Abstract
Phenological shifts are occurring in many ecosystems around the world. The capacity of species to adapt to changing phenology will be critical to their success under climate change scenarios. Failure to adjust migratory and reproductive timing to keep pace with the earlier onset of spring has led to negative demographic effects for populations of species across a variety of taxa. For caribou, there have been concerns that earlier spring green-up on calving areas might not be matched by earlier migration and parturition, potentially leading to a trophic mismatch with nutritional consequences for parturient and lactating caribou cows. However, there is limited evidence supporting these concerns. Here, we investigate the response of barren-ground caribou to changing spring phenology using data from telemetry and satellite imagery. From 2004 to 2016, we found that the average start of green-up on the calving area advanced by 7.25 days, while the start of migration advanced by 13.64 days, the end of migration advanced by 6.02 days, and the date of peak calving advanced by 9.42 days. Despite the advancing onset of green-up, we found no evidence for the development of a trophic mismatch because the advancing green-up coincided with earlier migration and calving by caribou. Changing snow cover on the late winter and migratory ranges was the most supported driver of advancing migratory behavior. The ability of caribou to adjust the timing of migratory and reproductive behavior in response to changing environmental conditions demonstrates the potential resilience of the species to some aspects of climate change.
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References
Alerstam T, Hedenstrom A, Akesson S (2003) Long-distance migration: evolution and determinants. Oikos 103:247–260
Arnold TW (2010) Uninformative parameters and model selection using akaike’s information criterion. J Wildl Manage 74:1175–1178. https://doi.org/10.2193/2009-367
Barnett TP, Adam JC, Lettenmaier DP (2005) Potential impacts of a warming climate on water availability in snow-dominated regions. Nature 438:303–309. https://doi.org/10.1038/nature04141
Bergerud AT, Luttich SN, Camps L (2008) The return of Caribou to Ungava. McGill-Queens University Press, New York
Bolger DT, Newmark WD, Morrison TA, Doak DF (2008) The need for integrative approaches to understand and conserve migratory ungulates. Ecol Lett 11:63–77. https://doi.org/10.1111/j.1461-0248.2007.01109.x
Both C, Van Turnhout CAM, Bijlsma RG et al (2009) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc B 277:1259–1266. https://doi.org/10.1098/rspb.2009.1525
Boulanger J, Poole KG, Gunn A, Wierzchowski J (2012) Estimating the zone of influence of industrial developments on wildlife: a migratory caribou Rangifer tarandus groenlandicus and diamond mine case study. Wildl Biol 18:164–179. https://doi.org/10.2981/11-045
Boulanger J, Croft B, Adamczewski J, et al (2017) An estimate of breeding females and analyses of demographics for the Bathurst herd of barren-ground caribou: 2015 calving ground photographic survey. GNWT Manuscript Report No. 267
Boulanger J, Campbell MW, Lee DS (2018) Estimating abundance and trend of the Qamanirjuaq mainland migratory barren-ground caribou subpopulation—June 2017. Department of Environment Technical Summary—No: 01-2018
Bowyer RT, Van Ballenberghe V, Kie JG, Maier JAK (1999) Birth-site selection by Alaskan moose: maternal strategies for coping with a risky environment. J Mamm 80:1070–1083. https://doi.org/10.2307/1383161
Brooks TM, Mittermeier RA, Mittermeier CG et al (2002) Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 16:909–923. https://doi.org/10.1046/j.1523-1739.2002.00530.x
Brown R, Derksen C, Wang L (2010) A multi-data set analysis of variability and change in Arctic spring snow cover extent, 1967–2008. J Geophys Res 115:D16111. https://doi.org/10.1029/2010JD013975
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Modell 197:516–519
Cameron RD, Smith WT, Fancy SG et al (1993) Calving success of female caribou in relation to body weight. Can J Zool 71:480–486
Cameron RD, Smith WT, White RG, Griffith B (2005) Central Arctic caribou and petroleum development: distributional, nutritional, and reproductive implications. Arctic 58:1–9
Campbell MW, Nishi JS, Boulanger J (2010) A calving ground photo survey of the Qamanirjuaq migratory barren-ground caribou (Rangifer tarandus groenlandicus) population—June 2008. GN Technical Report Series 2010—no. 1-10
Caro SP, Schaper SV, Hut RA et al (2013) The case of the missing mechanism: how does temperature influence seasonal timing in endotherms? PLoS Biol 11:e1001517. https://doi.org/10.1371/journal.pbio.1001517
Carstensen M, Delgiudice GD, Sampson BA (2003) Using doe behavior and vaginal-implant transmitters to capture neonate white-tailed deer in north-central Minnesota. Wildl Soc Bull 31:634–641
Cebrian MR, Kielland K, Finstad G (2008) Forage quality and reindeer productivity: multiplier effects amplified by climate change. Arctic, Antarct Alp Res 40:48–54. https://doi.org/10.1657/1523-0430(06-073)
Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260
Chen W, Adamczewski JZ, White L et al (2018) Impacts of climate-driven habitat change on the peak calving date of the Bathurst caribou in Arctic Canada. Polar Biol 41:1–15. https://doi.org/10.1007/s00300-018-2259-8
Cleland EE, Chuine I, Menzel A et al (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365. https://doi.org/10.1016/j.tree.2007.04.003
Collins WB, Smith TS (1991) Effects of wind-hardened snow on foraging by reindeer (Rangifer tarandus). Arctic 44:217–222. https://doi.org/10.2307/40511242
Cotton PA (2003) Avian migration phenology and global climate change. Proc Natl Acad Sci 100:12219–12222
Couturier S, Courtois R, Crépeau H et al (1996) Calving photocensus of the Rivière George Caribou Herd and comparison with an independent census. Rangifer 16:283–296
Couturier S, Côté SD, Otto RD et al (2009) Variation in calf body mass in migratory caribou: the role of habitat, climate, and movements. J Mammal 90:442–452
Crête M, Huot J (1993) Regulation of a large herd of migratory caribou: summer nutrition affects calf growth and body reserves of dams. Can J Zool 71:2291–2296
DeMars CA, Auger-Méthé M, Schlägel UE, Boutin S (2013) Inferring parturition and neonate survival from movement patterns of female ungulates: a case study using woodland caribou. Ecol Evol 3:4149–4160. https://doi.org/10.1002/ece3.785
Doiron M, Legagneux P, Gauthier G, Levesque E (2013) Broad-scale satellite Normalized Difference Vegetation Index data predict plant biomass and peak date of nitrogen concentration in Arctic tundra vegetation. Appl Veg Sci 16:343–351. https://doi.org/10.1111/j.1654-109X.2012.01219.x
Doiron M, Gauthier G, Levesque E (2015) Trophic mismatch and its effects on the growth of young in an Arctic herbivore. Glob Chang Biol 21:4364–4376. https://doi.org/10.1111/gcb.13057
Donnelly A, Caffarra A, O’Neill BF (2011) A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. Int J Biometeorol 55:805–817. https://doi.org/10.1007/s00484-011-0426-5
Dunn PO, Møller AP (2014) Changes in breeding phenology and population size of birds. J Anim Ecol 83:729–739. https://doi.org/10.1111/1365-2656.12162
Duquette LS (1988) Snow characteristics along caribou trails and within feeding areas during spring migration. Arctic 41:143–144
Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283
Fancy SG, White RG (1985) Energy expenditures by caribou while cratering in snow. J Wildl Manage 49:987–993
Fancy SG, White RG (1987) Energy expenditures for locomotion by barren-ground caribou. Can J Zool 65:122–128
Festa-Bianchet M, Ray JC, Boutin S et al (2011) Conservation of caribou (Rangifer tarandus) in Canada: an uncertain future. Can J Zool 89:419–434. https://doi.org/10.1139/z11-025
Fleck ES, Gunn A (1982) Characteristics of three barren-ground caribou calving grounds in the Northwest Territories N.W.T. Wildlife Service Progress Report No. 7. Yellowknife, N.W.T
Fryxell JM, Sinclair ARE (1988) Causes and consequences of migration by large herbivores. Trends Ecol Evol 3:237–241. https://doi.org/10.1016/0169-5347(88)90166-8
Gerhart KL, White RG, Cameron RD, Russell DE (1996) Body composition and nutrient reserves of arctic caribou. Can J Zool 74:136–146
Gerhart KL, Russell DE, Van DeWetering D et al (1997) Pregnancy of adult caribou (Rangifer tarandus): evidence for lactational infertility. J Zool 242:17–30
Gordo O, Brotons L, Ferrer X, Comas P (2005) Do changes in climate patterns in wintering areas affect the timing of the spring arrival of trans-Saharan migrant birds? Glob Chang Biol 11:12–21. https://doi.org/10.1111/j.1365-2486.2004.00875.x
Griffith B, Douglas DC, Walsh NE, et al (2002) Section 3: the porcupine caribou herd. US Geological Survey, Biological Resources Division, Biological Science Report USGS/BRD/BSR-2002-0001
Gurarie E, Hebblewhite M, Joly K et al (2019) Tactical departures and strategic arrivals: divergent effects of climate and weather on caribou spring migrations. Ecosphere 10:e02971
Gustine DD, Barboza PS, Adams L et al (2017) Advancing the match-mismatch framework for large herbivores in the Arctic: evaluating the evidence for a trophic mismatch in caribou. PLoS One 12:e0171807. https://doi.org/10.1371/journal.pone.0171807
Hall DK, Riggs GA, Salomonson VV et al (2002) MODIS snow-cover products. Remote Sens Environ 83:181–194. https://doi.org/10.1016/S0034-4257(02)00095-0
Hanski I (2011) Habitat loss, the dynamics of biodiversity, and a perspective on conservation. Ambio 40:248–255. https://doi.org/10.1007/s13280-011-0147-3
Heard DC, Williams TM, Melton DA (1996) The relationship between food intake and predation risk in migratory caribou and implications to caribou and wolf population dynamics. Rangifer 16:37–44
Helle T, Kojola I (2008) Demographics in an alpine reindeer herd: effects of density and winter weather. Ecography (Cop) 31:221–230. https://doi.org/10.1111/j.2008.0906-7590.04912.x
Johnson CJ, Russell DE (2014) Long-term distribution responses of a migratory caribou herd to human disturbance. Biol Conserv 177:52–63. https://doi.org/10.1016/j.biocon.2014.06.007
Johnson CJ, Parker KL, Heard DC (2001) Foraging across a variable landscape: behavioral decisions made by woodland caribou at multiple spatial scales. Oecologia 127:590–602. https://doi.org/10.1007/s004420000573
Johnson CJ, Boyce MS, Case RL et al (2005) Cumulative effects of human development on Arctic wildlife. Wildl Monogr 160:1–36. https://doi.org/10.2193/0084-0173
Kapnick S, Hall A (2012) Causes of recent changes in western North American snowpack. Clim Dyn 38:1885–1899. https://doi.org/10.1007/s00382-011-1089-y
Klein DR (1970) Tundra ranges north of the boreal forest. J Range Manag 23:8–14
Klein DR (1990) Variation in quality of caribou and reindeer forage plants associated with season, plant part, and phenology. Rangifer 10:123–130
Kunkel KE, Palecki M, Ensor L et al (2009) Trends in twentieth-century U.S. snowfall using a quality-controlled dataset. J Atmos Ocean Technol 26:33–44. https://doi.org/10.1175/2008JTECHA1138.1
Le Corre M, Dussault C, Côté SD (2017) Weather conditions and variation in timing of spring and fall migrations of migratory caribou. J Mamm 98:260–271. https://doi.org/10.1093/jmammal/gyw177
Leblond M, St-Laurent M-H, Côté SD (2016) Caribou, water, and ice—fine-scale movements of a migratory arctic ungulate in the context of climate change. Mov Ecol 4:1–12. https://doi.org/10.1186/s40462-016-0079-4
Long RA, Kie JG, Terry Bowyer R, Hurley MA (2009) Resource selection and movements by female mule deer Odocoileus hemionus: effects of reproductive stage. Wildl Biol 15:288–298. https://doi.org/10.2981/09-003
Mahoney SP, Schaefer JA (2002) Hydroelectric development and the disruption of migration in caribou. Biol Conserv 107:147–153. https://doi.org/10.1016/S0006-3207(02)00052-6
Mallory CD, Boyce MS (2018) Observed and predicted effects of climate change on Arctic caribou and reindeer. Environ Rev 26:13–25. https://doi.org/10.1139/er-2017-0032
McLoughlin PD, Dzus E, Wynes B, Boutin S (2003) Declines in populations of woodland caribou. J Wildl Manage 67:755–761
Miller FL, Gunn A (1986) Observations of barren-ground caribou travelling on thin ice during autumn migration. Arctic 39:85–88
Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc Natl Acad Sci 105:16195–16200
Moyes K, Nussey DH, Clements MN et al (2011) Advancing breeding phenology in response to environmental change in a wild red deer population. Glob Chang Biol 17:2455–2469. https://doi.org/10.1111/j.1365-2486.2010.02382.x
Myers-Smith IH, Forbes BC, Wilmking M et al (2011) Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett. https://doi.org/10.1088/1748-9326/6/4/045509
Nagy JA (2011) Use of space by caribou in northern Canada. University of Alberta, Alberta
Nagy JA, Campbell MW (2012) Herd structure, movements, calving grounds, activity periods, home range similarity, and behaviours of migratory and tundra-wintering barren-ground caribou on mainland Nunavut and eastern mainland Northwest Territories, Canada. Tech Rep Ser 2012—No 01-12 Nunavut Dep Environ Wildl Res Sect 190
Nicholson KL, Arthur SM, Horne JS, Garton EO (2016) Modeling caribou movements: seasonal ranges and migration routes of the Central Arctic Herd. PLoS One 11:e0150333. https://doi.org/10.1371/journal.pone.0150333
Pachkowski M, Côté SD, Festa-Bianchet M (2013) Spring-loaded reproduction: effects of body condition and population size on fertility in migratory caribou (Rangifer tarandus). Can J Zool 91:473–479
Paoli A, Weladji RB, Holand Ø, Kumpula J (2018) Winter and spring climatic conditions influence timing and synchrony of calving in reindeer. PLoS One 13:1–21. https://doi.org/10.1371/journal.pone.0195603
Paoli A, Weladji RB, Holand Ø, Kumpula J (2019) The onset in spring and the end in autumn of the thermal and vegetative growing season affect calving time and reproductive success in reindeer. Curr Zool. https://doi.org/10.1093/cz/zoz032
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Pearson RG, Phillips SJ, Loranty MM et al (2013) Shifts in Arctic vegetation and associated feedbacks under climate change. Nat Clim Chang 3:673–677. https://doi.org/10.1038/nclimate1858
Pettorelli N, Weladji RB, Holand Ø et al (2005) The relative role of winter and spring conditions: linking climate and phenology to alpine reindeer body mass. Biol Lett 1:24–26. https://doi.org/10.1098/rsbl.2004.0262
Plard F, Gaillard J-M, Coulson T et al (2014) Mismatch between birth date and vegetation phenology slows the demography of roe deer. PLoS One 12:e1001828. https://doi.org/10.1371/journal.pbio.1001828
Poole KG, Gunn A, Patterson BR, Dumond M (2010) Sea ice and migration of the Dolphin and Union caribou herd in the Canadian Arctic: an uncertain future. Arctic 63:414–428
Post E, Forchhammer MC (2008) Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos Trans R Soc B 363:2369–2375. https://doi.org/10.1098/rstb.2007.2207
Post E, Bøving PS, Pedersen C, Macarthur MA (2003) Synchrony between caribou calving and plant phenology in depredated and non-depredated populations. Can J Zool 81:1709–1714. https://doi.org/10.1139/Z03-172
R Core Team (2019) R: a language and environment for statistical computing
Reimers E, Klein DR, Sørumgård R (1983) Calving time, growth rate, and body size of Norwegian reindeer on different ranges. Arct Alp Res 15:107–118
Rienecker MM, Suarez MJ, Gelaro R et al (2011) MERRA: nASA’s modern-era retrospective analysis for research and applications. J Clim 24:3624–3648. https://doi.org/10.1175/JCLI-D-11-00015.1
Russell DE, Whitfield PH, Cai J et al (2013) CARMA’s caribou range climate database. Rangifer 33:145–152
Salomonson VV, Appel I (2004) Estimating fractional snow cover from MODIS using the normalized difference snow index. Remote Sens Environ 89:351–360. https://doi.org/10.1016/j.rse.2003.10.016
Sharma S, Magnuson JJ (2014) Oscillatory dynamics do not mask linear trends in the timing of ice breakup for Northern Hemisphere lakes from 1855 to 2004. Clim Change 124:835–847. https://doi.org/10.1007/s10584-014-1125-0
Sharma S, Couturier S, Côté SD (2009) Impacts of climate change on the seasonal distribution of migratory caribou. Glob Chang Biol 15:2549–2562. https://doi.org/10.1111/j.1365-2486.2009.01945.x
Stenseth NC, Mysterud A (2002) Climate, changing phenology, and other life history traits: nonlinearity and match—mismatch to the environment. Proc Natl Acad Sci 99:13379–13381
Taillon J, Barboza PS, Côté SD (2013) Nitrogen allocation to offspring and milk production in a capital breeder. Ecology 94:1815–1827
Turunen M, Soppela P, Kinnunen H et al (2009) Does climate change influence the availability and quality of reindeer forage plants? Polar Biol 32:813–832. https://doi.org/10.1007/s00300-009-0609-2
Tveraa T, Stien A, Bårdsen B-J, Fauchald P (2013) Population densities, vegetation green-up, and plant productivity: impacts on reproductive success and juvenile body mass in reindeer. PLoS One 8:e56450. https://doi.org/10.1371/journal.pone.0056450
Uboni A, Horstkotte T, Kaarlejärvi E et al (2016) Long-term trends and role of climate in the population dynamics of Eurasian reindeer. PLoS One 11:e0158359. https://doi.org/10.1371/journal.pone.0158359
Valkenburg P, Sellers RA, Squibb RC et al (2003) Population dynamics of caribou herds in southwestern Alaska. Rangifer 23:131–142
Veiberg V, Loe LE, Albon SD et al (2017) Maternal winter body mass and not spring phenology determine annual calf production in an Arctic herbivore. Oikos 126:980–987. https://doi.org/10.1111/oik.03815
Visser ME, Caro SP, van Oers K et al (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc B 365:3113–3127. https://doi.org/10.1098/rstb.2010.0111
Vistnes I, Nellemann C (2008) The matter of spatial and temporal scales: a review of reindeer and caribou response to human activity. Polar Biol 31:399–407. https://doi.org/10.1007/s00300-007-0377-9
Vistnes I, Nellemann C, Jordhøy P, Strand O (2004) Effects of infrastructure on migration and range use of wild reindeer. J Wildl Manage 68:101–108
Vors LS, Schaefer JA, Pond BA et al (2007) Woodland caribou extirpation and anthropogenic landscape disturbance in Ontario. J Wildl Manage 71:1249–1256. https://doi.org/10.2193/2006-263
Walther G-R, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395
Williams CT, Klaassen M, Barnes BM et al (2017) Seasonal reproductive tactics: annual timing and the capital-to-income breeder continuum. Philos Trans R Soc B 372:20160250. https://doi.org/10.1098/RSTB.2016.0250
Wilson RR, Parrett LS, Joly K, Dau JR (2016) Effects of roads on individual caribou movements during migration. Biol Conserv 195:2–8. https://doi.org/10.1016/j.biocon.2015.12.035
Xie SP, Deser C, Vecchi GA et al (2015) Towards predictive understanding of regional climate change. Nat Clim Chang 5:921–930. https://doi.org/10.1038/nclimate2689
Zeng H, Jia G, Forbes BC (2013) Shifts in Arctic phenology in response to climate and anthropogenic factors as detected from multiple satellite time series. Environ Res Lett 8:035036. https://doi.org/10.1088/1748-9326/8/3/035036
Acknowledgements
Funding for this study was provided by the Natural Sciences and Engineering Research Council of Canada, the World Wildlife Fund Canada Arctic Species Conservation Fund, and the W. Garfield Weston Foundation. The Government of Nunavut provided caribou telemetry data. We thank CL Mallory and the anonymous reviewers for comments that improved the manuscript.
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All authors contributed to the design of this study. CDM and SNW analyzed the data and wrote the manuscript. MWC and MSB provided editorial advice.
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Mallory, C.D., Williamson, S.N., Campbell, M.W. et al. Response of barren-ground caribou to advancing spring phenology. Oecologia 192, 837–852 (2020). https://doi.org/10.1007/s00442-020-04604-0
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DOI: https://doi.org/10.1007/s00442-020-04604-0