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Elevated CO2 increases energy-use efficiency of invasive Wedelia trilobata over its indigenous congener

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Abstract

Increasing atmospheric CO2 concentration is regarded as an important factor facilitating plants invasions by stimulating invasive species growth. However, the physiological mechanisms by which invasive plants increase at the expense of existing native plants are poorly understood. Plant growth is always related to energy-use process including energy assimilation and expenditure, and thus examination of energetic properties could provide mechanistic insight into growth responses to increased CO2. The aims of this study were to examine the effect of rising CO2 on the growth and energetic properties of alien invasive species (Wedelia trilobata (L.) Hitchc.) and its native congener (Wedelia chinensis (Osbeck.) Merr.) in South China, and to determine if the specific energetic properties of invasive species at elevated CO2 favoring its growth. Elevated CO2 stimulated a greater increase in biomass production for invasive W. trilobata (58.9%) than for its indigenous congener (48.1%). Meanwhile, elevated CO2 altered the energetic properties differently upon species. For invasive W. trilobata, elevated CO2 significantly increased total energetic gain via photosynthetic activity (A total), but decreased energetic cost of biomass construction (CC), and thus enhanced photosynthetic energy-use efficiency (PEUE) by 85.3%. In contrast, the indigenous W. chinensis showed a slight increase in PEUE by 43.8%. Additionally, W. trilobata individuals grown in elevated CO2 increased energy allocation towards stems. Statistic analysis revealed significant associations between growth characteristics (relative growth rate and biomass) and energetic properties (CC and PEUE), suggesting the greater growth stimulation in invasive species could be partly explained by its specific energetic properties in elevated CO2 concentration. The invasive species showed a greater increase in energy-use efficiency under elevated CO2, which consequently facilitated its growth. It might be a physiological mechanism promoting success of invasion with ongoing increase in atmospheric CO2 concentration.

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References

  • Amthor JS, Mitchell RJ, Runion G, Rogers HH, Prior SA, Wood CW (1994) Energy content, construction cost and phytomass accumulation of Glycine max (L.) Merr. and Sorghum bicolor (L.) Moench grown in elevated CO2 in the field. New Phytol 128:443–450

    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 

  • Baruch Z, Gómez JA (1996) Dynamics of energy and nutrient concentration and construction cost in a native and two alien C4 grasses from two neotropical savannas. Plant Soil 181:175–184

    Article  CAS  Google Scholar 

  • Booker FL, Shafer SR, Wei C, Horton SJ (2000) Carbon dioxide enrichment and nitrogen fertilization effects on cotton (Gossypium hirsutum L.) plant residue chemistry and decomposition. Plant Soil 220:89–98

    Article  CAS  Google Scholar 

  • Bowes G (1993) Facing the inevitable: plants and increasing atmospheric CO2. Annu Rev Plant Physiol Plant Mol Biol 44:309–332

    Article  CAS  Google Scholar 

  • Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biol 4:43–54

    Article  Google Scholar 

  • Curtis P, Wang X (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313

    Article  Google Scholar 

  • Deng X, Ye WH, Feng HL, Yang QH, Cao HL, Xu KY, Zhang Y (2004) Gas exchange characteristics of the invasive species Mikania micrantha and its indigenous congener M. cordata (Asteraceae) in South China. Bot Bull Acad Sinica 45:213–220

    Google Scholar 

  • Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:35–139

    Article  Google Scholar 

  • Durand LZ, Goldstein G (2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126:345–354

    Article  Google Scholar 

  • Forseth IN, Innis AF (2004) Kudzu (Pueraria montana): history, physiology, and ecology combine to make a major ecosystem threat. Criti Rev Plant Sci 23:401–413

    Article  Google Scholar 

  • George K, Norby RJ, Hamilton JG, DeLucia EH (2003) Fine-root respiration in a loblolly pine and sweetgum forest growing in elevated CO2. New Phytol 160:511–522

    Article  Google Scholar 

  • Griffin KL (1994) Calorimetric estimates of CC and their use in ecological studies. Funct Ecol 8:551–562

    Article  Google Scholar 

  • Griffin KL, Winner WE, Strain BR (1996) Construction cost of loblolly and ponderosa pine leaves grown with varying carbon and nitrogen availability. Plant Cell Environ 19:729–738

    Article  Google Scholar 

  • IPCC (2007) Summary for policymakers. 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. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • IUCN (2001) 100 of the world’s worst invasive alien species. Invasive Species Specialist Group, Auckland

    Google Scholar 

  • Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:188–261

    Google Scholar 

  • Li ZY, Xie Y (2002) Invasive species in China (in Chinese). China Forest Publishing House, Beijing

    Google Scholar 

  • Liu JX, Li ZF (2005) Effects of CO2 concentrations increasing on photosynthetic physiological characteristics of Wedelia trilobata. Guihaia 25:477–480

    Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology global consequences and control. Ecol Appl 10:689–710

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Nagel JM, Griffin KL (2001) Construction cost and invasive potential: comparing Lythrum salcaria (Lythraceae) with co-occurring native species along pond banks. Am J Bot 88:2252–2258

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Nagel JM, Wang XZ, Lewis JD, Fung HA, Tissue DT, Griffin KL (2005) Atmospheric CO2 enrichment alters energy assimilation, investment and allocation in Xanthium strumarium. New Phytol 166:513–523

    Article  CAS  PubMed  Google Scholar 

  • Nie CR, Zeng RS, Luo SM, Li HS, Hong MQ, Cheng LQ (2004) Allelopathic potentials of Wedelia trilobata L. on rice. Acta Agron Sinica 30:942–946

    Google Scholar 

  • Pattison RR, Goldstein G, Ares A (1998) Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117:449–459

    Article  Google Scholar 

  • Penning de Vries FWT, Brunsting AHM, Van Laar HH (1974) Products, requirements and efficiency of biosynthesis: a quantitative approach. J Theor Biol 45:339–377

    Article  CAS  PubMed  Google Scholar 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of non-indigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Poorter H (1993) Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. Vegetatio 104(105):77–97

    Article  Google Scholar 

  • Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198

    Article  Google Scholar 

  • Poorter H, Villar R (1997) The fate of acquired carbon in plants: chemical composition and construction costs. In: Bazzaz FA, Grace J (eds) Plant resource allocation. Academic Press, San Diego, pp 39–72

    Chapter  Google Scholar 

  • Poorter H, Van Berkel Y, Baxter R, Hertog JD, Dijkstra P, Gifford RM, Griffin KL, Roumet C, Roy J, Wong SC (1997) The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species. Plant Cell Environ 20:472–482

    Article  CAS  Google Scholar 

  • Rogers HH, Prior SA, Runion GB, Mitchell RJ (1996) Root to shoot ratio of crops as influenced by CO2. Plant Soil 187:229–248

    Article  CAS  Google Scholar 

  • Salo LF (2005) Red brome (Bromus rubens subsp. madritensis) in North America: possible modes for early introductions, subsequent spread. Biol Invasions 7:165–180

    Article  Google Scholar 

  • Saralabai VC, Vicekanandan M, Suresh BR (1997) Plant responses to high CO2 concentration in the atmosphere. Photosynthetica 33:7–37

    Article  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 

  • 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  CAS  PubMed  Google Scholar 

  • Song LY, Ni GY, Chen BM, Peng SL (2007) Energetic cost of leaf construction in the invasive weed Mikania micrantha H.B.K. and its co-occurring species: implications for invasiveness. Bot Stud 48:331–338

    CAS  Google Scholar 

  • Song LY, Wu JR, Li CH, Li FR, Peng SL, Chen BM (2009) Different responses of invasive and native species to elevated CO2 concentration. Acta Oecol 35:128–135

    Article  Google Scholar 

  • Thaman RR (1999) Wedelia trilobata: daisy invader of the pacific islands. University of the South Pacific, Suva

    Google Scholar 

  • Vieira HS, Takahashi JA, Boaventura MAD (2001) Constituents from aerial pars of Wedelia paludosa. Fitoterapia 72:854–856

    Article  CAS  PubMed  Google Scholar 

  • Vilà M, Corbin JD, Dukes JS, Pino J, Smith SD (2006) Linking plant invasions to environmental change. In: Canadell JG, Pataki D, Pitelka L (eds) Terrestrial ecosystems in a changing world. Springer, Berlin, pp 93–102

    Google Scholar 

  • Villar R, Merino J (2001) Comparison of leaf construction costs in woody species with differing leaf life-spans in contrasting ecosystems. New Phytol 151:213–226

    Article  Google Scholar 

  • Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawaii: plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59:247–265

    Article  Google Scholar 

  • Weining C (2000) Differing selection in alternative competitive environments: shade-avoidance responses and germination timing. Evolution 54:124–136

    Google Scholar 

  • Weltzin JF, Belote RT, Sanders NJ (2003) Biological invaders in a greenhouse world: will elevated CO2 fuel plant invasions? Front Ecol Environ 1:146–153

    Google Scholar 

  • Williams K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734

    CAS  Google Scholar 

  • Wu YQ, Hu YJ (2004) Researches on photosynthetic characteristics of exotic plants Wedelia trilobata, Pharbitis nil and Ipomoea cairica. Acta Ecol Sinica 24:2334–2339

    Google Scholar 

  • Wu YQ, Hu YJ, Chen JN (2005a) Reproductive characteristics of alien plant Wedelia trilobata. Acta Scientiarum Naturalium Universitatis Sunyatseni 44:93–96

    Google Scholar 

  • Wu YQ, Hu YJ, Liao FL (2005b) Wedelia trilobata—a species from introduced to potential invasive. Guihaia 25:413–418

    Google Scholar 

  • Wullschleger SD, Norby RJ, Love JC, Runck C (1997) Energetic costs of tissue construction in yellow-poplar and white oak trees exposed to long-term CO2 Enrichment. Ann Bot 80:289–297

    Article  Google Scholar 

  • Zhang YH, Liu MF, Ling TJ, Wei XY (2004) Allelopathic sesquiterpene lactones from Wedelia trilobata. J Trop Subtrop Bot 12:533–537

    CAS  Google Scholar 

  • Ziska LH (2003) Evaluation of the growth response of six invasive species to past, present and future atmospheric carbon dioxide. J Exp Bot 54:395–404

    Article  CAS  PubMed  Google Scholar 

  • Ziska LH, Bunce JA (1997) Influence of increasing carbon dioxide concentration on the photosynthetic and growth stimulation of selected C4 crops and weeds. Photosynth Res 54:199–208

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Key Program of the Ministry of Education of China (704037), the Natural Science Foundation of Guangdong Province (8451063101000535) and China Postdoctoral Science Foundation (20080440766). We greatly appreciate Dr. Guang-Yan Ni (Zhongshan University) and both the two anonymous referees for their constructive comments and suggestions for the improvement of this manuscript.

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Correspondence to Shao-Lin Peng.

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Song, LY., Li, CH. & Peng, SL. Elevated CO2 increases energy-use efficiency of invasive Wedelia trilobata over its indigenous congener. Biol Invasions 12, 1221–1230 (2010). https://doi.org/10.1007/s10530-009-9541-1

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