Large-scale variation in birth timing and synchrony of a large herbivore along the latitudinal and altitudinal gradients.
Bioclimatic Law
altitude
birth timing
climate change
large hervibore
latitude
parturition
phenology
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
21
06
2019
accepted:
28
04
2020
pubmed:
8
5
2020
medline:
20
3
2021
entrez:
8
5
2020
Statut:
ppublish
Résumé
Hopkins' Bioclimatic Law predicts geographical patterns in phenological timing by establishing a correspondence between latitudinal and altitudinal gradients. First proposed for key phenological events of plants, such as leaf sprouting or flowering dates, this law has rarely been used to assess the geographical equivalence of key life-history traits of mammals. We hypothesize that (H1) parturition dates of European roe deer Capreolus capreolus are delayed and more synchronized at higher latitudes and altitudes, (H2) parturition timing varies along latitudinal and altitudinal gradients in a way that matches the Hopkins' Bioclimatic Law and (H3) females adjust parturition timing to match the period of high energy demand with peak resource availability. We used parturition dates of 7,444 European roe deer from Switzerland to assess altitudinal variation in birth timing and synchrony from 288 to 2,366 m a.s.l. We then performed a literature survey to compare altitudinal results with those from different populations along the species' latitudinal range of distribution. Finally, we performed spatial analysis combining our highly resolved altitudinal data on parturition dates with plant phenology data. As expected, parturition dates were delayed with increasing latitude and altitude. This delay matched the Bioclimatic Law, as the effect of 1º increase in latitude was similar to 120 m increase in altitude. However, while parturitions were more synchronized with increasing altitude, we did not detect any trend along the latitudinal gradient. Finally, plant phenology explained altitudinal variation in parturition timing better than a linear effect of altitude. Our findings clearly demonstrate the ability of a large herbivore to match parturition timing with phenological conditions across the altitudinal gradient, even at the smallest spatial scales.
Identifiants
pubmed: 32379900
doi: 10.1111/1365-2656.13251
doi:
Banques de données
Dryad
['10.5061/dryad.z8w9ghx8g']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1906-1917Informations de copyright
© 2020 British Ecological Society.
Références
Aitken, R. J. (1974). Delayed implantation in roe deer (Capreolus capreolus). Journal of Reproduction and Fertility, 39, 225-233. https://doi.org/10.1530/jrf.0.0390225
Albon, S. D., & Langvatn, R. (1992). Plant phenology and the benefits of migration in a temperate ungulate. Oikos, 65, 502-513. https://doi.org/10.2307/3545568
Andersen, R., Gaillard, J. M., Linnell, J. D., & Duncan, P. (2000). Factors affecting maternal care in an income breeder, the European roe deer. Journal of Animal Ecology, 69(4), 672-682. https://doi.org/10.1046/j.1365-2656.2000.00425.x
Bears, H., Martin, K., & White, G. C. (2009). Breeding in high-elevation habitat results in shift to slower life-history strategy within a single species. Journal of Animal Ecology, 78, 365-375. https://doi.org/10.1111/j.1365-2656.2008.01491.x
Beldal, E. J., Barba, E., Gil-Delgado, J. A., Iglesias, D. J., López, G. M., & Monrós, J. S. (1998). Laying date and clutch size of Great Tits (Parus major) in the Mediterranean region: A comparison of four habitat types. Journal für Ornithologie, 139, 269-276. https://doi.org/10.1007/BF01653337
Bendix, J. (2002). A satellite-based climatology of fog and low-level stratus in Germany and adjacent areas. Atmospheric Research, 64, 3-18. https://doi.org/10.1016/S0169-8095(02)00075-3
Beniston, M., & Rebetez, M. (1996). Regional behavior of minimum temperatures in Switzerland for the period 1979-1993. Theoretical and Applied Climatology, 53, 231-243. https://doi.org/10.1007/BF00871739
Both, C., & te Marvelde, L. (2007). Climate change and timing of avian breeding and migration throughout Europe. Climate Research, 35, 93-105. https://doi.org/10.3354/cr00716
Boyce, M. S. (1979). Seasonality and patterns of natural selection for life histories. The American Naturalist, 114, 569-583. https://doi.org/10.1086/283503
Broennimann, O., Petitpierre, B., Randin, C., Engler, R., Breiner, F., D'Amen, M., … Di Cola, V. (2018). ecospat: Spatial ecology miscellaneous methods. R package version, 3. Retrieved from http://CRAN.R-project.org/package=ecospat
Bunnell, F. L. (1982). The lambing period of mountain sheep: Synthesis, hypotheses, and tests. Canadian Journal of Zoology, 60, 1-14. https://doi.org/10.1139/z82-001
Cagnacci, F., Focardi, S., Heurich, M., Stache, A., Hewison, A. J. M., Morellet, N., … Urbano, F. (2011). Partial migration in roe deer: Migratory and resident tactics are end points of a behavioural gradient determined by ecological factors. Oikos, 120, 1790-1802. https://doi.org/10.1111/j.1600-0706.2011.19441.x
Christen, N., Janko, C., & Rehnus, M. (2018). The effect of environmental gradients on the bed site selection of roe deer (Capreolus capreolus). Mammal Research, 63, 83-89. https://doi.org/10.1007/s13364-017-0343-z
Clutton-Brock, T. H., Guinness, F. E., & Albon, S. D. (1982). Red deer: Behavior and ecology of two sexes. Chicago, IL: University of Chicago Press.
Clutton-Brock, T. H., Guinness, F. E., & Albon, S. D. (1983). The costs of reproduction to red deer hinds. Journal of Animal Ecology, 52, 367-383. https://doi.org/10.2307/4560
Clutton-Brock, T. H., Major, M., Albon, S. D., & Guinness, F. E. (1987). Early development and population dynamics in red deer. I. Density-dependent effects on juvenile survival. Journal of Animal Ecology, 56, 53-67. https://doi.org/10.2307/4799
Coulon, A., Cosson, J. F., Angibault, J. M., Cargnelutti, B., Galan, M., Morellet, N., … Hewison, A. J. M. (2004). Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: An individual-based approach. Molecular Ecology, 13(9), 2841-2850. https://doi.org/10.1111/j.1365-294X.2004.02253.x
Coulson, T., Kruuk, L. E. B., Tavecchia, G., Pemberton, J. M., & Clutton-Brock, T. H. (2003). Estimating selection on neonatal traits in red deer using elasticity path analysis. Evolution, 57, 2879-2892. https://doi.org/10.1111/j.0014-3820.2003.tb01528.x
Couriot, O., Hewison, A. J. M., Saïd, S., Cagnacci, F., Chamaillé-Jammes, S., Linnell, J. D. C., … Morellet, N. (2018). Truly sedentary? The multi-range tactic as a response to resource heterogeneity and unpredictability in a large herbivore. Oecologia, 187, 47-60. https://doi.org/10.1007/s00442-018-4131-5
Dormann, C. F., Elith, J., Bacher, S., Buchmann, C., Carl, G., Carré, G., … Lautenbach, S. (2013). Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography, 36(1), 27-46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Dunmire, W. W. (1960). An altitudinal survey of reproduction in Peromyscus maniculatus. Ecology, 41, 174-182. https://doi.org/10.2307/1931951
Dupke, C., Bonenfant, C., Reineking, B., Hable, R., Zeppenfeld, T., Ewald, M., & Heurich, M. (2017). Habitat selection by a large herbivore at multiple spatial and temporal scales is primarily governed by food resources. Ecography, 40(8), 1014-1027.
Fargallo, J. A. (2004). Latitudinal trends of reproductive traits in the blue tit parus caeruleus. Ardeola, 51(1), 177-190. Retrieved from https://www.ardeola.org/es/volumenes/511/articulos/177-190/
Ferguson, S. H. (2002). The effects of productivity and seasonality on life history: comparing age at maturity among moose (Alces alces) populations. Global Ecology and Biogeography, 11, (4), 303-312. https://doi.org/10.1046/j.1466-822x.2002.00289.x
Festa-Bianchet, M. (1988). Birthdate and lamb survival in bighorn lambs (Ovis canadensis). Journal of Zoology, 214, 653-661.https://doi.org/10.1111/j.1469-7998.1988.tb03764.x
Festa-Bianchet, M., Jorgenson, J. T., & Réale, D. (2000). Early development, adult mass, and reproductive success in bighorn sheep. Behavioral Ecology, 11, 633-639. https://doi.org/10.1093/beheco/11.6.633
Fryxell, J. M., & Sinclair, A. R. E. (1988). Causes and consequences of migration by large herbivores. Trends in Ecology & Evolution, 3, 237-241. https://doi.org/10.1016/0169-5347(88)90166-8
Gaillard, J. M., Delorme, D., Jullien, J. M., & Tatin, D. (1993). Timing and synchrony of births in roe deer. Journal of Mammalogy, 74, 738-744. https://doi.org/10.2307/1382296
Gaillard, J. M., Mark Hewison, A. J., Klein, F., Plard, F., Douhard, M., Davison, R., & Bonenfant, C. (2013). How does climate change influence demographic processes of widespread species? Lessons from the comparative analysis of contrasted populations of roe deer. Ecology Letters, 16, 48-57. https://doi.org/10.1111/ele.12059
Gaudry, W., Saïd, S., Gaillard, J. M., Chevrier, T., Loison, A., Maillard, D., & Bonenfant, C. (2015). Partial migration or just habitat selection? Seasonal movements of roe deer in an Alpine population. Journal of Mammalogy, 96, 502-510. https://doi.org/10.1093/jmammal/gyv055
Gonseth, Y. W. T., Wohlgemuth, T., Sansonnens, B., & Buttler, A. (2001). Die biogeographischen Regionen der Schweiz. Erläuterungen und Einteilungsstandard. Umwelt Materialien Bundesamt Für Umwelt, Wald Und Landschaft Bern, 137, 1-48.
Güsewell, S., Pietragalla, B., Gehrig, R., & Furrer, R. (2018). Representativeness of stations and reliability of data in the Swiss phenology network (Vol. 267). Zürich, Switzerland: ETH Zurich.
Hass, C. C. (1997). Seasonality of births in bighorn sheep. Journal of Mammalogy, 78, 1251-1260. https://doi.org/10.2307/1383068
Hehman, E., Xie, S. Y., Ofosu, E. K., & Nespoli, G. A. (2018). Assessing the point at which averages are stable: A tool illustrated in the context of person perception. https://doi.org/10.31234/osf.io/2n6jq
Hemming, M. N., & Trevaskis, B. (2011). Make hay when the sun shines: The role of MADS-box genes in temperature-dependant seasonal flowering responses. Plant Science, 180(3), 447-453. https://doi.org/10.1016/j.plantsci.2010.12.001
Hewison, A. J. M., Gaillard, J. M., Angibault, J. M., Van Laere, G., & Vincent, J. P. (2002). The influence of density on post-weaning growth in roe deer Capreolus capreolus fawns. Journal of Zoology, 257(3), 303-309. https://doi.org/10.1017/S0952836902000900
Hewison, A. J. M., Morellet, N., Verheyden, H., Daufresne, T., Angibault, J.-M., Cargnelutti, B., … Cebe, N. (2009). Landscape fragmentation influences winter body mass of roe deer. Ecography, 32, 1062-1070. https://doi.org/10.1111/j.1600-0587.2009.05888.x
Hofmann, R. R. (1989). Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system. Oecologia, 78(4), 443-457. https://doi.org/10.1007/BF00378733
Hopkins, A. D. (1938). Bioclimatics: A science of life and climate relations (No. 280). Washington, DC: US Department of Agriculture.
Hurlbert, S. H. (1984). Pseudoreplication and the design of ecological field experiments. Ecological Monographs, 54, 187-211. https://doi.org/10.2307/1942661
Ineichen, P. (2015). Habitat selection of roe deer (Capreolus capreolus) in a landscape of fear shaped by human recreation. Master thesis, Department of Environmental Systems Science (D-USYS), Swiss Federal Institute of Technology (ETH) Zurich.
IPCC. (2013). Climate change 2013: The physical science basis. In T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, J. Boschung, A. Nauels, Y. Xia, V. Bex, & P. M. Midgley (Eds.), Contribution of working group I to the fifth assessment report of the Intergovernmental panel on climate change (pp. 1535). Cambridge, UK and New York, NY: Cambridge University Press.
Jönsson, K. I., & Jonsson, K. I. (1997). Capital and income breeding as alternative tactics of resource use in reproduction. Oikos, 57-66. https://doi.org/10.2307/3545800
Jullien, J. M., Delorme, D., & Gaillard, J. M. (1992). Détermination de l'âge chez le faon de chevreuil (Capreolus capreolus) dans son premier mois de vie. Mammalia, 56, 307-311.
Keech, M. A., Bowyer, R. T., Hoef, J. M. V., Boertje, R. D., Dale, B. W., & Stephenson, T. R. (2000). Life-history consequences of maternal condition in alaskan moose. The Journal of Wildlife Management, 64(2), 450-462. https://doi.org/10.2307/3803243
Kerby, J., & Post, E. (2013). Capital and income breeding traits differentiate trophic match-mismatch dynamics in large herbivores. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1624), 20120484. https://doi.org/10.1098/rstb.2012.0484
Larter, N. C., & Nagy, J. A. (2001). Seasonal and annual variability in the quality of important forage plants on Banks Island, Canadian High Arctic. Applied Vegetation Science, 4(1), 115-128. https://doi.org/10.1111/j.1654-109x.2001.tb00242.x
Lenormand, T. (2002). Gene flow and the limits to natural selection. Trends in Ecology & Evolution, 17, 183-189. https://doi.org/10.1016/S0169-5347(02)02497-7
Linnell, J. D. C., & Andersen, R. (1998). Timing and synchrony of birth in a hider species, the roe deer (Capreolus capreolus). Journal of Zoology, 244, 497-504. https://doi.org/10.1111/j.1469-7998.1998.tb00055.x
Loe, L. E., Bonenfant, C., Mysterud, A., Gaillard, J. M., Langvatn, R., Stenseth, N. C., … Pettorelli, N. (2005). Climate predictability and breeding phenology in red deer: Timing and synchrony of rutting and calving in timing and synchrony of rutting and calving in Norway and France. Journal of Animal Ecology, 74, 579-588. https://doi.org/10.1111/j.1365-2656.2005.00987.x.
López-López, P., García-Ripollés, C., & Urios, V. (2007). Population size, breeding performance and territory quality of Bonelli's eagle Hieraaetus fasciatus in eastern Spain. Bird Study, 54, 335-342. https://doi.org/10.1080/00063650709461493
Lovari, S., Herrero, J., Masseti, M., Ambarli, H., Lorenzini, R., & Giannatos, G. (2016). Capreolus capreolus. The IUCN Red List of Threatened Species 2016: e.T42395A22161386. 2018. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T42395A22161386.en
Moyes, K., Nussey, D. H., Clements, M. N., Guinness, F. E., Morris, A., Morris, S., … Clutton-brock, T. H. (2011). Advancing breeding phenology in response to environmental change in a wild red deer population. Global Change Biology, 17(7), 2455-2469. https://doi.org/10.1111/j.1365-2486.2010.02382.x
Mysterud, A. (1999). Seasonal migration pattern and home range of roe deer (Capreolus capreolus) in an altitudinal gradient in southern Norway. Journal of Zoology, 247, 479-486. https://doi.org/10.1111/j.1469-7998.1999.tb01011.x
Mysterud, A., Coulson, T., & Stenseth, N. C. (2002). The role of males in the dynamics of ungulate populations. Journal of Animal Ecology, 71, 907-915. https://doi.org/10.1046/j.1365-2656.2002.00655.x
Neter, J., Kutner, M. H., Nachtsheim, C. J., & Wasserman, W. (1996). Applied linear statistical models, New York, NY: McGraw-Hill/Irwin.
Oftedal, O. T. (1985). Pregnancy and lactation. In R. J. Hudson & R. G. White (Eds.), Bioenergetics of wild herbivores (pp. 215-238). Boca de Ratón, FL: CRC Press Inc.
Olsson, M. P., Widén, P., & Larkin, J. L. (2008). Effectiveness of a highway overpass to promote landscape connectivity and movement of moose and roe deer in Sweden. Landscape and Urban Planning, 85(2), 133-139. https://doi.org/10.1016/j.landurbplan.2007.10.006
Pagel, M. D., May, R. M., & Collie, A. (1991). Ecological aspects of the geographic distribution and diversity of mammal species. The American Naturalist, 137, 791-815.
Peláez, M., Gaillard, J. M., Bollmann, K., Heurich, M., & Rehnus, M. (2020). Data from: Large scale variation in birth timing and synchrony of a large herbivore along the latitudinal and altitudinal gradients. Dryad Digital Repository, https://doi.org/10.5061/dryad.z8w9ghx8g
Plard, F., Gaillard, J. M., Bonenfant, C., Hewison, A. J., Delorme, D., Cargnelutti, B., … Coulson, T. (2013). Parturition date for a given female is highly repeatable within five roe deer populations. Biology Letters, 9, 20120841.
Plard, F., Gaillard, J. M., Coulson, T., Hewison, A. J. M., Delorme, D., Warnant, C., & Bonenfant, C. (2014). Mismatch between birth date and vegetation phenology slows the demography of roe deer. PLoS Biology, 12, e1001828. https://doi.org/10.1371/journal.pbio.1001828
Post, E., Boving, P. S., Pedersen, C., & MacArthur, M. A. (2003). Synchrony between caribou calving and plant phenology in depredated and non-depredated populations. Canadian Journal of Zoology, 81, 1709-1714. https://doi.org/10.1139/z03-172
R Core Team. (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
Ramanzin, M., Sturaro, E., & Zanon, D. (2007). Seasonal migration and home range of roe deer (Capreolus capreolus) in the Italian eastern Alps. Canadian Journal of Zoology, 85, 280-289.
Rehnus, M., Arnold, J., Elliger, A., & Reimoser, F. (2018). Ear-marking of roe deer fawns (Capreolus capreolus): Results of long-term studies in Central Europe. Beiträge zur Jagd- und Wildforschung, 43, 1-20.
Rehnus, M., & Reimoser, F. (2014). Rehkitzmarkierung. Nutzen für Praxis und Forschung. Fauna Focus, 9, 1-16.
Rousset, F., & Ferdy, J.-B. (2014). Testing environmental and genetic effects in the presence of spatial autocorrelation. Ecography, 37, 781-790. https://doi.org/10.1111/ecog.00566
Rutberg, A. T. (1987). Adaptive hypotheses of birth synchrony in ruminants: An interspecific test. The American Naturalist, 130, 692-710. https://doi.org/10.1086/284739
Sadleir, R. M. F. S. (1969). The ecology of reproduction in wild and domestic mammals. London, UK: Methuen and Company Ltd.
Schönbrodt, F. D., & Perugini, M. (2013). At what sample size do correlations stabilize? Journal of Research in Personality, 47, 609-612. https://doi.org/10.1016/j.jrp.2013.05.009
Sigouin, D., Ouellet, J.-P., & Courtois, R. (1995). Moose (Alces alces) rutting period variations. Alces, 31, 185-197.
Stoner, D. C., Sexton, J. O., Nagol, J., Bernales, H. H., & Edwards Jr., T. C. (2016). Ungulate reproductive parameters track satellite observations of plant phenology across latitude and climatological regimes. PLoS ONE, 11, e0148780. https://doi.org/10.1371/journal.pone.0148780
Thompson, R. W., & Turner, J. C. (1982). Temporal geographic variation in the lambing season of bighorn sheep. Canadian Journal of Zoology, 60, 1781-1793. https://doi.org/10.1139/z82-231
Tixier, H., & Duncan, P. (1996). Are European roe deer browsers? A review of variations in the composition of their diets. Revue d'Écologie (Terre et vie), 51, 3-17.
Vitasse, Y., Signarbieux, C., & Fu, Y. H. (2018). Global warming leads to more uniform spring phenology across elevations. Proceedings of the National Academy of Sciences of the United States of America, 115(5), 1004-1008. https://doi.org/10.1073/pnas.1717342115
Weber, A. J. (1966). Regional differences in fawning times of North Carolina deer. Journal of Wildlife Management, 30, 843-845. https://doi.org/10.2307/3798295
Zammuto, R. M., & Millar, J. S. (1985). Environmental predictability, variability, and Spermophilus columbianus life history over an elevational gradient. Ecology, 66, 1784-1794. https://doi.org/10.2307/2937374
Zhao, Q. K. (1994). Birth timing shift with altitude and its ecological implication for Macaca thibetana at Mt Emei. Oecologia Montana, 3, 24-26.