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Extreme climate event promotes phenological mismatch between sexes in hibernating ground squirrels

  • 1.

    Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).

    Article 

    Google Scholar 

  • 2.

    IPCC. Climate change 2014: Synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change. (2014).

  • 3.

    Inouye, D. W., Barr, B., Armitage, K. B. & Inouye, B. D. Climate change is affecting altitudinal migrants and hibernating species. Proc. Natl. Acad. Sci. 97, 1630–1633 (2000).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 4.

    Adamík, P. & Král, M. Climate- and resource-driven long-term changes in dormice populations negatively affect hole-nesting songbirds. J. Zool. 275, 209–215 (2008).

    Article 

    Google Scholar 

  • 5.

    Ozgul, A. et al. Coupled dynamics of body mass and population growth in response to environmental change. Nature 466, 482–485 (2010).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 6.

    Moyes, K. et al. Advancing breeding phenology in response to environmental change in a wild red deer population. Glob. Chang. Biol. 17, 2455–2469 (2011).

    ADS 
    Article 

    Google Scholar 

  • 7.

    Both, C., Van Asch, M., Bijlsma, R. G., Van Den Burg, A. B. & Visser, M. E. Climate change and unequal phenological changes across four trophic levels: Constraints or adaptations?. J. Anim. Ecol. 78, 73–83 (2009).

    PubMed 
    Article 

    Google Scholar 

  • 8.

    Visser, M. E., Van Noordwijk, A. J., Tinbergen, J. M. & Lessells, C. M. Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. B Biol. Sci. 265, 1867–1870 (1998).

    Article 

    Google Scholar 

  • 9.

    Thackeray, S. J. et al. Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob. Chang. Biol. 16, 3304–3313 (2010).

    ADS 
    Article 

    Google Scholar 

  • 10.

    Spooner, F. E. B., Pearson, R. G. & Freeman, R. Rapid warming is associated with population decline among terrestrial birds and mammals globally. Glob. Chang. Biol. 24, 4521–4531 (2018).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 11.

    Sheriff, M. J., Boonstra, R., Palme, R., Loren Buck, C. & Barnes, B. M. Coping with differences in snow cover: The impact on the condition, physiology and fitness of an arctic hibernator. Conserv. Physiol. 5, 1–12 (2017).

    Article 

    Google Scholar 

  • 12.

    Easterling, D. R. et al. Climate extremes: Observations, modeling, and impacts. Science 289, 2068–2075 (2000).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 13.

    IPCC. Managing the risks of extreme events and disasters to advance climate change adaptation: Special report of the Intergovernmental Panel on Climate Change. (2012).

  • 14.

    Krause, J. S. et al. The effect of extreme spring weather on body condition and stress physiology in Lapland longspurs and white-crowned sparrows breeding in the Arctic. Gen. Comp. Endocrinol. 237, 10–18 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 15.

    Latimer, C. E. & Zuckerberg, B. How extreme is extreme? Demographic approaches inform the occurrence and ecological relevance of extreme events. Ecol. Monogr. 89, 1–15 (2019).

    Article 

    Google Scholar 

  • 16.

    Gutschick, V. P. & BassiriRad, H. Extreme events as shaping physiology, ecology, and evolution of plants: Toward a unified definition and evaluation of their consequences. New Phytol. 160, 21–42 (2003).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 17.

    Bailey, L. D. & van de Pol, M. Tackling extremes: Challenges for ecological and evolutionary research on extreme climatic events. J. Anim. Ecol. 85, 85–96 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 18.

    Welbergen, J. A., Klose, S. M., Markus, N. & Eby, P. Climate change and the effects of temperature extremes on Australian flying-foxes. Proc. R. Soc. B Biol. Sci. 275, 419–425 (2008).

    Article 

    Google Scholar 

  • 19.

    Boucek, R. E. & Rehage, J. S. Climate extremes drive changes in functional community structure. Glob. Chang. Biol. 20, 1821–1831 (2014).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 20.

    Hale, S. et al. Fire and climatic extremes shape mammal distributions in a fire-prone landscape. Divers. Distrib. 22, 1127–1138 (2016).

    Article 

    Google Scholar 

  • 21.

    Frederiksen, M., Daunt, F., Harris, M. P. & Wanless, S. The demographic impact of extreme events: Stochastic weather drives survival and population dynamics in a long-lived seabird. J. Anim. Ecol. 77, 1020–1029 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 22.

    Wingfield, J. C., Kelley, J. P. & Angelier, F. What are extreme environmental conditions and how do organisms cope with them?. Curr. Zool. 57, 363–374 (2011).

    Article 

    Google Scholar 

  • 23.

    Helm, B. et al. Annual rhythms that underlie phenology: Biological time-keeping meets environmental change. Proc. R. Soc. B Biol. Sci. 280, 1–10 (2013).

    Google Scholar 

  • 24.

    Sheriff, M. J., Richter, M. M., Buck, C. L. & Barnes, B. M. Changing seasonality and phenological responses of free-living male Arctic ground squirrels: The importance of sex. Philos. Trans. R. Soc. B Biol. Sci. 368, (2013).

  • 25.

    Michener, G. R. & Locklear, L. Differential costs of reproductive effort for male and female Richardson’s ground squirrels. Ecology 71, 855–868 (1990).

    Article 

    Google Scholar 

  • 26.

    Williams, C. T., Barnes, B. M., Kenagy, G. J. & Buck, C. L. Phenology of hibernation and reproduction in ground squirrels: Integration of environmental cues with endogenous programming. J. Zool. 292, 112–124 (2014).

    Article 

    Google Scholar 

  • 27.

    Michener, G. R. Age, sex, and species differences in the annual cycles of ground-dwelling sciurids: Implications for sociality. in The biology of ground-dwelling squirrels: annual cycles, behavioral ecology, and sociality (eds. Murie, J. O. & Michener, G. R.) 81–107 (University of Nebraska Press, Lincoln, 1984).

  • 28.

    Kenagy, G. J., Sharbaugh, S. M. & Nagy, K. A. Annual cycle of energy and time expenditure in a golden-mantled ground squirrel population. Oecologia 78, 269–282 (1989).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 29.

    Michener, G. R. Sexual Differences in over-winter torpor patterns of Richardson’s ground squirrels in natural hibernacula. Oecologia 89, 397–406 (1992).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 30.

    Michener, G. R. Effect of climatic conditions on the annual activity and hibernation cycle of Richardson’s ground squirrels and Columbian ground squirrels. Can. J. Zool. 55, 693–703 (1977).

    Article 

    Google Scholar 

  • 31.

    Michener, G. R. The circannual cycle of Richardson’s ground squirrels in southern Alberta. J. Mammal. 60, 760–768 (1979).

    Article 

    Google Scholar 

  • 32.

    Sheriff, M. J., Buck, C. L. & Barnes, B. M. Autumn conditions as a driver of spring phenology in a free-living arctic mammal. Clim. Chang. Responses 2, 1–7 (2015).

    Article 

    Google Scholar 

  • 33.

    Edic, M. N., Martin, J. G. A. & Blumstein, D. T. Heritable variation in the timing of emergence from hibernation. Evol. Ecol. 34, 763–776 (2020).

    Article 

    Google Scholar 

  • 34.

    Lane, J. E., Kruuk, L. E. B., Charmantier, A., Murie, J. O. & Dobson, F. S. Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489, 554–557 (2012).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 35.

    Dobson, F. S., Lane, J. E., Low, M. & Murie, J. O. Fitness implications of seasonal climate variation in Columbian ground squirrels. Ecol. Evol. 6, 5614–5622 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 36.

    Armitage, K. B. Climate change and the conservation of marmots. Nat. Sci. 05, 36–43 (2013).

    Google Scholar 

  • 37.

    Neuhaus, P., Bennett, R. & Hubbs, A. Effects of a late snowstorm and rain on survival and reproductive success in Columbian ground squirrels (Spermophilus columbianus). Can. J. Zool. 77, 879–884 (1999).

    Article 

    Google Scholar 

  • 38.

    Williams, C. T. et al. Sex-dependent phenological plasticity in an arctic hibernator. Am. Nat. 190, 854–859 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 39.

    Barnes, B. M. Relationship between hibernation and reproduction in male ground squirrels. in Adaptations to the Cold: Tenth International Hibernation Symposium (eds. Geiser, F., Hulbert, A. J. & Nicol, S. C.) 71–80 (University of New England Press, 1996).

  • 40.

    Lee, T. M., Pelz, K., Licht, P. & Zucker, I. Testosterone influences hibernation in golden-mantled ground squirrels. Am. J. Physiol. Regul. Integr. Comput. Physiol. 259, 760–767 (1990).

    Article 

    Google Scholar 

  • 41.

    Richter, M. M., Barnes, B. M., Reilly, K. M. O., Fenn, A. M. & Buck, C. L. The influence of androgens on hibernation phenology of free-livingmale arctic ground squirrels. Horm. Behav. 89, 92–97 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    Michener, G. R. Spring emergence schedules and vernal behavior of Richardson’s ground squirrels: Why do males emerge from hibernation before females?. Behav. Ecol. Sociobiol. 14, 29–38 (1983).

    Article 

    Google Scholar 

  • 43.

    Wells, L. J. Seasonal sexual Rhythm and its experimental modification in the male of the thirteen-lined ground squirrel (Citellus tridecemlineatus). Anat. Rec. 62, 409–447 (1935).

    Article 

    Google Scholar 

  • 44.

    Michener, G. R. & Locklear, L. Over-winter weight loss by Richardson’s ground squirrels in relation to sexual differences in mating effort. J. Mammal. 71, 489–499 (1990).

    Article 

    Google Scholar 

  • 45.

    Poiani, A. Complexity of seminal fluid: A review. Behav. Ecol. Sociobiol. 60, 289–310 (2006).

    Article 

    Google Scholar 

  • 46.

    Michener, G. R. Estrous and gestation periods in Richardson’s ground squirrels. J. Mammal. 61, 531–534 (1980).

    Article 

    Google Scholar 

  • 47.

    Michener, G. R. Chronology of reproductive events for female Richardson’s ground aquirrels. J. Mammal. 66, 280–288 (1985).

    Article 

    Google Scholar 

  • 48.

    Michener, G. R. & McLean, I. G. Reproductive behaviour and operational sex ratio in Richardson’s ground squirrels. Anim. Behav. 52, 743–758 (1996).

    Article 

    Google Scholar 

  • 49.

    Hare, J. F., Todd, G. & Untereiner, W. A. Multiple mating results in multiple paternity in Richardson’s Ground Squirrels Spermophilus richardsonii. Can. Field Nat. 118, 90–94 (2004).

    Article 

    Google Scholar 

  • 50.

    Grumm, R., Arnott, J. & Halblaub, J. The epic eastern North American warm episode of March 2012. J. Oper. Meteorol. 2, 36–50 (2014).

    Article 

    Google Scholar 

  • 51.

    Environment and Climate Change Canada (ECCC). Top ten weather stories for 2012: story four—March’s meteorological mildness. (2017). Available at: https://www.ec.gc.ca/meteo-weather/default.asp?lang=En&n=70B4A3E9-1. (Accessed: 20th May 2020)

  • 52.

    Wilson, D. F. & Hare, J. F. Ground squirrel uses ultrasonic alarms. Nature 430, 523 (2004).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 53.

    Waterman, J. M., Macklin, G. F. & Enright, C. Sex-biased parasitism in Richardson’s ground squirrels (Urocitellus richardsonii) depends on the parasite examined. Can. J. Zool. 92, 73–79 (2014).

    Article 

    Google Scholar 

  • 54.

    Murie, J. O. & Harris, M. A. Annual variation of spring emergence and breeding in Columbian ground squirrels (Spermophilus columbianus). J. Mammal. 63, 431–439 (1982).

    Article 

    Google Scholar 

  • 55.

    Sikes, R. S. & Gannon, W. L. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal. 92, 235–253 (2011).

    Article 

    Google Scholar 

  • 56.

    Gannon, W. L. & Sikes, R. S. Guidelines of the American society of mammalogists for the use of wild mammals in research. J. Mammal. 88, 809–823 (2007).

    Article 

    Google Scholar 

  • 57.

    Zucker, I. & Boshes, M. Circannual body weight rhythms of ground squirrels: Role of gonadal hormones. Am. J. Physiol. Regul. Int. Comput. Physiol. 12, 546–551 (1982).

    Article 

    Google Scholar 

  • 58.

    Boonstra, R., Hubbs, A. H., Lacey, E. A. & McColl, C. J. 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 (2001).

    Article 

    Google Scholar 

  • 59.

    Bottini Luzardo, M., Centurion Castro, F., Alfaro Gamboa, M., Lopez, A. & Ake Lopez, A. Osmolarity of coconut water (Cocos nucifera) based diluents and their effect over viability of frozen boar semen. Am. J. Anim. Vet. Sci. 5, 187–191 (2010).

    Article 

    Google Scholar 

  • 60.

    Mollineau, W. M., Adogwa, A. O. & Garcia, G. W. Liquid and frozen storage of agouti (Dasyprocta leporina) semen extended with UHT milk, unpasteurized coconut water, and pasteurized coconut water. Vet. Med. Int. 2011, 1–5 (2011).

    Article 

    Google Scholar 

  • 61.

    Schulte-Hostedde, A. I., Millar, J. S. & Hickling, G. J. Evaluating body condition in small mammals. Can. J. Zool. 79, 1021–1029 (2001).

    Article 

    Google Scholar 

  • 62.

    Møller, A. P. & Birkhead, T. R. Copulation behaviour in mammals: Evidence that sperm competition is widespread. Biol. J. Linn. Soc. 38, 119–131 (1989).

    Article 

    Google Scholar 

  • 63.

    Sugg, D. W. & Chesser, R. K. Effective population sizes with multiple paternity. Genetics 137, 1147–1155 (1994).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 64.

    Murie, J. O. & Harris, M. A. Territoriality and dominance in male Columbian ground squirrels (Spermophilus columbianus). Can. J. Zool. 56, 2402–2412 (1978).

    Article 

    Google Scholar 

  • 65.

    Morton, M. L. & Gallup, J. S. Reproductive cycle of the Belding ground squirrel (Spermophilus beldingi beldingi): Seasonal and age differences. Gt. Basin Nat. 35, 427–433 (1975).

    Google Scholar 

  • 66.

    Barnes, B. M., Kretzmann, M., Licht, P. & Zucker, I. The influence of hibernation on testis growth and spermatogenesis in the golden-mantled ground squirrel Spermophilus lateralis. Biol. Reprod. 35, 1289–1297 (1986).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 


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