How does increasing mast seeding frequency affect population dynamics of seed consumers? Wild boar as a case study.
Sus scrofa
climate change
climate projections
demographic population model
mast
population projections
resource budget model
spring temperatures
Journal
Ecological applications : a publication of the Ecological Society of America
ISSN: 1051-0761
Titre abrégé: Ecol Appl
Pays: United States
ID NLM: 9889808
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
18
09
2019
revised:
10
02
2020
accepted:
25
02
2020
pubmed:
17
4
2020
medline:
7
1
2021
entrez:
17
4
2020
Statut:
ppublish
Résumé
Mast seeding in temperate oak populations shapes the dynamics of seed consumers and numerous communities. Mast seeding responds positively to warm spring temperatures and is therefore expected to increase under global warming. We investigated the potential effects of changes in oak mast seeding on wild boar population dynamics, a widespread and abundant consumer species. Using long-term monitoring data, we showed that abundant acorn production enhances the proportion of breeding females. With a body-mass-structured population model and a fixed hunting rate of 0.424, we showed that high acorn production over time would lead to an average wild boar population growth rate of 1.197 whereas non-acorn production would lead to a stable population. Finally, using climate projections and a mechanistic model linking weather data to oak reproduction, we predicted that mast seeding frequency might increase over the next century, which would lead to increase in both wild boar population size and the magnitude of its temporal variation. Our study provides rare evidence that some species could greatly benefit from global warming thanks to higher food availability and therefore highlights the importance of investigating the cascading effects of changing weather conditions on the dynamics of wild animal populations to reliably assess the effects of climate change.
Banques de données
Dryad
['10.5061/dryad.0gb5mkkxr']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e02134Subventions
Organisme : Potenchene program
Pays : International
Organisme : Auvergne-Rhône-Alpes region
Pays : International
Organisme : Fédération Nationale des Chasseurs
Pays : International
Organisme : Research Council of Norway
ID : 223257
Pays : International
Organisme : Centre National de la Recherche Scientifique
Pays : International
Organisme : Office National des Forêts
Pays : International
Organisme : Office National de la Chasse et de la Faune Sauvage
Pays : International
Organisme : ANR program FOREPRO
ID : ANR-19-CE32-0008
Pays : International
Organisme : Institut National de la Recherche Agronomique
Pays : International
Organisme : European Research Council
ID : FP7-339728
Pays : International
Organisme : European Research Council
Pays : International
Informations de copyright
© 2020 by the Ecological Society of America.
Références
Ådahl, E., P. E. R. Lundberg, and N. Jonzen. 2006. From climate change to population change: the need to consider annual life cycles. Global Change Biology 12:1627-1633.
Augspurger, C. K. 2009. Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest. Functional Ecology 23:1031-1039.
Bergeron, P., D. Réale, M. M. Humphries, and D. Garant. 2011. Anticipation and tracking of pulsed resources drive population dynamics in eastern chipmunks. Ecology 92:2027-2034.
Bergqvist, G., S. Paulson, and B. Elmhagen. 2018. Effects of female body mass and climate on reproduction in northern wild boar. Wildlife Biology 2018. https://doi.org/10.2981/wlb.00421
Bieber, C., and T. Ruf. 2005. Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. Journal of Applied Ecology 42:1203-1213.
Bogdziewicz, M., M. Fernández-Martínez, R. Bonal, J. Belmonte, and J. M. Espelta. 2017. The Moran effect and environmental vetoes: phenological synchrony and drought drive seed production in a Mediterranean oak. Proceedings of the Royal Society B 284:20171784.
Bogdziewicz, M., M. A. Steele, S. Marino, and E. E. Crone. 2018. Correlated seed failure as an environmental veto to synchronize reproduction of masting plants. New Phytologist 219:98-108.
Bogdziewicz, M., R. Zwolak, and E. E. Crone. 2016. How do vertebrates respond to mast seeding? Oikos 125:300-307.
Boutin, S., L. A. Wauters, A. G. McAdam, M. M. Humphries, G. Tosi, and A. A. Dhondt. 2006. Anticipatory reproduction and population growth in seed predators. Science 314:1928-1930.
Brandt, S., E. Baubet, J. Vassant, and S. Servanty. 2006. Régime alimentaire du sanglier en milieu forestier de plaine agricole. Faune Sauvage 273:20-27.
Brooks, S. P., and A. Gelman. 1998. General methods for monitoring convergence of iterative simulations. Journal of Computational and Graphical Statistics 7:434-455.
Caignard, T., A. Kremer, C. Firmat, M. Nicolas, S. Venner, and S. Delzon. 2017. Increasing spring temperatures favor oak seed production in temperate areas. Scientific Reports 7:8555.
Caswell, H. 2001. Matrix population models. Second edition. Sinauer, Sunderland, Massachusetts, USA.
Chuine, I., M. Bonhomme, J. M. Legave, I. García de Cortázar-Atauri, G. Charrier, A. Lacointe, and T. Améglio. 2016. Can phenological models predict tree phenology accurately in the future? The unrevealed hurdle of endodormancy break. Global Change Biology 22:3444-3460.
Cutini, A., F. Chianucci, R. Chirichella, E. Donaggio, L. Mattioli, and M. Apollonio. 2013. Mast seeding in deciduous forests of the northern Apennines (Italy) and its influence on wild boar population dynamics. Annals of Forest Science 70:493-502.
De Cáceres, M., N. Martin-StPaul, M. Turco, A. Cabon, and V. Granda. 2018. Estimating daily meteorological data and downscaling climate models over landscapes. Environmental Modelling & Software 108:186-196.
Duputié, A., A. Rutschmann, O. Ronce, and I. Chuine. 2015. Phenological plasticity will not help all species adapt to climate change. Global Change Biology 21:3062-3073.
Engen, S., B. E. Saether, K. B. Armitage, D. T. Blumstein, T. H. Clutton-Brock, F. S. Dobson, M. Festa-Bianchet, M. K. Oli, and A. Ozgul. 2013. Estimating the effect of temporally autocorrelated environments on the demography of density-independent age-structured populations. Methods in Ecology and Evolution 4:573-584.
Ergon, T., X. Lambin, and N. C. Stenseth. 2001. Life-history traits of voles in a fluctuating population respond to the immediate environment. Nature 411:1043.
Focardi, S., J. M. Gaillard, F. Ronchi, and S. Rossi. 2008. Survival of wild boars in a variable environment: unexpected life-history variation in an unusual ungulate. Journal of Mammalogy 89:1113-1123.
Frauendorf, M., F. Gethöffer, U. Siebert, and O. Keuling. 2016. The influence of environmental and physiological factors on the litter size of wild boar (Sus scrofa) in an agriculture dominated area in Germany. Science of the Total Environment 541:877-882.
Gaillard, J. M., A. J. Mark Hewison, F. Klein, F. Plard, M. Douhard, R. Davison, and C. Bonenfant. 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.
Gamelon, M., M. Douhard, E. Baubet, O. Gimenez, S. Brandt, and J. M. Gaillard. 2013. Fluctuating food resources influence developmental plasticity in wild boar. Biology Letters 9:20130419.
Gamelon, M., S. Focardi, E. Baubet, S. Brandt, B. Franzetti, F. Ronchi, S. Venner, B.-E. Saether, and J. M. Gaillard. 2017a. Reproductive allocation in pulsed-resource environments: a comparative study in two populations of wild boar. Oecologia 183:1065-1076.
Gamelon, M., et al. 2017b. Interactions between demography and environmental effects are important determinants of population dynamics. Science Advances 3:e1602298.
Gamelon, M., J. M. Gaillard, S. Servanty, O. Gimenez, C. Toïgo, E. Baubet, F. Klein, and J. D. Lebreton. 2012. Making use of harvest information to examine alternative management scenarios: a body weight-structured model for wild boar. Journal of Applied Ecology 49:833-841.
Garca-Mozo, H., P. J. Hidlago, C. Galn, M. T. Gmez-Casero, and E. Domnguez. 2001. Catkin frost damage in Mediterranean cork-oak (Quercus suber L.). Israel Journal of Plant Sciences 49:42-47.
Gauthier, G., G. Péron, J.-D. Lebreton, P. Grenier, and L. van Oudenhove. 2016. Partitioning prediction uncertainty in climate-dependent population models. Proceedings of the Royal Society B 283:20162353.
Gea-Izquierdo, G., I. Cañellas, and G. Montero. 2006. Acorn production in Spanish holm oak woodlands. Forest Systems 15:339-354.
Geisser, H., and H. U. Reyer. 2005. The influence of food and temperature on population density of wild boar Sus scrofa in the Thurgau (Switzerland). Journal of Zoology 267:89-96.
Groot Bruinderink, G. W. T. A., E. Hazebroek, and H. van der Voot. 2009. Diet and condition of wild boar, Sus scrofa, without supplementary feeding. Journal of Zoology 233:631-648.
Hansen, B. B., et al. 2019. More frequent extreme climate events stabilize reindeer population dynamics. Nature Communications 10:1616.
Hunter, C. M., H. Caswell, M. C. Runge, E. V. Regehr, S. C. Amstrup, and I. Stirling. 2010. Climate change threatens polar bear populations: a stochastic demographic analysis. Ecology 91:2883-2897.
IPCC. 2013. Climate change 2013: the physical science basis. Pages 1535 in T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, editors. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.
Jenouvrier, S. 2013. Impacts of climate change on avian populations. Global Change Biology 19:2036-2057.
Jenouvrier, S., H. Caswell, C. Barbraud, M. Holland, J. Strœve, and H. Weimerskirch. 2009. Demographic models and IPCC climate projections predict the decline of an emperor penguin population. Proceedings of the National Academy of Sciences USA 106:1844-1847.
Jenouvrier, S., M. Holland, J. Stroeve, C. Barbraud, H. Weimerskirch, M. Serreze, and H. Caswell. 2012. Effects of climate change on an emperor penguin population: analysis of coupled demographic and climate models. Global Change Biology 18:2756-2770.
Jenouvrier, S., M. Holland, J. Stroeve, M. Serreze, C. Barbraud, H. Weimerskirch, and H. Caswell. 2014. Projected continent-wide declines of the emperor penguin under climate change. Nature Climate Change 4:715.
Jones, C. G., R. S. Ostfeld, M. P. Richard, E. M. Schauber, and J. O. Wolff. 1998. Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 279:1023-1026.
Kelly, D. 1994. The evolutionary ecology of mast seeding. Trends in Ecology & Evolution 9:465-470.
Kelly, D., and V. L. Sork. 2002. Mast seeding in perennial plants: Why, how, where? Annual Review of Ecology and Systematics 33:427-447.
Koenig, W. D., R. L. Mumme, W. J. Carmen, and M. T. Stanback. 1994. Acorn production by oaks in central coastal California: variation within and among years. Ecology 75:99-109.
Liebhold, A., V. Sork, M. Peltonen, W. Koenig, O. N. Bjørnstad, R. Westfall, J. Elkinton, and J. M. Knops. 2004. Within-population spatial synchrony in mast seeding of North American oaks. Oikos 104:156-164.
Malmsten, A., G. Jansson, N. Lundeheim, and A. M. Dalin. 2017. The reproductive pattern and potential of free ranging female wild boars (Sus scrofa) in Sweden. Acta Veterinaria Scandinavica 59:52.
Massei, G., P. V. Genov, and B. W. Staines. 1996. Diet, food availability and reproduction of wild boar in a Mediterranean coastal area. Acta Theriologica 41:307-320.
Melis, C., P. A. Szafrańska, B. Jędrzejewska, and K. Bartoń. 2006. Biogeographical variation in the population density of wild boar (Sus scrofa) in western Eurasia. Journal of Biogeography 33:803-811.
Metcalf, C. J. E., and D. N. Koons. 2007. Environmental uncertainty, autocorrelation and the evolution of survival. Proceedings of the Royal Society B 274:2153-2160.
Ostfeld, R. S., and F. Keesing. 2000. Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends in Ecology & Evolution 15:232-237.
Paniw, M., A. Ozgul, and R. Salguero-Gómez. 2018. Interactive life-history traits predict sensitivity of plants and animals to temporal autocorrelation. Ecology Letters 21:275-286.
Parmesan, C., and G. Yohe. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37.
Pearse, I. S., W. D. Koenig, and D. Kelly. 2016. Mechanisms of mast seeding: resources, weather, cues, and selection. New Phytologist 212:546-562.
Peery, M. Z., R. J. Gutiérrez, R. Kirby, O. E. LeDee, and W. LaHaye. 2012. Climate change and spotted owls: potentially contrasting responses in the Southwestern United States. Global Change Biology 18:865-880.
Plummer, M. 2003. JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. Pages 20-22 in K. Hornik, F. Leisch, and A. Zeileis, editors. Proceedings of the 3rd International Workshop on Distributed Statistical. Technische UniversitätWien, Vienna, Austria.
Plummer, M. 2016. Rjags: Bayesian graphical models using MCMC. https://rdrr.io/cran/rjags/
R Development Core Team. 2017. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org
Root, T. L., J. T. Price, K. R. Hall, S. H. Schneider, C. Rosenzweig, and J. A. Pounds. 2003. Fingerprints of global warming on wild animals and plants. Nature 421:57-60.
Ruf, T., J. Fietz, W. Schlund, and C. Bieber. 2006. High survival in poor years: life history tactics adapted to mast seeding in the edible dormouse. Ecology 87:372-381.
Schermer, É., et al. 2019. Pollen limitation as a main driver of fruiting dynamics in oak populations. Ecology Letters 22:98-107.
Schermer, É., M. C. Bel-Venner, J. M. Gaillard, S. Dray, V. Boulanger, I. Le Roncé, G. Olivier, I. Chuine, S. Delzon, and S. Venner. 2020. Flower phenology as a disruptor of the fruiting dynamics in temperate oak species. New Phytologist 225:1181-1192.
Schley, L., and T. J. Roper. 2003. Diet of wild boar Sus scrofa in Western Europe, with particular reference to consumption of agricultural crops. Mammal Review 33:43-56.
Schmidt, K. A. 2003. Linking frequencies of acorn masting in temperate forests to long-term population growth rates in a songbird: the veery (Catharus fuscescens). Oikos 103:548-558.
Schmidt, K. A., and R. S. Ostfeld. 2008. Numerical and behavioral effects within a pulse-driven system: consequences for shared prey. Ecology 89:635-646.
Servanty, S., R. Choquet, É. Baubet, S. Brandt, J. M. Gaillard, M. Schaub, C. Toïgo, J.-D. Lebreton, M. Buoro, and O. Gimenez. 2010. Assessing whether mortality is additive using marked animals: a Bayesian state-space modeling approach. Ecology 91:1916-1923.
Servanty, S., J. M. Gaillard, D. Allainé, S. Brandt, and E. Baubet. 2007. Litter size and fetal sex ratio adjustment in a highly polytocous species: the wild boar. Behavioral Ecology 18:427-432.
Servanty, S., J. M. Gaillard, T. Toïgo, S. Brandt, and E. Baubet. 2009. Pulsed resources and climate-induced variation in the reproductive traits of wild boar under high hunting pressure. Journal of Animal Ecology 78:1278-1290.
Silvertown, J. W. 1980. The evolutionary ecology of mast seeding in trees. Biological Journal of the Linnean Society 14:235-250.
Tuljapurkar, S., and C. V. Haridas. 2006. Temporal autocorrelation and stochastic population growth. Ecology Letters 9:327-337.
Vehtari, A., A. Gelman, and J. Gabry. 2017. Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Statistics and Computing 27:1413-1432.
Vetter, S. G., T. Ruf, C. Bieber, and W. Arnold. 2015. What is a mild winter? Regional differences in within-species responses to climate change. PLoS ONE 10:e0132178.
Yang, L. H., J. L. Bastow, K. O. Spence, and A. N. Wright. 2008. What can we learn from resource pulses. Ecology 89:621-634.