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History of exposure to herbivores increases the compensatory ability of an invasive plant

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Abstract

Release from natural enemies is frequently cited as an important factor contributing to plant invasions. But such effects are likely to be temporary—native herbivores can form new plant-herbivore associations and co-evolved insects might reach the new range. While the potential effects of the initial enemy release have been well studied, the consequences of any resumption of herbivory are poorly understood. Alternanthera philoxeroides is one of the most widespread invasive plants in China and is attacked both by a specialist herbivore introduced from the native range, Agasicles hygrophila, and a native beetle Cassida piperata Hope which has formed a new association. However, these insects are not found throughout the invaded range. To test the effect of the history of population exposure to herbivory on compensatory ability, plants were cultured from 14 populations around China that differed in whether A. hygrophila or C. piperata were present. Treatment plants were exposed to herbivory by A. hygrophila for a week until 50% of the leaf area was defoliated, then grown for 80 days. Plants from populations with prior exposure to herbivory (of any kind) accumulated more root mass than populations without prior exposure, indicating that prior exposure to insects can stimulate plant compensation to herbivory. We would recommend that potential changes in plant tolerance in response to prior exposure to herbivory are considered in invasive plant management plans that employ bio-control agents.

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References

  • Belsky AJ (1986) Does herbivory benefit plants? A review of the evidence. Am Nat 127:870–892

    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. doi:10.1007/s00442-005-0070-z

    Article  PubMed  Google Scholar 

  • Buckingham GR (2002) Alligatorweed. In: van Driesche R, Blossey B, Hoddle M, Lyon S, Reardon R (eds) Biological control of invasive plants in the Eastern United States, pp 5–15, USDA Forest Service Publication FHTET-2002-04

  • Carman JG, Briske DD (1985) Morphologic and allozymic variation between long-term grazed and non-grazed populations of the bunchgrass Schizachyrium scoparium var. frequens. Oecologia 66:332–337. doi:10.1007/BF00378294

    Article  Google Scholar 

  • Cronin G, Schlacher T, Lodge DM, Siska EL (1999) Intraspecific variation in feeding preference and performance of Galerucella nymphaeae (Chrysomelidae: Coleoptera) on aquatic macrophytes. J North Am Benthol Soc 18:391–405

    Article  Google Scholar 

  • Damhoureyeh SA, Hartnett DC (2002) Variation in grazing tolerance among three tallgrass prairie plant species. Am J Bot 89:1634–1643

    Article  PubMed  Google Scholar 

  • Detling JK, Painter EL (1983) Defoliation responses of western wheatgrass populations with diverse histories of prairie dog grazing. Oecologia 57:65–71. doi:10.1007/BF00379563

    Article  Google Scholar 

  • Gao LX, Geng YP, Li B, Chen JK, Yang J (2010) Genome-wide DNA methylation alterations of Alternanthera philoxeroides in natural and manipulated habitats: implications for epigenetic regulation of rapid responses to environmental fluctuation and phenotypic variation. Plant Cell Environ 33:1820–1827. doi:10.1111/j.1365-3040.2010.02186.x

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Rossi D, Rank N, Strong DR (2003) Potential for self-defeating biological control? Variation in herbivore vulnerability among invasive Spartina genotypes. Ecol Appl 13:1640–1649. doi:10.1890/01-5301

    Article  Google Scholar 

  • Geng YP, Pan XY, Xu CY, Zhang WJ, Li B, Chen JK, Lu BR, Song ZP (2007) Phenotypic plasticity rather than locally adapted ecotypes allows the invasive alligator weed to colonize a wide range of habitats. Biol Invasions 9:245–256. doi:10.1007/s10530-006-9029-1

    Article  Google Scholar 

  • Johansson ME (1994) Life history differences between central and marginal populations of the clonal aquatic plant Ranunculus lingua: a reciprocal transplant experiment. Oikos 70:65–72

    Article  Google Scholar 

  • Juenger T, Bergelson J (2000) The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance. Evolution 54:764–777. doi:10.1111/j.0014-3820.2000.tb00078.x

    PubMed  CAS  Google Scholar 

  • Julien MH, Bourne AS, Low VHK (1992) Growth of the weed Alternanthera philoxeriodes (Martius) Grisebach, (alligator weed) in aquatic and terrestrial habitats in Australia. Plant Prot Q 7:102–108

    Google Scholar 

  • Julien MH, Skarratt B, Maywald GF (1995) Potential geographical distribution of alligator weed and its biological control by Agasicles hygrophila. J Aquat Plant Manag 33:55–60

    Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. doi:10.1016/S0169-5347(02)02499-0

    Article  Google Scholar 

  • Lennartsson T, Tuomi J, Nilsson P (1997) Evidence for an evolutionary history of overcompensation in the grassland biennial Gentianella campestris (Gentianaceae). Am Nat 149:1147–1155

    Article  PubMed  CAS  Google Scholar 

  • Li W, Wang B, Wang J (2006) Lack of genetic variation of an invasive clonal plant Eichhornia crassipes in China revealed by RAPD and ISSR markers. Aquat Bot 84:176–180. doi:10.1016/j.aquabot.2005.09.008

    Article  CAS  Google Scholar 

  • Lin GL, Yang YZ, Hu JS (1990) Studies on biology and control of Alternanthera philoxeroiders. J Jiangsu Agric Coll 11:57–63

    Google Scholar 

  • Lu XM, Ding JQ (2010) Flooding compromises compensatory capacity of an invasive plant: implications for biological control. Biol Invasions 12:179–190. doi:10.1007/s10530-009-9441-4

    Article  CAS  Google Scholar 

  • Lu X, Dai H, Ding J (2010) Con-specific neighbours may enhance compensation capacity in an invasive plant. Plant Biol 12:445–452. doi:10.1111/j.1438-8677.2009.00247.x

    Article  PubMed  CAS  Google Scholar 

  • Ma RY (2001) Ecological adaptation for the intruduced biocontrol agent, Agasicles hygropghila, for Alligatorweed, Alternanthera philoxeroides, in China PhD. Chinese Academy of Agricultural Sciences, Beijing, China, p 120

    Google Scholar 

  • Mack RN, Thompson JN (1982) Evolution in steppe with few large, hooved mammals. Am Nat 119:757–773

    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. doi:10.1034/j.1600-0706.2001.950301.x

    Article  Google Scholar 

  • Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. Am Nat 134:1–19. doi:10.1086/284962

    Article  Google Scholar 

  • McIntire EJB, Hik DS (2002) Grazing history versus current grazing: leaf demography and compensatory growth of three alpine plants in response to a native herbivore (Ochotona collaris). J Ecol 90:348–359. doi:10.1046/j.1365-2745.2001.00672.x

    Article  Google Scholar 

  • McKey D, Elias M, Pujol B, Duputié A (2010) The evolutionary ecology of clonally propagated domesticated plants. New Phytol 186:318–332. doi:10.1111/j.1469-8137.2010.03210.x

    Article  PubMed  Google Scholar 

  • Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vázquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740. doi:10.1111/j.1461-0248.2006.00908.x

    Article  PubMed  Google Scholar 

  • Monro K, Poore AGB (2004) Selection in modular organisms: is intraclonal variation in macroalgae evolutionarily important? Am Nat 163:564–578. doi:10.1086/382551

    Article  PubMed  Google Scholar 

  • Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417–422. doi:10.1016/j.tree.2004.05.010

    Article  PubMed  Google Scholar 

  • Polley HW, Detling JK (1988) Herbivory tolerance of Agropyron smithii populations with different grazing histories. Oecologia 77:261–267. doi:10.1007/BF00379196

    Article  Google Scholar 

  • Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294. doi:10.1016/j.tplants.2008.03.004

    Article  PubMed  CAS  Google Scholar 

  • Sainty G, McCorkelle G, Julien M (1998) Control and spread of alligator weed Alternanthera pliloxeroides (Mart.) Griseb., in Australia: lessons for other regions. Wetlands Ecol Manage 5: 195–201. doi:10.1023/A:1008248921849

  • Schierenbeck KA, Mack RN, Sharitz RR (1994) Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera. Ecology 75:1661–1672. doi:10.2307/1939626

    Article  Google Scholar 

  • Schooler S, Baron Z, Julien M (2006) Effect of simulated and actual herbivory on alligator weed, Alternanthera philoxeroides, growth and reproduction. Biol Control 36:74–79. doi:10.1016/j.biocontrol.2005.06.012

    Article  Google Scholar 

  • Schooler SS, Yeates AG, Wilson JRU, Julien MH (2007) Herbivory, mowing, and herbicides differently affect production and nutrient allocation of Alternanthera philoxeroides. Aquat Bot 86:62068. doi:10.1016/j.aquabot.2006.09.004

    Article  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. doi:10.1098/rspb.2006.3644

    Article  PubMed  Google Scholar 

  • Smith SE (1998) Variation in response to defoliation between populations of Bouteloua curtipendula var. caespitosa (Poaceae) with different livestock grazing histories. Am J Bot 85:1266–1272

    Article  PubMed  CAS  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185. doi:10.1016/S0169-5347(98)01576-6

    Article  PubMed  Google Scholar 

  • Sun Y, Ding JQ, Ren MX (2009) Effects of simulated herbivory and resource availability on the invasive plant, Alternanthera philoxeroides in different habitats. Biol Control 48:287–293. doi:10.1016/j.biocontrol.2008.12.002

    Article  Google Scholar 

  • Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13:329–332. doi:10.1016/S0169-5347(98)01378-0

    Article  PubMed  CAS  Google Scholar 

  • Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536. doi:10.1023/A:1010881317261

    Article  Google Scholar 

  • Whitham TG, Slobodchikoff CN (1981) Evolution by individuals, plant-herbivore interactions, and mosaics of genetic variability: the adaptive significance of somatic mutations in plants. Oecologia 49:287–292

    Article  Google Scholar 

  • Wilsey BJ, Polley HW (2006) Aboveground productivity and root-shoot allocation differ between native and introduced grass species. Oecologia 150:300–309. doi:10.1007/s00442-006-0515-z

    Article  PubMed  Google Scholar 

  • Wilson JRU, Yeates A, Schooler S, Julien MH (2007) Rapid response to shoot removal by the invasive wetland plant, alligator weed (Alternanthera philoxeroides). Environ Exp Bot 60:20–25. doi:10.1016/j.envexpbot.2006.06.003

    Article  Google Scholar 

  • Yang ZH (2001) The establishment of Agasicles hygrophila population in suburb of Shanghai city. Shanghai Agric Sci 1:87–88

    Google Scholar 

  • Zangerl AR, Berenbaum MR (2005) Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proc Natl Acad Sci USA 102:15529–15532. doi:10.1073/pnas.0507805102

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Wenfeng Guo, Yi Wang, Xia Jin, Hongjun Dai, Yan Sun and Kai Wu for their field and lab assistance. The manuscript was improved by comments from Richard N. Mack, John Wilson, Heinz Müller-Schärer, David Lodge, Ashley Baldridge, Matthew Barnes, Victoria Nuzzo, Sathyamurthy Raghu, Anjana Dewanji, Jianwen Zou and three anonymous reviewers. This work was funded by the Knowledge Innovation Program of the Chinese Academy of Sciences and the National Science Foundation of China (30871650 & 31100302) while preparing this manuscript.

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Lu, X., Ding, J. History of exposure to herbivores increases the compensatory ability of an invasive plant. Biol Invasions 14, 649–658 (2012). https://doi.org/10.1007/s10530-011-0106-8

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