Skip to main content

Advertisement

Log in

Secondary invasion of Acer negundo: the role of phenotypic responses versus local adaptation

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

During plant species invasions, the role of adaptive processes is particularly of interest in later stages of range expansion when populations start invading habitats that initially have not been disposed to invasions. The dioecious tree Acer negundo, primarily invasive in Europe in wet habitats along riversides and in floodplains, has increased its abundance in dry habitats of industrial wasteland and ruderal sites during the last decades in Eastern Germany. We chose 21 invasive populations from wet and from dry habitats in the region of Halle, Saxony-Anhalt, Germany, to test whether Acer negundo exhibits a shift in life-history strategy during expansion into more stressful habitats. We analyzed variables of habitat quality (pH, soil moisture, exchangeable cations, total C and N content) and determined density, sex ratio and regeneration of the populations. In addition, we conducted germination experiments and greenhouse studies with seedlings in four different soil moisture environments. Local adaptation was studied in a reciprocal transplant experiment. We found habitat type differentiation with lower nutrient and water supply at the dry sites than at the moist sites and significant differences in the number of seedlings in the field. In accordance, seeds from moist habitats responded significantly faster to germination treatments. In the transplant experiment, leaf life span was significantly larger for populations originating from dry habitat types than from moist habitats. This observed shift in life history strategy during secondary invasion of A. negundo from traits of establishment and rapid growth towards traits connected with persistence might be counteracted by high gene flow among populations of the different habitat types. However, prolonged leaf life span at dry sites contributed remarkably to the invasion of less favourable habitats, and, thus, is a first indication of ongoing adaptation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Antonovics J, Bradshaw AD (1970) Evolution in closely adjacent plant populations. VIII. Clinal patterns at a mine boundary. Heredity 25:349–365

    Article  Google Scholar 

  • Antonovics J, Primack RB (1982) Experimental ecological genetics in Plantago—VI. The demography of seedling transplants of P. lanceolata. J Ecol 70:55–75

    Article  Google Scholar 

  • Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 147–172

    Google Scholar 

  • Barrett SCH, Richardson BJ (1986) Genetic attributes of invading species. In: Groves RH, Burdon JJ (eds) Ecology of biological invasions. Cambridge University Press, Cambridge, pp 21–33

    Google Scholar 

  • Bennington CC, McGraw JB (1995) Natural selection and ecotypic differentiation in Impatiens pallida. Ecol Monogr 65:303–323

    Article  Google Scholar 

  • Berendse F, Braakhekke W, van der Krift T (1998) Adaptations of plant populations to nutrient-poor environments and their implications for soil nutrient mineralisation. In: Lambers H, Poorter H, van Vuuren MMI (eds) Inherent variation in plant growth. Backhuys Publishers, Leiden, pp 503–514

    Google Scholar 

  • Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035–3042

    Article  Google Scholar 

  • Brown JS, Eckert CG (2005) Evolutionary increase in sexual and clonal reproductive capacity during biological invasion in an aquatic plant Butomus umbellatus (Butomaceae). Am J Bot 92:495–502

    Article  Google Scholar 

  • Brunner E, Puri ML (2001) Nonparametric methods in factorial designs. Statistical papers 42:1–52

    Article  Google Scholar 

  • Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Ann Rev Ecol Syst 13:229–259

    Article  Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Ann Rev Ecol Syst 11:233–260

    Article  CAS  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  PubMed  CAS  Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 74:798–815

    Article  Google Scholar 

  • Dawson TE, Geber MA (1999) Sexual dimorphism in physiology and morphology. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin, Heidelberg, pp 175–215

    Google Scholar 

  • Dawson TE, Ward JK, Ehleringer JR (2004) Temporal scaling of physiological response from gas exchange to tree rings: a gender-specific study of Acer negundo (Boxelder) growing under different conditions. Funct Ecol 18:212–222

    Article  Google Scholar 

  • Dietz H, Edwards PJ (2006) Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87:1359–1367

    Article  PubMed  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecol Lett 11:701–709

    Article  PubMed  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Nat Acad Sci US 97:7043–7050

    Article  CAS  Google Scholar 

  • Eränen JK, Nilsen J, Zverev VE, Kozlov MV (2009) Mountain birch under multiple stressors–heay-metal resistant populations co-resistant to biotic stress but maladapted to abiotic stress. J Evol Biol 22:840–851

    Article  PubMed  Google Scholar 

  • Erfmeier A, Bruelheide H (2005) Invasive and native Rhododendron ponticum populations: Is there evidence for genotypic differences in germination and growth? Ecography 28:417–428

    Article  Google Scholar 

  • Erfmeier A, Bruelheide H (2010) Invasibility or invasiveness? Effects of habitat, genotype, and their interaction on invasive Rhododendron ponticum populations. Biol Invasions 12:657–676

    Article  Google Scholar 

  • Facon B, Genton BJ, Shykoff JA, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135

    Article  PubMed  Google Scholar 

  • Farris MA (1987) Natural selection on the plant-water relations of Cleome serrulata growing along natural moisture gradients. Oecologia 72:434–439

    Article  Google Scholar 

  • Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Freeman DC, Klikoff LG, Harper KT (1976) Differential resource utilization by sexes of dioecious plants. Science 193:597–599

    Article  PubMed  CAS  Google Scholar 

  • Grime JP (2001) Plant strategies and vegetation processes. Chichester, Wiley

    Google Scholar 

  • Gurevitch J, Teeri JA, Wood AM (1986) Differentiation among populations of Sedum wrightii (Crassulaceae) in response to limited water availability: water relations, CO2, assimilation, growth and survivorship. Oecologia 70:198–204

    Article  Google Scholar 

  • Hacker JB (1984) Genetic variation in seed dormancy in Digitaria milanjiana in relation to rainfall at the collection site. J Appl Ecol 21:947–959

    Article  Google Scholar 

  • Hacker JB, Ratcliff D (1989) Seed dormancy and factors controlling dormancy breakdown in buffel grass accessions from contrasting provenances. J Appl Ecol 26:201–212

    Article  Google Scholar 

  • Hänfling B, Kollmann J (2002) An evolutionary perspective of biological invasions. Trends Ecol Evol 17:545–546

    Article  Google Scholar 

  • Hedrick PW (2005) Genetics of populations. Jones and Bartlett Publishers, Sudbury, Massachusetts

    Google Scholar 

  • Huang X, Schmitt J, Dorn L, Griffith C, Effgen S, Takao S, Koorneef M, Donohue K (2010) The earliest stages of adaptation in an experimental plant population: strong selection on QTLS for seed dormancy. Mol Ecol 19:1335–1351

    Article  PubMed  Google Scholar 

  • Hunt R (1989) Basic growth analysis. Unwin Hyman, London

    Google Scholar 

  • Jäger EJ (1975) Wo liegen die Grenzen der Kulturareale von Pflanzen? Möglichkeiten der Beobachtung in Botanischen Gärten. Wissenschaftliche Beiträge MLU Halle-Wittenberg 6:101–113

    Google Scholar 

  • Jain SK, Bradshaw AD (1966) Evolutionary divergence among adjacent plant populations. Heredity 21:407–441

    Article  Google Scholar 

  • Jonas CJ, Geber MA (1999) Variation among populations of Clarkia unguiculata (Onagraceae) along altitudinal and latitudinal gradients. Am J Bot 86:333–343

    Article  PubMed  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kikuzawa K (2003) Phenological and morphological adaptations to the light environment in two woody and two herbaceous plant species. Funct Ecol 17:29–38

    Article  Google Scholar 

  • King DA (1994) Influence of light level on the growth and morphology of saplings in a Panamanian forest. Am J Bot 81:948–957

    Article  Google Scholar 

  • Kowarik I (2003) Biologische Invasionen: Neophyten und Neozoen in Mitteleuropa. Ulmer, Stuttgart

    Google Scholar 

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

    Article  Google Scholar 

  • Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Nat Acad Sci USA 104:3883–3888

    Article  PubMed  CAS  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Leger EA, Rice KJ (2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol Lett 6:257–264

    Article  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS System for mixed models, 1st edn. SAS Institute Inc, Cary, North C

    Google Scholar 

  • Little EL Jr (1971) Atlas of US trees, vol.1–Conifers and important hardwoods. U.S. Government Printing Office, Washington, D.C.

    Google Scholar 

  • Little EL Jr (1979) Checklist of United States Trees (native and naturalized). Agriculture Handbook 541. U.S. Department of Agriculture, Forest Service, Washington, D.C, p 375

    Google Scholar 

  • Maeglin RR, Ohman LF (1973) Boxelder (Acer negundo): A review and commentary. Bulletin of the Torrey Botanical Club 100:357–363

    Article  Google Scholar 

  • Maron JL, Elmendorf SC, Vilà M (2007) Contrasting plant physiological adaptation to climate change in the native and introduced range of Hypericum perforatum. Evolution 61:1912–1924

    Article  PubMed  Google Scholar 

  • McGraw JB, Antonovics J (1983) Experimental ecology of Dryas octopetala ecotypes I. Ecotypic differentiation and life-cycle stages of selection. J Ecol 71:879–897

    Article  Google Scholar 

  • McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291

    Article  Google Scholar 

  • Meyer GH, Hull-Sanders HM (2008) Altered patterns of growth, physiology and reproduction in invasive genotypes of Solidago gigantea (Asteraceae). Biol Invasions 10:303–317

    Article  Google Scholar 

  • Meyer SE, Pendleton BK (2005) Factors affecting seed germination and seedling establishment of a long-lived desert shrub (Coleogyne ramosissima: Rosaceae). Plant Ecol 178:171–187

    Article  Google Scholar 

  • Milbau A, Nijs I, Van Peer L, Reheul D, De Cauwer B (2003) Disentangling invasiveness and invasibility during invasion in synthesized grassland communities. New Phytol 159:657–667

    Article  Google Scholar 

  • Moloney KA, Knaus F, Dietz H (2009) Evidence for a shift in life-history strategy during the secondary phase of a plant invasion. Biol Invasions 11:625–634

    Article  Google Scholar 

  • Moyers BT, Kane NC (2010) The genetics of adaptation to novel environments: selection on germination timing in Arabidopsis thaliana. Mol Ecol 19:1270–1272

    Article  PubMed  Google Scholar 

  • Novak SJ (2007) The role of evolution in the invasion process. Proc Nat Acad Sci USA 104:3671–3672

    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 

  • Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87:1733–1743

    Article  PubMed  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. University Press, Cambridge

    Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62:365–392

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Roloff A (2006) Flora der Gehölze. Eugen Ulmer, Stuttgart

    Google Scholar 

  • Ross MA, Harper JL (1972) Occupation of biological space during seedling establishment. J Ecol 60:77–88

    Article  Google Scholar 

  • Rothmaler W (1972) Exkursionsflora für die Gebiete der DDR und der BRD - Gefäßpflanzen, 7th edn. Volk und Wissen, Berlin

    Google Scholar 

  • Rothmaler W (1984) Exkursionsflora für die Gebiete der DDR und der BRD - Gefäßpflanzen, 12th edn. Volk und Wissen, Berlin

    Google Scholar 

  • Rothmaler W (2005) Exkursionsflora von Deutschland. In: Jäger EJ, Werner K (eds) Gefäßpflanzen: Kritischer Band. Spektrum Akademischer Verlag

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sambatti JBM, Rice KJ (2007) Functional ecology of ecotypic differentiation in the Californian serpentine sunflower (Helianthus exilis). New Phytol 175:107–119

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute (2000) SAS Procedures Guide. Cary, North Carolina

  • Savolainen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Ann Rev Ecol Evol Syst 38:595–619

    Article  Google Scholar 

  • 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 

  • Siemann E, Rogers WE (2001) Genetic differences in growth of an invasive tree species. Ecol Lett 4:514–518

    Article  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Ann Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374

    Article  PubMed  Google Scholar 

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273

    Article  PubMed  Google Scholar 

  • Volis S, Mendlinger S, Ward D (2002) Differentiation in populations of Hordeum spontaneum along a gradient of environmental productivity and predictability: life history and local adaptation. Biol J Linn Soc 77:479–490

    Article  Google Scholar 

  • von Schlechtendahl DFL (1884) Flora von Deutschland. Fr. Eugen Köhler, Gera

    Google Scholar 

  • Weber E (2003) Invasive plant species of the world. A reference guide to environmental weeds. CABI Publishing, Oxon

    Google Scholar 

  • Weber E, Schmid B (1998) Latitudinal population differentiation in two species of Solidago (Asteraceae) introduced into Europe. Am J Bot 85:1110–1121

    Article  Google Scholar 

  • Westoby M, Falster DS, Moles A, Vesk PA, Wrigth IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Ann Rev Ecol Syst 33:125–159

    Article  Google Scholar 

  • Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distr 14:569–580

    Article  Google Scholar 

  • Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. J Ecol 90:534–543

    Article  Google Scholar 

Download references

Acknowledgments

We thank the office for the environment, Landesamt für Umweltschutz, Saxony-Anhalt, and the regional government authority, Landesverwaltungsamt, Saxony-Anhalt for their support in locating suitable populations and for the permission of nature reserve access. We acknowledge the help of A. Zeuner, S. Kosellek, A. Hallensleben during field work trips and especially appreciate the technical help in the greenhouse and in the laboratory by E. Bremer, C. Voigt, J. Treiber and S. Hammer.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexandra Erfmeier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Erfmeier, A., Böhnke, M. & Bruelheide, H. Secondary invasion of Acer negundo: the role of phenotypic responses versus local adaptation. Biol Invasions 13, 1599–1614 (2011). https://doi.org/10.1007/s10530-010-9917-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9917-2

Keywords

Navigation