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Synergistic interactions of CO2 enrichment and nitrogen deposition promote growth and ecophysiological advantages of invading Eupatorium adenophorum in Southwest China

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Abstract

Global environmental change and ongoing biological invasions are the two prominent ecological issues threatening biodiversity worldwide, and investigations of their interaction will aid to predict plant invasions and inform better management strategies in the future. In this study, invasive Eupatorium adenophorum and native congener E. stoechadosmum were compared at ambient and elevated atmospheric carbon dioxide (CO2) concentrations combined with three levels of nitrogen (N; reduced, control and increased) in terms of growth, energy gain, and cost. Compared with E. stoechadosmum, E. adenophorum adopted a quicker-return energy-use strategy, i.e. higher photosynthetic energy-use efficiency and shorter payback time. Lower leaf mass per area may be a pivotal trait for the invader, which contributed to an increased N allocation to Rubisco at the expense of cell walls and therefore to higher photosynthetic energy gain. CO2 enrichment and N deposition synergistically promoted plant growth and influenced some related ecophysiological traits, and the synergistic effects were greater for the invader than for the native congener. Reducing N availability by applying sugar eliminated the advantages of the invader over its native congener at both CO2 levels. Our results indicate that CO2 enrichment and N deposition may exacerbate E. adenophorum’s invasion in the future, and manipulating environmental resources such as N availability may be a feasible tool for managing invasion impacts of E. adenophorum.

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Abbreviations

A growth :

Photosynthetic rate measured at growth CO2 concentration

CC:

Construction cost

Cell wall-N:

Proportion of leaf N allocated to cell walls

LMA:

Leaf mass per area

PEUE:

Photosynthetic energy-use efficiency

Rubisco-N:

Proportion of leaf N allocated to Rubisco

References

  • Albert KR, Ro-Poulsen H, Mikkelsen TN, Michelsen A, van der Linden L, Beier C (2011) Interactive effects of elevated CO2, warming, and drought on photosynthesis of Deschampsia flexuosa in a temperate heath ecosystem. J Exp Bot 12:4253–4266

    Article  Google Scholar 

  • Baruch Z, Goldstein G (1999) Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 121:183–192

    Article  Google Scholar 

  • Bleier JS, Jackson RD (2007) Manipulating the quantity, quality, and manner of C addition to reduce soil inorganic N and increase C4:C3 grass biomass. Rest Ecol 15:688–695

    Article  Google Scholar 

  • Blumenthal DM, Jordan NR, Russelle MP (2003) Soil carbon addition controls weeds and facilitates prairie restoration. Ecol Appl 13:605–615

    Article  Google Scholar 

  • Bradford MA, Schumacher HB, Catovsky S, Eggers T, Newingtion JE, Tordoff GM (2007) Impacts of invasive plant species on riparian plant assemblages: interactions with elevated atmospheric carbon dioxide and nitrogen deposition. Oecologia 152:791–803

    Article  PubMed  Google Scholar 

  • Corbin JD, D’Antonio CM (2004) Can carbon addition increase competitiveness of native grasses? A case study from California. Restor Ecol 12:36–43

    Article  Google Scholar 

  • Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211

    Article  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Article  Google Scholar 

  • Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139

    Article  PubMed  Google Scholar 

  • Dukes JS, Chiariello NR, Loarie SR, Field C (2011) Strong response of an invasive plant species (Centaurea solstitialis L.) to global environmental changes. Ecol Appl 21:1887–1894

    Article  PubMed  Google Scholar 

  • Feng Y-L, Auge H, Ebeling SK (2007) Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 153:501–510

    Article  PubMed  Google Scholar 

  • Feng Y-L, Fu G-L, Zheng Y-L (2008) Specific leaf area relates to the differences in leaf construction cost, photosynthesis, nitrogen allocation and use efficiencies between invasive and noninvasive alien congeners. Planta 228:383–390

    Article  PubMed  CAS  Google Scholar 

  • Feng Y-L, Lei Y-B, Wang R-F, Callaway RM, Valiente-Banuet A, Inderjit, Li Y-P, Zheng Y-L (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci USA 106:1853–1856

    Article  PubMed  CAS  Google Scholar 

  • Feng Y-L, Li Y-P, Wang R-F, Callaway RM, Valiente-Banuet A, Inderjit (2011) A quicker return energy-use strategy by populations of a subtropical invader in the non-native range: a potential mechanism for the evolution of increased competitive ability. J Ecol 99:1116–1123

    Article  Google Scholar 

  • Funk J, Vitousek P (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081

    Article  PubMed  CAS  Google Scholar 

  • Gill RA, Anderson LJ, Polley HW, Johnson HB, Jackson RB (2006) Potential nitrogen constraints on soil carbon sequestration under low and elevated atmospheric CO2. Ecology 87:41–52

    Article  PubMed  Google Scholar 

  • Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–1191

    Article  CAS  Google Scholar 

  • Hattenschwiler S, Koner C (2003) Does elevated CO2 facilitate naturalization of the non-indigenous Prunus laurocerasus in Swiss temperate forests? Funct Ecol 17:778–785

    Article  Google Scholar 

  • He W-M, Yu G-L, Sun Z-K (2011) Nitrogen deposition enhances Bromus tectorum invasion: biogeographic differences in growth and competitive ability between China and North America. Ecography 34:1059–1066

    Article  Google Scholar 

  • IPCC (2007) Summary for policy makers. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Cambridge University Press, Cambridge

    Google Scholar 

  • Langley JA, Megonigal JP (2010) Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature 406:96–99

    Article  Google Scholar 

  • Lee TD, Tjoelker MG, Reich PB, Russelle M (2003) Contrasting growth response of an N2-fixing and non-fixing forb to elevated CO2: dependence on soil N supply. Plant Soil 255:475–486

    Article  CAS  Google Scholar 

  • Lei Y-B, Feng Y-L, Zheng Y-L, Wang R-F, Gong H-D, Zhang Y-P (2011) Innate and evolutionary advantages of invasive Eupatorium adenophorum over native E. japonicum under ambient and doubled atmospheric CO2 concentrations. Biol Invasions 13:2703–2714

    Article  Google Scholar 

  • Leishman MR, Thomson VP, Cooke J (2010) Native and exotic invasive plants have fundamental similar carbon capture strategies. J Ecol 98:28–42

    Article  CAS  Google Scholar 

  • Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739

    Article  Google Scholar 

  • Manea A, Leishman MR (2011) Competitive interactions between native and invasive exotic plant species are altered under elevated carbon dioxide. Oecologia 165:735–744

    Article  PubMed  Google Scholar 

  • McDowell SCL (2002) Photosynthetic characteristics of invasive and noninvasive species of Rubus (Rosaceae). Am J Bot 89:1431–1438

    Article  PubMed  Google Scholar 

  • Nagel JM, Huxman TE, Griffin KL, Smith SD (2004) CO2 Enrichment reduces the energetic cost of biomass construction in an invasive desert grass. Ecology 85:100–106

    Article  Google Scholar 

  • Norby RJ, Warren JM, Iversen CM, Garten CT, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci USA 107:19368–19373

    Article  PubMed  CAS  Google Scholar 

  • Ordonez A, Wright IJ, Olff H (2010) Functional differences between native and alien species: a global-scale comparison. Funct Ecol 24:1353–1361

    Article  Google Scholar 

  • Osunkoya OO, Bayliss D, Panetta FD, Vivian-Smith G (2010) Leaf trait co-ordination in relation to construction cost, carbon gain and resource-use efficiency in exotic invasive and native woody vine species. Ann Bot (London) 106:371–380

    Article  CAS  Google Scholar 

  • Penuelas J, Sardans J, Llusià J, Owen SM, Carnicer J, Giambelluca TW, Rezende EL, Waite M, Niinemets U (2010) Faster returns on “leaf economics” and different biogeochemical niche in invasive compared with native plant species. Global Change Biol 16:2171–2185

    Article  Google Scholar 

  • Perry LG, Blumenthal DM, Monaco TA, Paschke MW, Redente EF (2010) Immobilizing nitrogen to control plant invasion. Oecologia 163:13–24

    Article  PubMed  Google Scholar 

  • Poorter H, Pepin S, Rijkers T, De Jong Y, Evans JR, Körner C (2006) Construction costs, chemical composition and payback time of high- and low-irradiance leaves. J Exp Bot 57:355–371

    Article  PubMed  CAS  Google Scholar 

  • Pyšek P, Richardson DM, Pergl J, Jarošík V, Sixtová Z, Weber E (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23:237–244

    Article  PubMed  Google Scholar 

  • Raizada P, Singh A, Rajhubanshi AS (2009) Comparative response of seedlings of selected native dry tropical and alien invasive species to CO2 enrichment. J Plant Ecol 2:69–75

    Article  Google Scholar 

  • Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925

    Article  PubMed  CAS  Google Scholar 

  • Sasek TW, Strain BR (1991) Effects of CO2 enrichment on the growth and morphology of a native and an introduced honeysuckle vine. Am J Bot 78:69–75

    Article  CAS  Google Scholar 

  • Scharfy D, Funk A, Venterink HO, Güsewell S (2011) Invasive forbs differ functionally from native graminoids, but are similar to native forbs. New Phytol 189:818–828

    Article  PubMed  Google Scholar 

  • Shen X-Y, Peng S-L, Chen B-M, Pang J-X, Chen L-Y, Xu H-M, Hou Y-P (2011) Do higher resource capture ability and utilization efficiency facilitate the successful invasion of native plants? Biol Invasions 13:869–881

    Article  Google Scholar 

  • Smith SD, Huxman TE, Zitzer SF, Charlet TN, Housman DC, Coleman JS, Fenstermaker LK, Seemann JR, Nowak RS (2000) Elevated CO2 increases productivity and invasive species success in an arid ecosystem. Nature 408:79–82

    Article  PubMed  CAS  Google Scholar 

  • Song L-Y, Li C-H, Peng S-L (2010) Elevated CO2 increase energy-use efficiency of invasive Wedelia trilobata over its indigenous congener. Biol Invasions 12:1221–1230

    Article  Google Scholar 

  • Vilà M, Corbin JD, Dukes JS, Pino J, Smith SD (2007) Linking plant invasions to global environmental change. In: Canadell JJ, Pataki DE, Pitelka LF (eds) Terrestrial ecosystems in a changing world. The IGBP series. Springer, Berlin

    Google Scholar 

  • Wang R, Wang Y-Z (2006) Invasion dynamics and potential spread of the invasive alien plant species Ageratina adenophora (Asteraceae) in China. Divers Distrib 12:397–408

    Article  Google Scholar 

  • Williams K, Field CB, Mooney HA (1989) Relationships among leaf construction costs, leaf longevity, and light environment in rain-forest plants of the genus Piper. Am Nat 133:198–211

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  PubMed  CAS  Google Scholar 

  • Ye L-F, Fu X, Ge F (2011) Enhanced sensitivity to higher ozone in a pathogen-resistant tobacco cultivar. J Exp Bot 63:1341–1347

    Article  PubMed  Google Scholar 

  • Zhang L, Yang Y-X, Zhan X-Y, Zhang C-J, Zhou S-X, Wu D-X (2010) Responses of a dominant temperate grassland plant (Leymus chinensis) to elevated carbon dioxide and nitrogen addition in China. J Environ Qual 39:251–259

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to National Forest Ecosystem Research Station at Ailaoshan for logistic supports, Mr Jin-Hua Qi for assistances in measurements, Dr Jiao-lin Zhang and Dr Yong-jiang Zhang for helps in data analysis. This study was funded by the projects of Natural Science Foundation of China (30830027, 30900220), the Applied Basic Study Project of Yunnan Province (2009CD119).

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Authors and Affiliations

  1. Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, 666303, Yunnan, China

    Yan-bao Lei, Wei-bin Wang, Yu-long Feng, Yu-long Zheng & He-de Gong

  2. College of Bioscience and Biotechnology, Shenyang Agricultural University, Shenyang, 110866, Liaoning, China

    Yu-long Feng

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  1. Yan-bao Lei
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  2. Wei-bin Wang
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Correspondence to Yu-long Feng.

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Y. Lei and W. Wang contributed equally to this manuscript.

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Lei, Yb., Wang, Wb., Feng, Yl. et al. Synergistic interactions of CO2 enrichment and nitrogen deposition promote growth and ecophysiological advantages of invading Eupatorium adenophorum in Southwest China. Planta 236, 1205–1213 (2012). https://doi.org/10.1007/s00425-012-1678-y

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