Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

High Arctic lemmings remain reproductively active under predator-induced elevated stress


Non-consumptive effects of predation have rarely been assessed in wildlife populations even though their impact could be as important as lethal effects. Reproduction of individuals is one of the most important demographic parameters that could be affected by predator-induced stress, which in turn can have important consequences on population dynamics. We studied non-consumptive effects of predation on the reproductive activity (i.e., mating and fertilization) of a cyclic population of brown lemmings exposed to intense summer predation in the Canadian High Arctic. Lemmings were live-trapped, their reproductive activity (i.e., testes visible in males, pregnancy/lactation in females) assessed, and predators were monitored during the summers of 2014 and 2015 within a 9 ha predator-reduction exclosure delimited by a fence and covered by a net, and on an 11 ha control area. Stress levels were quantified non-invasively with fecal corticosterone metabolites (FCM). We found that FCM levels of lemmings captured outside the predator exclosure (n = 50) were 1.6 times higher than inside (n = 51). The proportion of pregnant/lactating adult females did not differ between the two areas, nor did the proportion of adult scrotal males. We found that lemmings showed physiological stress reactions due to high predation risk, but had no sign of reduced mating activity or fertility. Thus, our results do not support the hypothesis of reproductive suppression by predator-induced stress.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2


  1. Banks PB (2000) Nonlinearity in the predation risk of prey mobility. Proc R Soc Lond B Biol Sci 267:1621–1625

  2. Banks EM, Brooks RJ, Schnell J (1975) A radiotracking study of home range and activity of the brown lemming (Lemmus trimucronatus). J Mammal 56:888–901. https://doi.org/10.2307/1379659

  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01

  4. Bethea CL, Centeno ML, Cameron JL (2008) Neurobiology of stress-induced reproductive dysfunction in female macaques. Mol Neurobiol 38:199–230. https://doi.org/10.1007/s12035-008-8042-z

  5. Bian J-H, Du S-Y, Wu Y et al (2015) Maternal effects and population regulation: maternal density-induced reproduction suppression impairs offspring capacity in response to immediate environment in root voles Microtus oeconomus. J Anim Ecol 84:326–336. https://doi.org/10.1111/1365-2656.12307

  6. Boonstra R (1985) Demography of Microtus pennsylvanicus in Southern Ontario: enumeration versus Jolly-Seber estimation compared. Can J Zool 63:1174–1180. https://doi.org/10.1139/z85-175

  7. Boonstra R (2013) Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. Funct Ecol 27:7–10. https://doi.org/10.1111/1365-2435.12008

  8. Boonstra R, Boag PT (1992) Spring declines in Microtus pennsylvanicus and the role of steroid hormones. J Anim Ecol 61:339–352. https://doi.org/10.2307/5326

  9. Boonstra R, Hik D, Singleton GR, Tinnikov A (1998a) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 68:371–394. https://doi.org/10.1890/0012-9615(1998)068[0371:tiopis]2.0.co;2

  10. Boonstra R, Krebs CJ, Stenseth NC (1998b) Population cycles in small mammals: the problem of explaining the low phase. Ecology 79:1479–1488. https://doi.org/10.1890/0012-9658(1998)079[1479:pcismt]2.0.co;2

  11. Boonstra R, Hubbs AH, Lacey EA, McColl CJ (2001a) Seasonal changes in glucocorticoid and testosterone concentrations in free-living arctic ground squirrels from the boreal forest of the Yukon. Can J Zool 79:49–58. https://doi.org/10.1139/z00-175

  12. Boonstra R, McColl CJ, Karels TJ (2001b) Reproduction at all costs: the adaptive stress response of male arctic ground squirrels. Ecology 82:1930–1946. https://doi.org/10.1890/0012-9658(2001)082[1930:raacta]2.0.co;2

  13. Bosson CO, Palme R, Boonstra R (2013) Assessing the impact of live-capture, confinement, and translocation on stress and fate in eastern gray squirrels. J Mammal 94:1401–1411. https://doi.org/10.1644/13-MAMM-A-046.1

  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

  15. Carpenter SR, Chisholm SW, Krebs CJ et al (1995) Ecosystem experiments. Science 269:324–327. https://doi.org/10.1126/science.269.5222.324

  16. Charbonnel N, Chaval Y, Berthier K et al (2008) Stress and demographic decline: a potential effect mediated by impairment of reproduction and immune function in cyclic vole populations. Physiol Biochem Zool 81:63–73. https://doi.org/10.1086/523306

  17. Christian JJ (1950) The adreno-pituitary system and population cycles in mammals. J Mammal 31:247–259. https://doi.org/10.2307/1375290

  18. Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5:374–381

  19. Cook RD (1977) Detection of influential observation in linear regression. Technometrics 19:15–18. https://doi.org/10.2307/1268249

  20. Creel S, Dantzer B, Goymann W, Rubenstein DR (2013) The ecology of stress: effects of the social environment. Funct Ecol 27:66–80. https://doi.org/10.1111/j.1365-2435.2012.02029.x

  21. Crespi EJ, Williams TD, Jessop TS, Delehanty B (2013) Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol 27:93–106. https://doi.org/10.1111/1365-2435.12009

  22. Dantzer B, Newman AEM, Boonstra R et al (2013) Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science 340:1215–1217. https://doi.org/10.1126/science.1235765

  23. Duchesne D, Gauthier G, Berteaux D (2011) Habitat selection, reproduction and predation of wintering lemmings in the Arctic. Oecologia 167:967–980. https://doi.org/10.1007/s00442-011-2045-6

  24. Erlinge S, Hasselquist D, Svensson M et al (2000) Reproductive behaviour of female Siberian lemmings during the increase and peak phase of the lemming cycle. Oecologia 123:200–207. https://doi.org/10.1007/s004420051006

  25. Fauteux D, Gauthier G, Berteaux D (2015) Seasonal demography of a cyclic lemming population in the Canadian Arctic. J Anim Ecol 84:1412–1422. https://doi.org/10.1111/1365-2656.12385

  26. Fauteux D, Gauthier G, Berteaux D (2016) Top-down limitation of lemmings revealed by experimental reduction of predators. Ecology 97:3231–3241. https://doi.org/10.1002/ecy.1570

  27. Fauteux D, Gauthier G, Berteaux D et al (2017) Assessing stress in arctic lemmings: fecal metabolite levels reflect plasma free corticosterone levels. Physiol Biochem Zool 90:370–382. https://doi.org/10.1086/691337

  28. Fauteux D, Gauthier G, Slevan-Tremblay G, Berteaux D (2018) Life in the fast lane: learning from the rare multiyear recaptures of brown lemmings in the High Arctic. Arctic Sci 4:146–151. https://doi.org/10.1139/as-2017-0017

  29. Fletcher QE, Boonstra R (2006) Do captive male meadow voles experience acute stress in response to weasel odour? Can J Zool 84:583–588. https://doi.org/10.1139/z06-033

  30. Gilg O, Hanski I, Sittler B (2003) Cyclic dynamics in a simple vertebrate predator-prey community. Science 302:866–868. https://doi.org/10.1126/science.1087509

  31. Gilg O, Sittler B, Sabard B et al (2006) Functional and numerical responses of four lemming predators in High Arctic Greenland. Oikos 113:193–216. https://doi.org/10.1111/j.2006.0030-1299.14125.x

  32. Gruyer N, Gauthier G, Berteaux D (2010) Demography of two lemming species on Bylot Island, Nunavut, Canada. Polar Biol 33:725–736. https://doi.org/10.1007/s00300-009-0746-7

  33. Herod SM, Dettmer AM, Novak MA et al (2010) Sensitivity to stress-induced reproductive dysfunction is associated with a selective but not a generalized increase in activity of the adrenal axis. Am J Physiol Endocrinol Metab 300:E28–E36

  34. Huck UW, Banks EM (1982) Male dominance status, female choice and mating success in the brown lemming, Lemmus trimucronatus. Anim Behav 30:665–675. https://doi.org/10.1016/S0003-3472(82)80136-X

  35. Huitu O, Koivula M, Korpimaki E et al (2003) Winter food supply limits growth of northern vole populations in the absence of predation. Ecology 84:2108–2118. https://doi.org/10.1890/02-0040

  36. Inchausti P, Ginzburg LR (2009) Maternal effects mechanism of population cycling: a formidable competitor to the traditional predator-prey view. Philos Trans R Soc B-Biological Sci 364:1117–1124. https://doi.org/10.1098/rstb.2008.0292

  37. Jochym M, Halle S (2012) To breed, or not to breed? Predation risk induces breeding suppression in common voles. Oecologia 170:943–953. https://doi.org/10.1007/s00442-012-2372-2

  38. Kokko H, Ranta E (1996) Evolutionary optimality of delayed breeding in voles. Oikos 77:173–175. https://doi.org/10.2307/3545599

  39. Korpimaki E, Norrdahl K, Valkama J (1994) Reproductive investment under fluctuating predation risk: microtine rodents and small mustelids. Evol Ecol 8:357–368. https://doi.org/10.1007/bf01238188

  40. Krebs CJ (2011) Of lemmings and snowshoe hares: the ecology of northern Canada. Proc R Soc B Biol Sci 278:481–489. https://doi.org/10.1098/rspb.2010.1992

  41. Legagneux P, Gauthier G, Berteaux D et al (2012) Disentangling trophic relationships in a High Arctic tundra ecosystem through food web modeling. Ecology 93:1707–1716. https://doi.org/10.1890/11-1973.1

  42. Lima SL (1986) Predation risk and unpredictable feeding conditions: determinants of body mass in birds. Ecology 67:377–385. https://doi.org/10.2307/1938580

  43. Mazerolle MJ (2017) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.1-1. https://cran.r-project.org/package=AICcmodavg. Accessed 11 Nov 2017

  44. McDonald IR, Lee AK, Bradley AJ, Than KA (1981) Endocrine changes in dasyurid marsupials with differing mortality patterns. Gen Comp Endocrinol 44:292–301. https://doi.org/10.1016/0016-6480(81)90004-6

  45. McDonald IR, Lee AK, Than KA, Martin RW (1988) Concentration of free glucocorticoids in plasma and mortality in the Australian bush rat (Rattus fuscipes Waterhouse). J Mammal 69:740–748. https://doi.org/10.2307/1381629

  46. McKinnon L, Berteaux D, Bêty J (2014) Predator-mediated interactions between lemmings and shorebirds: a test of the alternative prey hypothesis. Auk 131:619–628. https://doi.org/10.1642/AUK-13-154.1

  47. Monclús R, Palomares F, Tablado Z et al (2009) Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia 158:615–623. https://doi.org/10.1007/s00442-008-1201-0

  48. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x

  49. Norrdahl K, Korpimäki E (1995) Effects of predator removal on vertebrate prey populations: birds of prey and small mammals. Oecologia 103:241–248. https://doi.org/10.1007/bf00329086

  50. Norrdahl K, Korpimäki E (1998) Does mobility or sex of voles affect risk of predation by mammalian predators? Ecology 79:226–232. https://doi.org/10.2307/176877

  51. Palme R, Touma C, Arias N et al (2013) Steroid extraction: get the best our of faecal samples. Wiener Tierärztliche Monatsschrift. 100:238–246

  52. Pinheiro J, Bates D, DebRoy S, Sarkar D (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1-131. http://cran.r-project.org/package=nlme. Accessed 11 Nov 2017

  53. Predavec M, Krebs CJ (2000) Microhabitat utilisation, home ranges, and movement patterns of the collared lemming (Dicrostonyx groenlandicus) in the central Canadian Arctic. Can J Zool 78:1885–1890. https://doi.org/10.1139/z00-135

  54. Reid DG, Krebs CJ, Kenney A (1995) Limitation of collared lemming population-growth at low-densities by predation mortality. Oikos 73:387–398. https://doi.org/10.2307/3545963

  55. Rogovin KA, Naidenko SV (2010) Noninvasive assessment of stress in bank voles (Myodes glareolus, Cricetidae, Rodentia) by means of enzyme-linked immunosorbent assay (ELISA). Biol Bull 37:959–964. https://doi.org/10.1134/s1062359010090098

  56. Rogovin KA, Randall JA, Kolosova IE, Moshkin MP (2008) Long-term dynamics of fecal corticosterone in male great gerbils (Rhombomys opimus Licht.): effects of environment and social demography. Physiol Biochem Zool 81:612–626. https://doi.org/10.1086/588757

  57. Romero LM, Meister CJ, Cyr NE et al (2008) Seasonal glucocorticoid responses to capture in wild free-living mammals. Am J Physiol Integr Comp Physiol 294:R614–R622. https://doi.org/10.1152/ajpregu.00752.2007

  58. Salo P, Banks PB, Dickman CR, Korpimaki E (2010) Predator manipulation experiments: impacts on populations of terrestrial vertebrate prey. Ecol Monogr 80:531–546. https://doi.org/10.1890/09-1260.1

  59. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89. https://doi.org/10.1210/er.21.1.55

  60. Sheriff MJ, Love OP (2013) Determining the adaptive potential of maternal stress. Ecol Lett 16:271–280. https://doi.org/10.1111/ele.12042

  61. Sheriff MJ, Krebs CJ, Boonstra R (2009) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78:1249–1258. https://doi.org/10.1111/j.1365-2656.2009.01552.x

  62. Sinclair AR, Krebs CJ (2002) Complex numerical responses to top-down and bottom-up processes in vertebrate populations. Philos Trans R Soc London Ser B Biol Sci 357:1221–1231. https://doi.org/10.1098/rstb.2002.1123

  63. Takahashi LK, Baker EW, Kalin NH (1990) Ontogeny of behavioral and hormonal responses to stress in prenatally stressed male rat pups. Physiol Behav 47:357–364. https://doi.org/10.1016/0031-9384(90)90154-V

  64. Therrien JF, Gauthier G, Korpimäki E, Bêty J (2014) Predation pressure by avian predators suggests summer limitation of small-mammal populations in the Canadian Arctic. Ecology 95:56–67. https://doi.org/10.1890/13-0458.1

  65. Touma C, Sachser N, Mostl E, Palme R (2003) Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 130:267–278. https://doi.org/10.1016/s0016-6480(02)00620-2

  66. Touma C, Palme R, Sachser N (2004) Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm Behav 45:10–22. https://doi.org/10.1016/j.yhbeh.2003.07.002

  67. Whirledge S, Cidlowski JA (2013) A role for glucocorticoids in stress-impaired reproduction: beyond the hypothalamus and pituitary. Endocrinology 154:4450–4468. https://doi.org/10.1210/en.2013-1652

  68. Wilson DJ, Krebs CJ, Sinclair T (1999) Limitation of collared lemming populations during a population cycle. Oikos 87:382–398. https://doi.org/10.2307/3546754

  69. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724. https://doi.org/10.1046/j.1365-2826.2003.01033.x

  70. Ylönen H, Eccard JA, Jokinen I, Sundell J (2006) Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent? Behav Ecol Sociobiol 60:350–358. https://doi.org/10.1007/s00265-006-0171-7

Download references


The research relied on the logistic assistance of the Polar Continental Shelf Program (Natural Resources Canada) and of Sirmilik National Park. The research was funded by the Natural Sciences and Engineering Research Council of Canada (Discovery Grants and Frontiers to Discovery programs), the Northern Student Training Program of Indian and Northern Affairs Canada, the Canadian Network of Centres of Excellence ArcticNet, Environord, the W. Garfield Weston Foundation, and the Fonds de recherche du Québec—Nature et technologies. We thank Christine Lambert, Gabriel Montpetit, and David Gaspard for their help with the field work. We also thank all the Bylot Island field team for their assistance in this project. We thank Dennis Murray, Marc J. Mazerolle, Conrad Cloutier, Doug Morris, and Mark Hewitt for their constructive comments on a previous version of this manuscript.

Data accessibility

All data used in this manuscript are available at the NordicanaD website: http://www.cen.ulaval.ca/nordicanad/en_index.aspx. http://dx.doi.org/10.5885/45400AW-9891BD76704C4CE2.

Author information

DF performed data collection in the field and in the laboratory, completed the statistical analyses, and wrote a complete draft of the manuscript; GG and DB co-supervised the project, performed data collection in the field, and significantly contributed to revisions of the text; RP and RB performed laboratory analyses and substantially contributed to revisions of the text.

Correspondence to Dominique Fauteux.

Additional information

Communicated by Janne Sundell.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 20 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fauteux, D., Gauthier, G., Berteaux, D. et al. High Arctic lemmings remain reproductively active under predator-induced elevated stress. Oecologia 187, 657–666 (2018). https://doi.org/10.1007/s00442-018-4140-4

Download citation


  • Cyclic populations
  • Top-down limitation
  • Glucocorticoids
  • Population regulation
  • Reproduction suppression