Abstract
Climate warming and biological invasions by alien species are two key factors threatening the world’s biodiversity. To date, their impact has largely been studied independently, and knowledge on whether climate warming will promote invasions relies strongly on bioclimatic models. We therefore set up a study to experimentally compare responses to warming in native and alien plant species. Ten congeneric species pairs were exposed to ambient and elevated temperature (+3°C) in sunlit, climate-controlled chambers, under optimal water and nutrient supply to avoid interaction with other factors. All species pairs combined, total plant biomass reacted differently to warming in alien versus native species, which could be traced to significantly different root responses. On average, native species became less productive in the warmer climate, whereas their alien counterparts showed no response. The three alien species with the strongest warming response (Lathyrus latifolius, Cerastium tomentosum and Artemisia verlotiorum) are currently non-invasive but all originate from regions with a warmer climate. Still, other alien species that also originate from warmer regions became less or remained equally productive. Structural or ecophysiological acclimation to warming was largely absent, both in native and alien species, apart from light-saturated photosynthetic rate, where warming tended to restrain the native but not the alien species. A difference in the capacity to acclimate photosynthetic rates to the new climate may therefore have caused the contrasting biomass response. Future experiments are needed to ascertain whether climate warming can effectively tip the balance between native and alien competitors.
Similar content being viewed by others
References
Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspect Plant Ecol 3:52–66
Apple ME, Olszyk DM, Ormrod DP, Lewis J, Southworth D, Tingey DT (2000) Morphology and stomatal function of Douglas fir needles exposed to climate change: elevated CO2 and temperature. Int J Plant Sci 161:127–132
Atkin OK, Edwards EJ, Loveys BR (2000) Response of root respiration to changes in temperature and its relevance to global warming. New Phytol 147:141–154
Baguis P, Roulin E, Willems P, Ntegeka V (2009) Climate change scenarios for precipitation and potential evapotranspiration over central Belgium. Theor Appl Climatol. doi:10.1007/s00704-009-0146-5
Barnes BV, Zak DR, Denton SR, Spurr SH (1998) Forest ecology, 4th edn. John Wiley, New York
Callaway RM, DeLucia EH, Thomas EM, Schlesinger WH (1994) Compensatory responses of CO2 exchange and biomass allocation and their effects on the relative growth rate of ponderosa pine in different CO2 and temperature regimes. Oecologia 98:159–166
Chown SL, Slabber S, McGeoch MA, Janion C, Leinaas HP (2007) Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proc R Soc B Biol Sci 274:2531–2537
Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restorations. Annu Rev Ecol Syst 34:183–211
De Boeck HJ, Lemmens CMHM, Zavalloni C, Gielen B, Malchair S, Carnol M, Merckx R, Van den Berge J, Ceulemans R, Nijs I (2008) Biomass production in experimental grasslands of different species richness during three years of climate warming. Biogeosciences 5:585–894
Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139
Durand LZ, Goldstein G (2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126:345–354
Dury SJ, Good JEG, Perrins CM, Buse A, Kaye T (1998) The effects of increasing CO2 and temperature on oak leaf palatability and the implications for herbivorous insects. Glob Chang Biol 4:55–61
Edwards EJ, Benham DG, Marland LA, Fitter AH (2004) Root production is determined by radiation flux in a temperate grassland community. Glob Chang Biol 10:209–227
Ellenbergh H, Weber HE, Düll R, Writh V, Werner W, Pauliβen D (1992) Zeigerwerte von Pflanzen in Mitteleuropa. Scripta Geobotanica 18:1–258
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Gielen B, Naudts K, D’Haese D, Lemmens CMHM, De Boeck HJ, Biebaut E, Serneels R, Valcke R, Nijs I, Ceulemans R (2007) Effects of climate warming and species richness on photochemistry of grasslands. Physiol Plantarum 131:251–262
Goodwin BJ, McAllistar AJ, Fahrig L (1999) Predicting invasiveness of plant species based on biological information. Conserv Biol 13:422–426
Gritti ES, Smith B, Sykes MT (2006) Vulnerability of Mediterranean Basin ecosystems to climate change and invasion by exotic plant species. J Biogeogr 33:145–157
Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC, Harris CJ (2005) Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett 8:1066–1074
Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conserv Biol 22:534–543
Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. J Exp Bot 57:291–302
IPCC (2007) Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Contribution of working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Ishikawa K, Onoda Y, Hikosaka K (2007) Intraspecific variation in temperature dependence of gas exchange characteristics among Plantago asiatica ecotypes from different temperature regimes. New Phytol 176:356–364
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
Lake JC, Leishman MR (2004) Invasion success of exotic plants in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biol Conserv 117:215–226
Larcher W (2003) Physiological plant ecology, 4th edn. Springer, Berlin
Lemmens CMHM, De Boeck HJ, Gielen B, Bossuyt H, Malchair S, Carnol M, Merckx R, Nijs I, Ceulemans R (2006) End-of-season effects of elevated temperature on ecophysiological processes of grassland species at different species richness levels. Environ Exp Bot 56:245–254
Levy PE, Cannell MGR, Friend AD (2004) Modeling the impact of future changes in climate, CO2 concentration and land use on natural ecosystems and the terrestrial carbon sink. Glob Environ Chang 14:21–30
Llorens L, Penuelas J, Estiarte M (2003) Ecophysiological responses of two Mediterranean shrubs, Erica multiflora and Globularia alypum, to experimentally drier and warmer conditions. Physiol Plantarum 119:231–243
Llorens L, Penuelas J, Beier C, Emmett B, Estiarte M, Tietema A (2004) Effects of an experimental increase of temperature and drought on the photosynthetic performance of two ericaceous shrubs species along a North-South European gradient. Ecosystems 7:613–624
Loik ME, Redar SP, Harte J (2000) Photosynthetic responses to a climate-warming manipulation for contrasting meadow species in the Rocky Mountains, Colorado, USA. Funct Ecol 14:166–175
Luo YQ, Wan SQ, Hui DF, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–625
Maron JL, Elmendorf SC, Montserrat V (2007) Contrasting plant physiological adaptation to climate in the native and introduced range of Hypericum perforatum. Evolution 61:1912–1924
McDougall KL, Morgan JW, Walsh NG, Williams RJ (2005) Plant invasions in treeless vegetation of the Australian Alps. Perspect Plant Ecol 7:159–171
McDowell SCL (2002) Photosynthetic characteristics of invasive and non-invasive species of Rubus (Rosaceae). Am J Bot 89:1431–1438
Milberg P, Lamont BB, Pérez-Férnandez MA (1999) Survival and growth of native and exotic composites in response to a nutrient gradient. Plant Ecol 145:125–132
Niu S, Li Z, Xia J, Han Y, Wu M, Wan S (2008) Climatic warming changes plant photosynthesis and its temperature dependence in a temperate steppe of northern China. Environ Exp Bot 63:91–101
Norby RJ, Luo Y (2004) Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. New Phytol 162:281–293
Patterson DT (1995) Weeds in a changing climate. Weed Sci 43:685–700
Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Glob Ecol Biogeogr 12:361–371
Peterson AT, Stewart A, Mohamed KI, Araujo MB (2008) Shifting global invasive potential of European plants with climate change. Plose One 3(6):e2441
Pyke CR, Thomas R, Porter RD, Hellemann JJ, Dukes JS, Lodge DM, Chavarria G (2008) Current practices and future opportunities for policy on climate change and invasive species. Conserv Biol 22:585–592
Pysek P, Richardson DM (2006) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 97–125
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993
Richardson DM, Pysek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geog 30:409–431
Roy J, Navas ML, Sonié L (1991) Invasion by annual bromegrasses: a case study challenging in the homoclime approach to invasion. In: Groves RH, Di Castri F (eds) Biogeography of Mediterranean invasions. Cambridge University Press, Cambridge, pp 207–224
Roy BA, Gusewell S, Harte J (2004) Response of plant pathogens and herbivores to a warming experiment. Ecology 85:2570–2581
Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562
Saleska SR, Harte J, Torn MS (1999) The effect of experimental ecosystem warming on CO2 fluxes in a montane meadow. Glob Chang Biol 5:125–141
Sexton JP, McKay JK, Sala A (2002) Plasticity and genetic diversity may allow saltcedar to invade cold climates in North America. Ecol Appl 12:1652–1660
Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci USA 99:15497–15500
Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82:328–343
Sutherst R (2000) Climate variability, seasonal forecasting and invertebrate pests—the need for a synoptic view. In: Hammer GL, Nichols N, Mitchell C (eds) Applications of seasonal climate forecasting in agricultural and natural ecosystems. Kluwer, Boston, pp 381–397
Thuiller W, Richardson DM, Pysek P, Midgley GF, Hughes GO, Rouget M (2005) Niche-based modeling as a tool for predicting the risk of alien plant invasions at a global scale. Glob Chang Biol 11:2234–2250
Verloove F (2002) Ingeburgerde plantensoorten in Vlaanderen. Mededeling van het Instituut voor Natuurbehoud 20, Brussels
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:359–395
Wan S, Norby RJ, Pregitzer KS, Ledford J, O’Neill EG (2004) CO2 enrichment and warming of the atmosphere enhance both productivity and mortality of maple tree fine roots. New Phytol 162:437–446
Ward NL, Masters GJ (2007) Linking climate change and species invasion: an illustration using insect herbivores. Glob Chang Biol 13:1605–1615
White TA, Campbell BD, Kemp PD, Hunt CL (2000) Sensitivity of three grassland communities to simulated extreme temperature and rainfall events. Glob Chang Biol 6:671–684
Willis SG, Hulme PE (2002) Does temperature limit the invasion of Impatiens glandulifera and Heracleum mantegazzianum in the UK? Funt Ecol 16:530–539
Wythers KR, Reich PB, Tjoelker MG, Bolstad PB (2005) Foliar respiration acclimation to temperature and temperature variable Q10 alter ecosystem carbon balance. Glob Chang Biol 11:435–449
Acknowledgments
We thank F. Kockelbergh and N. Calluy for technical assistance, professor of biostatistics S. Van Dongen for statistical advice and H. De Boeck for comments on the manuscript. This research was financed by the Belgian Science Policy (framed within the ALIEN IMPACT project).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Verlinden, M., Nijs, I. Alien plant species favoured over congeneric natives under experimental climate warming in temperate Belgian climate. Biol Invasions 12, 2777–2787 (2010). https://doi.org/10.1007/s10530-009-9683-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-009-9683-1