Skip to main content
SpringerLink
Log in

Repeated damage by specialist insects suppresses the growth of a high tolerance invasive tree

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Many invasive plant species have high tolerance to herbivore damage, which can lead to low impacts of introduced biological control insects. High herbivore tolerance may be a trait acquired by invasive plants in their invaded range which makes it difficult to predict impacts of introduced insects. In this study, we compared the growth and foliar secondary chemical responses of invasive and native populations of Triadica sebifera (Chinese tallow tree) to repeated damage by specialist or generalist herbivores. We found repeated damage significantly decreased plant biomass and increased foliar tannin and flavonoid concentrations compared to a single damage event. These effects were significantly stronger with specialist damage than with generalist damage but the magnitudes of these differences were small. Plants from invasive populations had lower foliar tannins and higher foliar flavonoids than plants from native populations and had greater biomass in every damage treatment. Our results suggest that repeated damage could suppress the growth of invasive plants with high tolerance. Thus using multivoltine herbivores as biological control agents may overcome herbivore tolerance and increase biological control efficacy.

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

Similar content being viewed by others

References

  • Bale JS, van Lenteren JC, Bigler F (2008) Biological control and sustainable food production. Philos Trans R Soc B 363:761–776

    Article  CAS  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 

  • Blumenthal D, Mitchell CE, Pysek P, Jarosık V (2009) Synergy between resource availability and pathogen releasein plant invasion. Proc Nat Acad Sci USA 106:7899–7904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

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

    Google Scholar 

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

    Article  Google Scholar 

  • DeWalt SJ, Siemann E, Rogers WE (2011) Geographic distribution of genetic variation among native and introduced populations of Chinese tallow tree, Triadica sebifera (Euphorbiaceae). Am J Bot 98:1128–1138

    Article  PubMed  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 

  • Gerber E, Hinz HL, Blossey B (2008) Pre-release impact assessment of two stemboring weevils proposed as biological control agents for Alliaria petiolata. Biol Control 45:360–367

    Article  Google Scholar 

  • Huang W, Siemann E, Wheeler WS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98:1157–1167

  • Huang W, Wheeler GS, Purcell M, Ding J (2011) The host range and impact of Bikasha collaris (Coleoptera: Chrysomelidae), a promising candidate agent for biological control of Chinese tallow, Triadica sebifera (Euphorbiaceae) in the United States. Biol Control 56:230–238

    Article  Google Scholar 

  • Julien M, Griffiths M (1998) Biological control of weeds: a word catalogue of agents and their target weeds, 4th edn. CABI Publishing, Wallingford

    Google Scholar 

  • Koricheva J, Nykanen H, Gianoli E (2004) Meta-analysis of tradeoffs among plant antiherbivore defences: are plants jacks of all trades, masters of all? Am Nat 163:E64–E75

    Article  PubMed  Google Scholar 

  • McFadyen R (1998) Biological control of weeds. Annu Rev Entomol 43:369–393

    Article  CAS  PubMed  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 

  • Milbrath LR (2008) Growth and reproduction of invasive Vincetoxicum rossicum and V. nigrum under artificial defoliation and different light environments. Botany 86:1279–1290

    Article  Google Scholar 

  • Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417–422

    Article  PubMed  Google Scholar 

  • Olson BE, Richards JH (1988) Tussock regrowth after grazing: intercalary meristem and axillary bud activity of tillers of Agropyron desertorum. Oikos 51:374–382

    Article  Google Scholar 

  • Olson BE, Wallander RT, Lacey JR (1997) Effects of sheep grazing on a spotted knapweed-infested Idaho fescue community. J Range Manage 50:386–390

  • Pattison RR, Mack RN (2008) Potential distribution of the invasive tree Triadica sebifera (Euphorbiaceae) in the United States: evaluating CLIMEX predictions with field trials. Glob Change Biol 14:813–826

    Article  Google Scholar 

  • Pearson DE, Callaway RM (2003) Indirect effects of host-specific biological control agents. Trends Ecol Evol 18:456–461

    Article  Google Scholar 

  • Raghu S, Dhileepan K, Treviño M (2006) Response of an invasive liana to simulated herbivory: implications for its biological control. Acta Oecol 29:335–345

    Article  Google Scholar 

  • Ridenour WM, Vivanco JM, Feng Y, Horiuchi J, Callaway RM (2008) No evidence for trade-offs: centaurea plants from America are better competitors and defenders. Ecol Monogr 78:369–386

    Article  Google Scholar 

  • Rogers WE, Siemann E (2003) Effects of simulated herbivory and resources on Chinese tallow tree (Sapium sebiferum, Euphorbiaceae) invasion of native coastal prairie. Am J Bot 90:243–249

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Sampedro L, Moreira X, Zas R (2011) Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability. J Ecol 99:818–827

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith L (2005) Host plant specificity and potential impact of Aceria salsolae (Acari: Eriophyidae), an agent proposed for biological control of Russian thistle (Salsola tragus). Biol Control 34:83–92

    Article  Google Scholar 

  • Stamp N (2003) Out of the quagmire of plant defence hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • Striker GG, Manzur ME, Grimoldi AA (2011) Increasing defoliation frequency constrains regrowth of the forage legume Lotus tenuis under flooding: the role of crown reserves. Plant Soil 343:261–272

    Article  CAS  Google Scholar 

  • Underwood N (2012) When herbivores come back: effects of repeated damage on induced resistance. Funct Ecol 26:1441–1449

    Article  Google Scholar 

  • USDA/NRCS (2016). Plants profile: Triadica sebifera (L.) small Chinese tallow tree. (http://plants.usda.gov/core/profile?symbol=TRSE6)

  • 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 

  • van Lenteren JC, Bueno VHBP (2003) Augmentative biological control of arthropods in Latin America. BioControl 48:123–139

    Article  Google Scholar 

  • Wang Y, Huang W, Siemann E, Zou J, Wheeler GS, Carrillo J, Ding J (2011) Lower resistance and higher tolerance of invasive host plants: biocontrol agents reach high densities but exert weak control. Ecol Appl 21:729–738

    Article  PubMed  Google Scholar 

  • Wang Y, Siemann E, Wheeler GS, Zhu L, Gu X, Ding J (2012a) Genetic variation in anti-herbivore chemical defenses in an invasive plant. J Ecol 100:894–904

    Article  Google Scholar 

  • Wang Y, Zhu L, Gu X, Wheeler GS, Purcell M, Ding J (2012b) Pre-release assessment of a noctuid Gadirtha inexacta (= Iscadia inexacta) proposed as a biological control agent of Chinese tallow (Triadica sebifera) in the United States. Biol Control 63:304–309

    Article  Google Scholar 

  • Weis AE, Simms EL, Hochberg ME (2000) Will plant vigor and tolerance be genetically correlated? Effects of intrinsic growth rate and self-limitation on regrowth. Evol Ecol 14:331–352

    Article  Google Scholar 

  • Zas R, Moreira X, ampedro SL (2011) Tolerance and induced resistance in a native and an exotic pine species: relevant traits for invasion ecology. J Ecol 99:1316–1326

    Article  Google Scholar 

  • Zhang KD, Lin YT (1994) Chinese Tallow. China Forestry Press, Beijing

    Google Scholar 

  • Zou JW, Rogers WE, Siemann E (2008a) Increased competitive ability and herbivory tolerance in the invasive plant Sapium sebiferum. Biol Invasions 10:291–302

    Article  Google Scholar 

  • Zou JW, Siemann E, Rogers WE, Dewalt SJ (2008b) Decreased resistance and increased tolerance to native herbivores of the invasive plant Sapium sebiferum. Ecography 31:663–671

    Article  Google Scholar 

  • Zou JW, Rogers WE, Siemann E (2009) Plasticity of Sapium sebiferum seedling growth to light and water resources: inter- and intraspecific comparisons. Basic Appl Ecol 10:79–88

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Xue Gu for field assistance, two reviewers and editor’s comments improved our manuscript. This study was supported by the China National Basic Study Program (2012CB114104 to J.D.), the US National Science Foundation (DEB 0820560 to E.S.), a Foreign Visiting Professorship of the Chinese Academy of Sciences (to E.S.), the Chinese National Science Foundation (Y411041H01 to Y.W.) and Youth Innovation Foundation by Chinese Academy of Sciences (Y329341H02 to Y.W.).

Author information

Authors and Affiliations

  1. Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Institute/Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, Hubei, 430074, China

    Yi Wang, Lin Zhu & Jianqing Ding

  2. Graduate University of Chinese Academy of Sciences, Beijing, 100049, China

    Yi Wang

  3. Institute of Environmental Biology and Insect Resources, College of Plant Protection, Shandong Agriculture University, Taian, Shandong, 271018, China

    Lin Zhu

  4. Biosciences Department, Rice University, Houston, TX, 77005, USA

    Evan Siemann

Authors
  1. Yi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lin Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Evan Siemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jianqing Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jianqing Ding.

Additional information

Handling Editor: S. Raghu

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Zhu, L., Siemann, E. et al. Repeated damage by specialist insects suppresses the growth of a high tolerance invasive tree. BioControl 61, 793–801 (2016). https://doi.org/10.1007/s10526-016-9746-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-016-9746-z

Keywords

Search

Navigation