Skip to main content
SpringerLink
Log in

Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species

  • Ecophysiology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The general-purpose genotype hypothesis and the hypothesis of the evolution of invasiveness predict that invasive species are characterized by particular traits that confer invasiveness. However, these traits are still not well-defined. In this study, ecophysiological traits of eight populations of the invasive shrub Buddleja davidii from a wide range of European locations and five co-occurring native woody species in Germany were compared in a common garden experiment. We hypothesized that the invader has higher resource capture ability and utilization efficiency than the natives. No differences were detected among the eight populations of B. davidii in any of the traits evaluated, indicating that the invader did not evolve during range expansion, thus providing support to the general-purpose genotype hypothesis. The invader showed significantly higher maximum electron transport rate, maximum carboxylation rate, carboxylation efficiency, light-saturated photosynthetic rate (P max) and photosynthetic nitrogen utilization efficiency (PNUE) than the five natives. Leaf nitrogen content was not significantly different between the invader and the natives, but the invader allocated more nitrogen to the photosynthetic machinery than the natives. The increased nitrogen content in the photosynthetic machinery resulted in a higher resource capture ability and utilization efficiency in the invader. At the same intercellular CO2 concentration, P max was significantly higher in the invader than in the natives, again confirming the importance of the higher nitrogen allocation to photosynthesis. The invader reduced metabolic cost by increasing the ratio of P max to dark respiration rate (R d), but it did not reduce carbon cost by increasing the specific leaf area and decreasing leaf construction cost. The higher nitrogen allocation to the photosynthetic machinery, P max, PNUE and P max/R d may facilitate B. davidii invasion, although studies involving a wide range of invasive species are needed to understand the generality of this pattern and to fully assess the ecological advantages afforded by these features.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

C B :

ratio of leaf chlorophyll to leaf nitrogen in light-harvesting components in mmol g−1

C C :

leaf chlorophyll concentration in mmol g−1

C i :

intercellular CO2 concentration in μmol mol−1

CC:

leaf construction cost in g dm−2

CE:

carboxylation efficiency

G s :

stomatal conductance in mol m−2 s−1

J max :

maximum electron transport rate in μmol m−2 s−1

J mc :

the potential rate of photosynthetic electron transport per unit cytochrome f in μmol μmol−1 s−1

K c :

the Michaelis–Menten constant of Rubisco for carboxylation in μmol mol−1

K o :

the Michaelis–Menten constant of Rubisco for oxidation in mmol mol−1

N A :

total leaf nitrogen content in g m−2

N M :

mass-based leaf nitrogen content in g g−1

N P :

nitrogen content in photosynthetic machinery in g m−2

O :

intercellular oxygen concentration in mmol mol−1

P B :

fraction of leaf nitrogen allocated to bioenergetics in g g−1

P C :

fraction of leaf nitrogen allocated to carboxylation in g g−1

P L :

fraction of leaf nitrogen allocated to light-harvesting components in g g−1

P max :

light-saturated photosynthetic rate in μmol m−2 s−1

P max-M :

mass-based light-saturated photosynthetic rate in μmol g−1 s−1

P max′:

light- and CO2-saturated photosynthetic rate in μmol m−2 s−1

P n :

net photosynthetic rate in μmol m−2 s−1

P T :

fraction of leaf nitrogen allocated to all components of photosynthetic machinery in g g−1

PNUE:

photosynthetic nitrogen utilization efficiency (P max/N A) in μmol g−1 s−1

PPFD:

photosynthetic photon flux density in μmol m−2 s−1

R d :

dark respiration rate in μmol m−2 s−1

RE:

respiration efficiency (P max/R d)

SLA:

specific leaf area in cm2 mg−1

V cmax :

maximum carboxylation rate in μmol m−2 s−1

V cr :

specific activity of Rubisco in μmol g−1 s−1

WUE:

water utilization efficiency (P max/G s) in μmol mol−1

Γ*:

CO2 compensation point in μmol mol−1

References

  • Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic, New York, pp 147–168

    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 

  • Bazzaz FA (1996) Plants in changing environments: linking physiological, population, and community ecology. Cambridge University Press, Cambridge

    Google Scholar 

  • Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24:253–259

    Article  CAS  Google Scholar 

  • Binggeli P (1998) An overview of invasive woody plants in the tropics (School of Agricultural and Forest Sciences Publication no. 13). University of Wales, Bangor, UK

  • Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive non-indigenous plants: a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11

    Article  PubMed  Google Scholar 

  • Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Diaz S (2000) Functional and societal consequences of changing biodiversity. Nature 405:234–242

    Article  PubMed  CAS  Google Scholar 

  • Chen S-P, Bai Y-F, Zhang L-X, Han X-G (2005) Comparing physiological responses of two dominant grass species to nitrogen addition in Xilin River Basin of China. Environ Exp Bot 53:65–75

    Article  Google Scholar 

  • Cornelissen JHC, Werger MJA, Castro-Díez P, van Rheenen JWA, Rowland AP (1997) Foliar nutrients in relation to growth, allocation and leaf traits in seedlings of a wide range of woody plant species and types. Oecologia 111:460–469

    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 

  • D’Antonio CM, Kark S (2002) Impacts and extent of biotic invasions in terrestrial ecosystems. Trends Ecol Evol 17:202–204

    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 

  • Delucia EH, Schlesinger WH (1991) Resource-use efficiency and drought tolerance in adjacent great basin and Sierran plants. Ecology 72:51–58

    Article  Google Scholar 

  • DeWalt SJ, Denslow JS, Hamrick JL (2004) Biomass allocation, growth, and photosynthesis of genotypes from native and introduced ranges of the tropical shrub Clidemia hirta. Oecologia 138:521–531

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Ewe SML, Sternberg LSL (2003) Seasonal exchange characteristics of Schinus terebinthifolius in a native and disturbed upland community in Everglade national park, Florida. For Ecol Manage 179:27–36

    Article  Google Scholar 

  • Farnsworth EJ, Meyerson LA (2003) Comparative ecophysiology of four wetland plant species along continuum of invasiveness. Wetlands 23:750–762

    Article  Google Scholar 

  • Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 11:191–210

    Google Scholar 

  • Feng Y-L, Wang J-F, Sang W-G (2007) Irradiance acclimation, capture ability, and efficiency in invasive and non-invasive alien plant species. Photosynthetica 45:245–253

    Article  Google Scholar 

  • Harrington RA, Brown BJ, Reich PB (1989) Ecophysiology of exotic and native shrubs in southern Wisconsin I. Relationship of leaf characteristics, resource availability, and phenology to seasonal patterns of carbon gain. Oecologia 80:356–367

    Article  Google Scholar 

  • He J-S, Fang J-Y, Wang Z-H, Guo D-L, Flynn AFB, Geng Z (2006) Stoichiometry and large-scale patterns of leaf carbon and nitrogen in the grassland biomes of China. Oecologia 149:115–122

    Article  PubMed  Google Scholar 

  • Hill JP, Germino MJ, Wraith JM, Olson BE, Swan MB (2006) Advantages in water relations contribute to greater photosynthesis in Centaurea maculosa compared with established grasses. Int J Plant Sci 167:269–277

    Article  Google Scholar 

  • Humphries RN, Guarino L (1987) Soil nitrogen and the growth of birch and buddleia in abandoned chalk quarries. Reclam Reveg Res 6:55–61

    Google Scholar 

  • Humphries RN, Jordan MA, Guarino L (1982) The effect of water stress on the mortality of Betula pendula Roth. and Buddleja davidii Franch seedlings. Plant Soil 64:273–276

    Article  Google Scholar 

  • Laisk A (1977) Kinetics photosynthesis and photorespiration in C3 plants. Nauka, Moscow

    Google Scholar 

  • Lambrinos JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology 85:2061–2070

    Article  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochem Soc Trans 603:591–592

    Google Scholar 

  • Lodge DM (1993) Biological invasion: lessons for ecology. Trends Ecol Evol 8:133–136

    Article  Google Scholar 

  • Loustau D, Beahim M, Gaudillère JP, Dreyer E (1999) Photosynthetic responses to phosphorous nutrition in two-year-old maritime pine seedlings. Tree Physiol 19:707–715

    PubMed  Google Scholar 

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

    Google Scholar 

  • McKay JK, Bishop JG, Lin J-Z, Richards JH, Sala A, Mitchell-Olds T (2001) Local adaptation across a climatic gradient despite small effective population size in the rare sapphire rockcress. Proc R Soc Lond B Biol Sci 268:1715–1721

    Article  CAS  Google Scholar 

  • Metzger MJ, Bunce RGH, Jongman RHG, Mücher CA, Watkins JW (2005) A climatic stratification of the environment of Europe. Glob Ecol Biogeogr 14:549–563

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell Environ 20:845–866

    Article  Google Scholar 

  • Niinemets Ü, Olevikull, Tenhunen JD (1998) An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance. Tree Physiol 18:681–696

    PubMed  Google Scholar 

  • Niinemets Ü, Valladares F, Ceulemans R (2003) Leaf-level phenotypic variability and plasticity of invasive Rhododendron ponticum and non-invasive Ilex aquifolium co-occurring at two contrasting European sites. Plant Cell Environ 26:941–956

    Article  PubMed  Google Scholar 

  • Normile D (2004) Expanding trade with China creates ecological backlash. Science 306:968–969

    Article  PubMed  CAS  Google Scholar 

  • Parker IM, Rodriguez J, Loik ME (2003) An evolutionary approach to understanding the biology of invasions: local adaptation and general-purpose genotypes in the weed Verbascum thapsus. Conserv Biol 17:59–72

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734

    Article  PubMed  CAS  Google Scholar 

  • Schmitz J (1991) Vorkommen und Soziologie neophytischer Sträucher im Raum Aachen. Decheniana 144:22–38

    Google Scholar 

  • Schubert R, Hilbig W, Klotz S (2001) Bestimmungsbuch der Pflanzengesellschaften Deutschlands. Spektrum Akademischer Verlag, Heidelberg

  • 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

    Article  Google Scholar 

  • Smith MD, Knapp AK (2001) Physiological and morphological traits of exotic, invasive exotic and native species in tallgrass prairie. Int J Plant Sci 162:785–792

    Article  Google Scholar 

  • Vertregt N, Penning de Vries FWT (1987) A rapid method for determining the efficiency of synthesis of plant biomass. J Theor Biol 128:109–119

    Google Scholar 

  • Vitousek PM (1986) Biological invasions and ecosystem properties: can species make a difference? Ecol Stud 58:163–176

    Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr Heike Vibrans (Colegio de Postgraduados en Ciencias Agrícolas, México), the Editor-in-Chief Dr Christian Körner, the handling editor Dr Fernando Valladares and three anonymous reviewers for their valuable advice and comments on an earlier version of the manuscript. This version of the manuscript has been improved greatly by their insightful comments. Furthermore, we thank Antje Thondorf for carrying out the carbon and nitrogen analyses. Y.-L. Feng was funded by the Key Project of Knowledge Innovation Engineering of Chinese Academy of Sciences (KSCX1-SW-13-0X-0X) and the Project of National Natural Science Foundation of China (30670394). The experiments comply with the current laws of the country in which they were performed.

Author information

Authors and Affiliations

  1. Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, 88 Xuefu Road, Kunming, 650223, China

    Yu-Long Feng

  2. Department of Community Ecology, UFZ, Helmholtz Centre for Environmental Research, Theodor-Lieser-Strasse 4, 06120, Halle, Germany

    Harald Auge & Susan K. Ebeling

Authors
  1. Yu-Long Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Harald Auge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan K. Ebeling
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yu-Long Feng.

Additional information

Communicated by Fernando Valladares.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feng, YL., Auge, H. & Ebeling, S.K. Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 153, 501–510 (2007). https://doi.org/10.1007/s00442-007-0759-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-007-0759-2

Keywords

Search

Navigation