Skip to main content
Log in

Increased competitive ability and herbivory tolerance in the invasive plant Sapium sebiferum

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

Abstract

The evolution of increased competitive ability (EICA) hypothesis predicts that release from natural enemies in the introduced range favors exotic plants evolving to have greater competitive ability and lower herbivore resistance than conspecifics from the native range. We tested the EICA hypothesis in a common garden experiment with Sapium sebiferum in which seedlings from native (China) and invasive (USA) populations were grown in all pairwise combinations in the native range (China) in the presence of herbivores. When paired seedlings were from the same continent, shoot mass and leaf damage per seedling were significantly greater for plants from invasive populations than those from native populations. Despite more damage from herbivores, plants from invasive populations still outperformed those from native populations when they were grown together. Increased competitive ability and higher herbivory damage of invasive populations relative to native populations of S. sebiferum support the EICA hypothesis. Regression of biomass against percent leaf damage showed that plants from invasive populations tolerated herbivory more effectively than those from native populations. The results of this study suggest that S. sebiferum has become a faster-growing, less herbivore-resistant, and more herbivore-tolerant plant in the introduced range. This implies that increased competitive ability of exotic plants may be associated with evolutionary changes in both resistance and tolerance to herbivory in the introduced range. Understanding these evolutionary changes has important implications for biological control strategies targeted at problematic invaders.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agrawal AA, Conner JK, Stinchcombe JR (2004) Evolution of plant resistance and tolerance to frost damage. Ecol Lett 7:1199–1208

    Article  Google Scholar 

  • Bastlová D, Květ J (2002) Differences in dry weight partitioning and flowering phenology between native and non-native plants of purple loosestrife (Lythrum salicaria L.). Flora 197:332–340

    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 

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

    Article  Google Scholar 

  • Bossdorf O, Prati D, Auge H, Schmid B (2004a) Reduced competitive ability in an invasive plant. Ecol Lett 7:346–353

    Article  Google Scholar 

  • Bossdorf O, Schröder S, Prati D, Auge H (2004b) Palatability and tolerance to simulated herbivory in native and introduced populations of Alliaria petiolata (Brassicaceae). Am J Bot 91:856–862

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bruce KA, Cameron GN, Harcombe PA, Jubinsky G (1997) Introduction, impact on native habitats, and management of a wood invader, the Chinese tallow tree, Sapium sebiferum (L.) Roxb. Nat Areas J 17:255–260

    Google Scholar 

  • Buschmann H, Edwards PJ, Dietz H (2005) Variation in growth pattern and response to slug damage among native and invasive provenances of four perennial Brassicaceae species. J Ecol 93:322–334

    Article  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • DeWalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483

    Article  Google Scholar 

  • DeWalt SJ, Siemann E, Rogers WE (2006) Microsatellite markers for an invasive tetraploid tree, Chinese Tallow (Triadica sebifera). Mol Ecol Notes 6:505–507

    Article  CAS  Google Scholar 

  • Elberse IAM, Turin JHB, Wäckers FL, van Damme JMM, van Tienderen PH (2003) The relationship between relative growth rate and susceptibility to aphids in wild barley under different nutrient levels. Oecologia 137:564–571

    Article  PubMed  CAS  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 

  • Goldberg DE (1996) Competitive ability: definitions, contingency and correlated traits. Philos Trans R Soc B 351:1377–1385

    Article  Google Scholar 

  • García LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105:657–663

    Article  Google Scholar 

  • Grime JP (1979) Plant strategies and vegetation processes. Wiley, Chichester, UK

    Google Scholar 

  • Grotkopp E, Rejmánek M, Rost TL (2002) Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. Am Nat 159:396–419

    Article  Google Scholar 

  • Güsewell S, Jakobs G, Weber E (2006) Native and introduced populations of Solidago gigantea differ in shoot production but not in leaf traits or litter decomposition. Funct Ecol 20:575–584

    Article  Google Scholar 

  • Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15

    Article  Google Scholar 

  • Jones RH, McLeod KW (1990) Growth and photosynthetic responses to light environment in Chinese tallow tree and Carolina ash seedlings. Forest Sci 36:851–862

    Google Scholar 

  • Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • van Kleunen M, Schmid B (2003) No evidence for evolutionary increased competitive ability (EICA) in the invasive plant Solidago canadensis. Ecology 84:2824–2831

    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 

  • Leger EA, Forister ML (2005) Increased resistance to generalist herbivores in invasive populations of the California poppy (Eschscholiza californica). Divers Distrib 11:311–317

    Article  Google Scholar 

  • Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545

    Article  Google Scholar 

  • Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Article  Google Scholar 

  • Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280

    Article  Google Scholar 

  • Maxwell SE, Delaney HD (1990) Designing experiments and analyzing data: a model comparison perspective. Belmont, Wadsworth, CA

    Google Scholar 

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

    Google Scholar 

  • van der Meijden E, Wijn M, Verkaar HJ (1988) Defence and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355–363

    Article  Google Scholar 

  • van der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol Exp Appl 80:307–310

    Article  Google Scholar 

  • Memmott J, Fowler SV, Paynter Q, Sheppard AW, Syrett P (2000) The invertebrate fauna on broom, Cytisus scopartius, in two native and two exotic habitats. Acta Oecol 21:213–222

    Article  Google Scholar 

  • Meyer G, Clare R, Weber E (2005) An experimental test of the evolution of increased competitive ability hypothesis in goldenrod, Solidago gigantea. Oecologia 144:299–307

    Article  PubMed  Google Scholar 

  • Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451

    Article  PubMed  CAS  Google Scholar 

  • Müller C, Martens N (2005) Testing predictions of the ‘evolution of increased competitive ability’ hypothesis for an invasive crucifer. Evol Ecol 19:533–550

    Article  Google Scholar 

  • Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:418–422

    Google Scholar 

  • Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967

    Article  Google Scholar 

  • Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  PubMed  CAS  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 

  • Rogers WE, Siemann E (2004) Invasive ecotypes tolerate herbivory more effectively than native ecotypes of the Chinese tallow tree Sapium sebiferum. J Appl Ecol 41:561–570

    Article  Google Scholar 

  • Rogers WE, Siemann E (2005) Herbivory tolerance and compensatory differences in native and invasive ecotypes of Chinese tallow tree (Sapium sebiferum). Plant Ecol 181:57–68

    Article  Google Scholar 

  • Rosenthal JP, Kotanen PM (1994) Terrestrial plant tolerance to herbivory. Trends Ecol Evol 9:145–148

    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 

  • Siemann E, Rogers WE (2003a) Reduced resistance of invasive varieties of the alien tree Sapium sebiferum to a generalist herbivore. Oecologia 135:451–457

    PubMed  Google Scholar 

  • Siemann E, Rogers WE (2003b) Increased competitive ability of an invasive tree may be limited by an invasive beetle. Ecol Appl 13:1503–1507

    Article  Google Scholar 

  • Siemann E, Rogers WE (2003c) Herbivory, disease, recruitment limitation and success of alien and native tree species. Ecology 84:1489–1505

    Article  Google Scholar 

  • Siemann E, Rogers WE, DeWalt SJ (2006) Rapid adaptation of insect herbivores to an invasive plant. P Roy Soc B-Biol Sci 273:2763–2769

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37

    Article  Google Scholar 

  • Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Evol S 31:565–595

    Article  Google Scholar 

  • Strauss S, Agrawal A (1999) The ecology and evolution of tolerance to herbivory. Trends Ecol Evol 14:179–185

    Article  PubMed  Google Scholar 

  • Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13:329–332

    Article  Google Scholar 

  • Tiffin P (2000) Are tolerance, avoidance, and antibiosis evolutionarily and ecologically equivalent responses of plants to herbivores? Am Nat 155:128–138

    Article  PubMed  Google Scholar 

  • Vilà M, Gómez A, Maron J (2003) Are alien plants more competitive than their native conspecifics? A test using Hypericum perforatum L. Oecologia 137:211–215

    Article  PubMed  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:218–228

    Google Scholar 

  • Wilcove DS, Rothstein D, Bubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615

    Article  Google Scholar 

  • Willis AJ, Blossey B (1999) Benign environments do not explain the increased vigour of non-indigenous plants: a cross-continental transplant experiment. Biocontrol Sci Technol 9:567–577

    Article  Google Scholar 

  • Willis AJ, Memmott J, Forrester RI (2000) Is there evidence for the post-invasion evolution of increased size among invasive plant species? Ecol Lett 3:275–283

    Article  Google Scholar 

  • Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711

    Article  Google Scholar 

  • Wolfe LM, Elzinga JA, Biere A (2004) Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol Lett 7:813–820

    Article  Google Scholar 

  • Zhang K, Lin Y (1994) Chinese tallow tree. China Forestry Press, Beijing [in Chinese]

  • Zou JW, Rogers WE, DeWalt SJ, Siemann E (2006) The effect of Chinese tallow tree (Sapium sebiferum) ecotype on soil-plant system carbon and nitrogen processes. Oecologia 150:272–281

    Article  PubMed  Google Scholar 

  • Zou JW, Rogers WE, Siemann E (2007) Differences in morphological and physiological traits of native and invasive populations of Sapium sebiferum. Funct Ecol doi:10.1111/j.1365-2435.2007.01298.x

Download references

Acknowledgments

We would like to thank Yao Huang, Lianggang Zong, Yanyu Lu, and Shutao Chen for their help in collecting S. sebiferum seeds in China, and maintenance of the experimental garden. This study was supported by the US National Science Foundation (DEB-0315796) and by the USDA (2003-35320-13498).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jianwen Zou.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zou, J., Rogers, W.E. & Siemann, E. Increased competitive ability and herbivory tolerance in the invasive plant Sapium sebiferum . Biol Invasions 10, 291–302 (2008). https://doi.org/10.1007/s10530-007-9130-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-007-9130-0

Keywords

Navigation