biological processes at a sufficiently fine timescale. In this study, we used a 10-year individual-based data set with an infra-annual timescale to investigate both intra- and inter-annual survival patterns according to intrinsic and environmental covariates in an introduced population of a small hibernating rodent, the Siberian chipmunk. We compared three distinct periods related to particular life history events: spring reproduction, summer reproduction and hibernation. Our results revealed strong interactions between intrinsic and temporal effects. First, survival of male chipmunks strongly decreases during the reproduction periods, while survival is high and equal between sexes during hibernation. Second, the season of birth affects the survival of juveniles during their first hibernation, which does not have long-lasting consequences at the adult stage. Third, at an inter-annual scale, we found that high food resource availability before hibernation and low chipmunk densities specifically favour subsequent winter survival. Overall, our results confirm that the well-known patterns of yearly and inter-individual variation of mortality observed in animals are themselves strongly variable within a given year, suggesting that they are associated with various functional components of the animals’ life history.
Similar content being viewed by others
References
Aars J, Ims RA (2002) Intrinsic and climatic determinants of population demography: the winter dynamics of tundra voles. Ecology 83:3449–3456
Andersson MB (1994) Sexual selection. Princeton University Press, Princeton
Badeck F-W, Bondeau A, Bottcher K et al (2004) Responses of spring phenology to climate change. New Phytol 162:295–309. doi:10.1111/j.1469-8137.2004.01059.x
Bergeron P, Montiglio P-O, Réale D et al (2013) Disruptive viability selection on adult exploratory behaviour in eastern chipmunks. J Evol Biol 26:766–774. doi:10.1111/jeb.12081
Bieber C, Juškaitis R, Turbill C, Ruf T (2012) High survival during hibernation affects onset and timing of reproduction. Oecologia 169:155–166. doi:10.1007/s00442-011-2194-7
Boyer N, Réale D, Marmet J et al (2010) Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538–547. doi:10.1111/j.1365-2656.2010.01659.x
Bronson FH (2009) Climate change and seasonal reproduction in mammals. Philos Trans R Soc Lond B Biol Sci 364:3331–3340. doi:10.1098/rstb.2009.0140
Burnham K, Anderson D (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer Science & Business Media, New York
Chantepie S, Teplitsky C, Pavard S et al (2015) Age-related variation and temporal patterns in the survival of a long-lived scavenger. Oikos. doi:10.1111/oik.02216
Chapuis J-L, Obolenskaya E V, Pisanu B, Lissovsky AA (2009) Datasheet on Tamias sibiricus. CABI, Wallingford, UK. (http://www.cabi.org/isc/)
Choquet R, Lebreton J-D, Gimenez O et al (2009) U-CARE: utilities for performing goodness of fit tests and manipulating CApture–REcapture data. Ecography 32:1071–1074. doi:10.1111/j.1600-0587.2009.05968.x
Clutton-Brock TH (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press
Clutton-Brock TH, Isvaran K (2007) Sex differences in ageing in natural populations of vertebrates. Proc R Soc Lond B Biol Sci 274:3097–3104. doi:10.1098/rspb.2007.1138
Clutton-Brock TH, Albon SD, Guinness FE (1985) Parental investment and sex differences in juvenile mortality in birds and mammals. Nature 313:131–133. doi:10.1038/313131a0
Cooch EG, White GC (2014) Program MARK—a gentle introduction, 13th edn
Coulson T, Catchpole EA, Albon SD et al (2001) Age, sex, density, winter weather, and population crashes in Soay sheep. Science (80) 292:1528–1531. doi:10.1126/science.292.5521.1528
Descamps S, Boutin S, McAdam AG et al (2009) Survival costs of reproduction vary with age in North American red squirrels. Proc R Soc Lond B Biol Sci 276:1129–1135. doi:10.1098/rspb.2008.1401
Duriez O, Ens BJ, Choquet R et al (2012) Comparing the seasonal survival of resident and migratory oystercatchers: carry-over effects of habitat quality and weather conditions. Oikos 121:862–873. doi:10.1111/j.1600-0706.2012.20326.x
Efford MG, Borchers DL, Byrom AE (2009) Density estimation by spatially explicit capture–recapture: likelihood-based methods. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations. Springer, New York, pp 255–269
Feder C, Martin JGA, Festa-Bianchet M et al (2008) Never too late? Consequences of late birthdate for mass and survival of bighorn lambs. Oecologia 156:773–781. doi:10.1007/s00442-008-1035-9
Forslund P, Part T (1995) Age and reproduction in birds—hypotheses and tests. Trends Ecol Evol 10:374–378. doi:10.1016/S0169-5347(00)89141-7
Garratt M, Lemaître J-F, Douhard M et al (2015) High juvenile mortality is associated with sex-specific adult survival and lifespan in wild roe deer. Curr Biol 25:759–763. doi:10.1016/j.cub.2014.11.071
Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875
Grant TA, Shaffer TL, Madden EM, Pietz PJ (2005) Time-specific variation in passerine nest survival: new insights into old questions. Auk 122:661–672. doi:10.1642/0004-8038(2005)122[0661:TVIPNS]2.0.CO;2
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
Hamel S, Gaillard J-M, Yoccoz NG et al (2010) Fitness costs of reproduction depend on life speed: empirical evidence from mammalian populations. Ecol Lett 13:915–935. doi:10.1111/j.1461-0248.2010.01478.x
Hardouin LA, Nevoux M, Robert A et al (2012) Determinants and costs of natal dispersal in a lekking species. Oikos 121:804–812. doi:10.1111/j.1600-0706.2012.20313.x
Hardouin LA, Robert A, Nevoux M et al (2014) Meteorological conditions influence short-term survival and dispersal in a reinforced bird population. J Appl Ecol 51:1494–1503. doi:10.1111/1365-2664.12302
Heldmaier G (1989) Seasonal acclimation of energy requirements in mammals: functional significance of body weight control, hypothermia, torpor and hibernation. In: Wieser W, Erich G (eds) Energy transformations in cells and organisms. Thieme, Stuttgart, pp 130–139
Hines JE, Kendall WL, Nichols JD (2003) On the use of the robust design with transient capture–recapture models. Auk 120:1151–1158. doi:10.1642/0004-8038(2003)120[1151:OTUOTR]2.0.CO;2
Huggins R (1989) On the statistical analysis of capture experiments. Biometrika 76:133–140
Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179
Kawamichi M (1996) Ecological factors affecting annual variation in commencement of hibernation in wild chipmunks (Tamias sibiricus). J Mammal 77:731–744
Kendall WL, Bjorkland R (2001) Using open robust design models to estimate temporary emigration from capture–recapture data. Biometrics 57:1113–1122
Kendall WL, Hines JE (1999) Program RDSURVIV: an estimation tool for capture–recapture data collected under Pollock’s robust design. Bird Study 46:S32–S38. doi:10.1080/00063659909477229
Kendall WL, Nichols JD, Hines JE (1997) Estimating temporary emigration using capture–recapture data with Pollock’s robust design. Ecology 78:563–578
Kerbiriou C, Le Viol I, Robert A et al (2009) Tourism in protected areas can threaten wild populations: from individual response to population viability of the chough Pyrrhocorax pyrrhocorax. J Appl Ecol 46:657–665. doi:10.1111/j.1365-2664.2009.01646.x
Kirkwood TBL, Rose MR (1991) Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc Lond B Biol Sci 332:15–24. doi:10.1098/rstb.1991.0028
Krasnov BR, Morand S, Hawlena H et al (2005) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146:209–217. doi:10.1007/s00442-005-0189-y
Kraus C, Thomson DL, Künkele J, Trillmich F (2005) Living slow and dying young? Life-history strategy and age-specific survival rates in a precocial small mammal. J Anim Ecol 74:171–180. doi:10.1111/j.1365-2656.2004.00910.x
Kraus C, Eberle M, Kappeler PM (2008) The costs of risky male behaviour: sex differences in seasonal survival in a small sexually monomorphic primate. Proc R Soc Lond B Biol Sci 275:1635–1644. doi:10.1098/rspb.2008.0200
Laake J, Rexstad E (2014) RMark—an alternative approach to building linear models in MARK. In: Cooch EG, White GC (eds) Programme MARK—a gentle introduction, 13th edn, pp C–1–C–113
Lane JE, Boutin S, Speakman JR, Humphries MM (2010) Energetic costs of male reproduction in a scramble competition mating system. J Anim Ecol 79:27–34. doi:10.1111/j.1365-2656.2009.01592.x
Le Coeur C, Robert A, Pisanu B, Chapuis J-L (2015a) Seasonal variation in infestations by ixodids on Siberian chipmunks: effects of host age, sex, and birth season. Parasitol Res 114:2069–2078. doi:10.1007/s00436-015-4391-5
Le Coeur C, Thibault M, Pisanu B et al (2015b) Temporally fluctuating selection on a personality trait in a wild rodent population. Behav Ecol 26:1285–1291. doi:10.1093/beheco/arv074
Lebl K, Bieber C, Adamík P et al (2011) Survival rates in a small hibernator, the edible dormouse: a comparison across Europe. Ecography 34:683–692. doi:10.1111/j.1600-0587.2010.06691.x
Leyrer J, Lok T, Brugge M et al (2013) Mortality within the annual cycle: seasonal survival patterns in Afro-Siberian red knots Calidris canutus canutus. J Ornithol 154:933–943. doi:10.1007/s10336-013-0959-y
Libert C, Dejager L, Pinheiro I (2010) The X chromosome in immune functions: when a chromosome makes the difference. Nat Rev Immunol 10:594–604. doi:10.1038/nri2815
Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348
Loison A, Festa-Bianchet M, Gaillard J-M et al (1999) Age-specific survival in five populations of ungulates: evidence of senescence. Ecology 80:2539–2554. doi:10.1890/0012-9658(1999)080[2539:ASSIFP]2.0.CO;2
Marmet J, Pisanu B, Chapuis J-L (2009) Home range, range overlap, and site fidelity of introduced Siberian chipmunks in a suburban French forest. Eur J Wildl Res 55:497–504. doi:10.1007/s10344-009-0266-3
Marmet J, Pisanu B, Chapuis J-L (2011) Natal dispersal of introduced Siberian chipmunks, Tamias sibiricus, in a suburban forest. J Ethol 29:23–29. doi:10.1007/s10164-010-0215-3
Marmet J, Pisanu B, Chapuis J-L et al (2012) Factors affecting male and female reproductive success in a chipmunk (Tamias sibiricus) with a scramble competition mating system. Behav Ecol Sociobiol 66:1449–1457. doi:10.1007/s00265-012-1399-z
Marsot M, Chapuis J-L, Gasqui P et al (2013) Introduced Siberian chipmunks (Tamias sibiricus barberi) contribute more to Lyme borreliosis risk than native reservoir rodents. PLoS One 8:e55377. doi:10.1371/journal.pone.0055377
Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science (80) 297:2015–20188. doi:10.1126/science.1074196
Neuhaus P, Pelletier N (2001) Mortality in relation to season, age, sex, and reproduction in Columbian ground squirrels (Spermophilus columbianus). Can J Zool 79:465–470. doi:10.1139/cjz-79-3-465
Noël F, Machon N, Robert A (2013) Integrating demographic and genetic effects of connections on the viability of an endangered plant in a highly fragmented habitat. Biol Conserv 158:167–174. doi:10.1016/j.biocon.2012.07.029
Obolenskaya EV, Lee M-Y, Dokuchaev NE et al (2009) Diversity of Palaearctic chipmunks (Tamias, Sciuridae). Mammalia 73:281–298. doi:10.1515/MAMM.2009.047
Pisanu B, Obolenskaya EV, Baudry E et al (2013) Narrow phylogeographic origin of five introduced populations of the Siberian chipmunk Tamias (Eutamias) sibiricus (Laxmann, 1769) (Rodentia: Sciuridae) established in France. Biol Invasions 15:1201–1207. doi:10.1007/s10530-012-0375-x
Pollock KH (1982) A capture–recapture design robust to unequal probability of capture. J Wildl Manage 46:752–757
Prendergast BJ, Freeman DA, Zucker I, Nelson RJ (2002) Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am J Physiol Integr Comp Physiol 282:R1054–R1062. doi:10.1152/ajpregu.00562.2001
Promislow D (1992) Costs of sexual selection in natural populations of mammals. Proc Biol Sci 247:203–210
Radchuk V, Johst K, Groeneveld J et al (2014) Appropriate resolution in time and model structure for population viability analysis: insights from a butterfly metapopulation. Biol Conserv 169:345–354. doi:10.1016/j.biocon.2013.12.004
Rexstad E, Burnham KP (1992) User’s guide for interactive program CAPTURE. Colorado Cooperative Fish and Wildlife Research Unit
Robert A, Paiva VH, Bolton M et al (2012) The interaction between reproductive cost and individual quality is mediated by oceanic conditions in a long-lived bird. Ecology 93:1944–1952. doi:10.1890/11-1840.1
Rödel HG, Bora A, Kaetzke P et al (2004) Over-winter survival in subadult European rabbits: weather effects, density dependence, and the impact of individual characteristics. Oecologia 140:566–576. doi:10.1007/s00442-004-1616-1
Roff DA (1992) Evolution of life histories: theory and analysis. Springer Science & Business Media, New York
R Core Team (2014) R: a language and environment for statistical computing
Schaub M, Vaterlaus-Schlegel C (2001) Annual and seasonal variation of survival rates in the garden dormouse (Eliomys quercinus). J Zool 255:89–96. doi:10.1017/S0952836901001133
Skalski JR, Hoffmann A, Smith SG (1993) Testing the significance of individual-and cohort-level covariates in animal survival studies. In Lebreton JD, North OM (eds) Marked individuals in the study of bird populations. Birkäuser, Base pp 9–28
Stanley TR, Burnham KP (1999) A closure test for time-specific capture–recapture data. Environ Ecol Stat 6:197–209
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Théoret-Gosselin R, Hamel S, Côté SD (2015) The role of maternal behavior and offspring development in the survival of mountain goat kids. Oecologia 178:175–186. doi:10.1007/s00442-014-3198-x
Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc Lond B Biol Sci 278:3355–3363. doi:10.1098/rspb.2011.0190
Wang LCH (1989) Ecological, physiological, and biochemical aspects of torpor in mammals and birds. Animimal adaptations to cold. Springer, Berlin Heidelberg New York, pp 361–401
West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science (80) 295:1685–1688. doi: 10.1126/science.1069043
White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139. doi:10.1080/00063659909477239
Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1:124–131. doi:10.1046/j.1474-9728.2002.00020.x
Wilson JA, Kelt DA, Van Vuren DH, Johnson ML (2008) Population dynamics of small mammals in relation to production of cones in four types of forests in the northern Sierra Nevada, California. Southwest Nat 53:346–356. doi:10.1894/MLK-02.1
Acknowledgments
We are thankful to the Office National des Forêts, France for financial support and for allowing fieldwork in the La Faisanderie site (Sénart Forest, France). This work was also funded by the Conseil Régional d’Ile-de-France, the Conseil Départemental des Hauts-de-Seine and the Ministère de l’Ecologie, du Développement durable et de l’Energie. We are thankful to J. Marmet and M. Marsot for their contribution to the mark-recapture monitoring. We wish to thank J. E. Hines for his helpful explanations of RDSURVIV and CAPTURE software and A. Bel (Bureau de Recherches Géologiques et Minières Ile-de-France) for sharing data on Champigny groundwater.
Author contribution statement
J. L. C. and B. P. conceived the monitoring design; J. L. C., B. P. and C. L. C. conducted the fieldwork; C. L. C., S. C. and A. R. analysed the data. C. L. C., S. C. and A. R. wrote the manuscript; other authors provided editorial advice.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Janne Sundell.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Le Cœur, C., Chantepie, S., Pisanu, B. et al. Inter-annual and inter-individual variations in survival exhibit strong seasonality in a hibernating rodent. Oecologia 181, 795–807 (2016). https://doi.org/10.1007/s00442-016-3597-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-016-3597-2