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Decreased indirect defense in the invasive tree, Triadica sebifera

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Abstract

In the absence of coevolved natural enemies, plants are expected to experience selection away from costly herbivore defenses toward growth and reproduction [evolution of increased competitive ability hypothesis (EICA)], yet no one has demonstrated EICA for an indirect defense trait. Likewise, we have little understanding of how constitutive and induced levels of defense vary among native and invasive plant populations. We conducted a greenhouse experiment in the introduced range to test whether invasive populations have reduced constitutive and induced investment in an indirect defense trait, extrafloral nectar (EFN) production, compared to native populations of Chinese tallow tree, Triadica sebifera, through an experimental leaf damage treatment. Overall, native populations invested more in indirect defense: Native populations had a greater number (+16 %) and percentage of leaves producing EFN (35 vs. 28 %), produced more EFN (63 % greater volume), and produced more sugar (+33 %) compared to invasive populations, independent of damage treatment. Of these traits, number of leaves producing EFN and volume of EFN exhibited a trade-off between constitutive and induced investment but these did not depend on plant origin. Our results are the first to support the EICA hypothesis for an indirect defense trait. This suggests that tri-trophic interactions such as indirect defense are under similar selection as direct defense traits within introduced populations. Despite reduced investment in EFN production, invasive populations still retain the ability to produce EFN, which may enable invasive plants to defend against herbivores in the introduced range.

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References

  • Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta 1734:91–111

    PubMed  CAS  Google Scholar 

  • Baldwin IT (1990) Herbivory simulations in ecological research. Trends Ecol Evol 5:91–93

    Article  PubMed  CAS  Google Scholar 

  • Beaton LL, Van Zandt PA, Esselman EJ, Knight TM (2011) Comparison of the herbivore defense and competitive ability of ancestral and modern genotypes of an invasive plant, Lespedeza cuneata. Oikos 120:1413–1419

    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, 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 

  • 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 Area J 17:255–260

    Google Scholar 

  • Cano L, Escarre J, Vrieling K, Sans FX (2009) Palatability to a generalist herbivore, defence and growth of invasive and native Senecio species: testing the evolution of increased competitive ability hypothesis. Oecologia 159:95–106

    Article  PubMed  CAS  Google Scholar 

  • Cipollini D, Heil M (2010) Costs and benefits of induced resistance to pathogens and herbivores in plants. CAB Rev 5:1–25

    Google Scholar 

  • Cipollini D, Mbagwu J, Barto K, Hillstrom C, Enright S (2005) Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata. J Chem Ecol 31:1255–1267

    Article  PubMed  CAS  Google Scholar 

  • Cripps MG, Hinz HL, McKenney JL, Price WJ, Schwarzlander M (2009) No evidence for an ‘evolution of increased competitive ability’ for the invasive Lepidium draba. Basic Appl Ecol 10:103–112

    Article  Google Scholar 

  • DeWalt SJ, Siemann E, Rogers W (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 

  • Eichhorn MP, Ratliffe LC, Pollard KM (2011) Attraction of ants by an invasive Acacia. Insect Conserv Divers 4:235–238

    Article  Google Scholar 

  • Eigenbrode SD, Andreas JE, Cripps MG, Ding H, Biggam RC, Schwarzlaender M (2008) Induced chemical defenses in invasive plants: a case study with Cynoglossum officinale L. Biol Invasions 10:1373–1379

    Article  Google Scholar 

  • Franks SJ, Pratt PD, Dray FA, Simms EL (2008) No evolution of increased competitive ability or decreased allocation to defense in Melaleuca quinuenervia since release from natural enemies. Biol Invasions 10:455–466

    Article  Google Scholar 

  • Galen C (2005) Catching ants with honey: an experimental test of distraction and satiation as alternative modes of escape from flower-damaging ants. Oecologia 144:80–87

    Article  PubMed  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Herrera AM, Carruthers RI, Mills NJ (2011) No evidence for increased performance of a specialist psyllid on invasive French broom. Acta Oecol 37:79–86

    Article  Google Scholar 

  • Huang W, Siemann E, Wheeler GS, Zou JW, 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

    Article  Google Scholar 

  • Hull-Sanders HM, Clare R, Johnson RH, Meyer GA (2007) Evaluation of the evolution of increased competitive ability (EICA) hypothesis: loss of defense against generalist but not specialist herbivores. J Chem Ecol 33:781–799

    Article  PubMed  CAS  Google Scholar 

  • Kempel A, Schadler M, Chrobock T, Fischer M, van Kleunen M (2011) Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc Natl Acad Sci USA 108:5685–5689

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357

    Article  Google Scholar 

  • Koptur S (1992) Interactions between insects and plants mediated by extrafloral nectaries. In: Bernay E (ed) Insect/plants interactions, vol 4. CRC Press, Boca Raton, pp 85–132

    Google Scholar 

  • Morris WF, Traw MB, Bergelson J (2006) On testing for a tradeoff between constitutive and induced resistance. Oikos 112:102–110

    Article  Google Scholar 

  • Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459

    Article  PubMed  CAS  Google Scholar 

  • Ridenour WM, Vivanco JM, Feng YL, 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, Lankau RA (2003) Damage induced production of extrafloral nectaries in native and invasive seedlings of Chinese tallow tree (Sapium sebiferum). Am Midl Nat J 149:413–417

    Article  Google Scholar 

  • Rudgers JA (2004) Enemies of herbivores can shape plant traits: selection in a facultative ant–plant mutualism. Ecology 85:192–205

    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) Herbivory, disease, recruitment limitation, and success of alien and native tree species. Ecology 84:1489–1505

    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

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Stinchcombe JR, Rausher MD (2002) The evolution of tolerance to deer herbivory: modifications caused by the abundance of insect herbivores. Proc R Soc Lond B 269:1241–1246

    Article  Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol Syst 35:435–466

    Article  Google Scholar 

  • Tiffin P, Inouye BD (2000) Measuring tolerance to herbivory: accuracy and precision of estimates made using natural versus imposed damage. Evolution 54:1024–1029

    PubMed  CAS  Google Scholar 

  • Wang Y, Huang W, Siemann E, Zou JW, Wheeler GS, Carrillo J, Ding JQ (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 

  • Xu FF, Chen J (2009) Comparison of the differences in response to the change of the extrafloral nectar-ant-herbivore interaction system between a native and an introduced Passiflora species. Acta Bot Yun 31:543–550

    Article  Google Scholar 

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

    Google Scholar 

  • Zou JW, Rogers WE, Siemann E (2007) Differences in morphological and physiological traits between native and invasive populations of Sapium sebiferum. Funct Ecol 21:721–730

    Article  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 

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Acknowledgments

We thank C. Gabler, K. Horn, S. Siemann, M. Siemann, K. Klimas, and A. Luckey for their help in data collection and four anonymous reviewers whose comments significantly improved the manuscript. This study was supported by a U.S. NSF Graduate Research and Ford Foundation fellowship (to J. Carrillo), the 100 Talent Program of the Chinese Academy of Sciences (to J. Ding), the U.S. National Science Foundation (DEB 0820560 to E. Siemann), and the foreign visiting professorship of the Chinese Academy of Sciences (2009S1-30 to E. Siemann).

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Rice University, Houston, TX, 77005, USA

    Juli Carrillo, Kyle Klootwyk & Evan Siemann

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

    Yi Wang & Jiangqing Ding

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  1. Juli Carrillo
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  2. Yi Wang
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  3. Jiangqing Ding
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  4. Kyle Klootwyk
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  5. Evan Siemann
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Correspondence to Juli Carrillo.

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Carrillo, J., Wang, Y., Ding, J. et al. Decreased indirect defense in the invasive tree, Triadica sebifera . Plant Ecol 213, 945–954 (2012). https://doi.org/10.1007/s11258-012-0055-z

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