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Multi-generational effects of simulated herbivory and habitat types on the invasive weed Alternanthera philoxeroides: implications for biological control

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Abstract

Long-term pre-release evaluations of how invasive plants respond to herbivory in introduced ranges can help identify the most effective biological control agents. However, most evaluations have been conducted within only one generation of introduced invasive species. This study tested effects across seven generations of simulated herbivory (i.e., defoliation) and habitat types on the invasive weed Alternanthera philoxeroides. We found total biomass of A. philoxeroides was decreased by defoliation during the first three generations when grown in a simulated aquatic habitat, but was decreased by defoliation only in the first generation when grown in a simulated terrestrial habitat. Defoliation significantly decreased stem diameter and collenchyma thickness and increased cortex thickness and total phenol production in A. philoxeroides grown in a simulated terrestrial or aquatic habitat during the first generation, but showed little effect during the following six successive generations. The associations between stem anatomical structural parameters and biomass significantly differed between non-defoliation and defoliation treatments in the simulated aquatic habitat, but not in the simulated terrestrial habitat. Our results suggest simulated herbivory exerted successful biological control on A. philoxeroides during the first generation in a simulated terrestrial habitat and the first three generations in a simulated aquatic habitat, but failed to restrain the vegetative offspring of A. philoxeroides. This failure of long-term biological control on A. philoxeroides might be caused by changes in the stem anatomical structure and compensatory growth. Our study highlights the need for long-term pre-release evaluation when testing the efficiency of biological control agents.

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References

  • Ackerly DD, Dudley SA, Sultan SE et al (2000) The evolution of plant ecophysiological traits: recent advances and future directions new research addresses natural selection, genetic constraints, and the adaptive evolution of plant ecophysiological traits. Bioscience 50:979–995

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Barbehenn RV, Constabel CP (2011) Tannins in plant–herbivore interactions. Phytochemistry 72:1551–1565

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Bianka S, Thomas G, Margret S (2010) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytol 190:369–378

    Google Scholar 

  • Capinera JL, Roltsch WJ (1980) Response of wheat seedlings to actual and simulated migratory grasshopper defoliation. J Econ Entomol 73:258–261

    Google Scholar 

  • Colpetzer K, Hough-Goldstein J, Harkins KR et al (2004) Feeding and oviposition behavior of Rhinoncomimus latipes Korotyaev (Coleoptera: Curculionidae) and its predicted effectiveness as a biological control agent for Polygonum perfoliatum L. (Polygonales: Polygonaceae). Environ Entomol 33:990–996

    Google Scholar 

  • Cowie BW, Venturi G, Witkowski ETF et al (2016) Does climate constrain the spread of Anthonomus santacruzi, a biological control agent of Solanum mauritianum, in South Africa? Biol Control 101:1–7

    Google Scholar 

  • Dong BC, Aplert P, Guo W et al (2012) Effects of fragmentation on the survival and growth of the invasive, clonal plant Alternanthera philoxeroides. Biol Invasions 14:1101–1110

    Google Scholar 

  • Dong BC, Fu T, Luo FL et al (2017) Herbivory-induced maternal effects on growth and defense traits in the clonal species Alternanthera philoxeroides. Sci Total Environ 605:114–123

    PubMed  Google Scholar 

  • Du L, Yang B, Guan W et al (2016) Phenotypic variation and water selection potential in the stem structure of invasive alligator weed. Acta Oecol Int J Ecol 71:22–30

    Google Scholar 

  • Du L, Liu H, Guan W et al (2019) Drought affects the coordination of belowground and aboveground resource-related traits in Solidago canadensis in China. Ecol Evol 3:3. https://doi.org/10.1002/ece3.5536

    Article  Google Scholar 

  • Dudley SA, Schmitt J (1996) Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. Am Nat 147:445–465

    Google Scholar 

  • Fine PVA, Miller ZJ, Mesones I et al (2006) The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:S150–S162

    PubMed  Google Scholar 

  • Franks SJ, Kral AM, Pratt PD (2006) Herbivory by introduced insects reduces growth and survival of Melaleuca quinquenervia seedlings. Environ Entomol 35:366–372

    Google Scholar 

  • Gilpin M (1990) Biological invasions—a global perspective. Science 248:88–89

    CAS  PubMed  Google Scholar 

  • Gioria M, Osborne BA (2014) Resource competition in plant invasions: emerging patterns and research needs. Front Plant Sci 5:1–21

    Google Scholar 

  • Griffith TC, Paterson ID, Owen CA et al (2019) Thermal plasticity and microevolution enhance establishment success and persistence of a water hyacinth biological control agent. Entomol Exp Appl 167:616–625

    Google Scholar 

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

    Google Scholar 

  • Hogg BN, Moran PJ, Smith L (2016) Multi-generational impacts of the psyllid Arytinnis hakani (Hemiptera: Psyllidae) on growth and survival of the invasive weed Genista monspessulana. Biol Control 100:87–93

    Google Scholar 

  • Hough-Goldstein J, LaCoss SJ (2012) Interactive effects of light environment and herbivory on growth and productivity of an invasive annual vine, Persicaria perfoliata. Arthropod Plant Interact 6:103–112

    Google Scholar 

  • Huang W, Siemann E, Wheeler GS et al (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

    Google Scholar 

  • Jin Z, Li J, Zhu X (2006) Analysis of the total phenols content in differentorgans of Calycanthus chinensis from different habitat. J Anhui Agric Univ 33:454–457

    CAS  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 

  • Julien M, Sosa A, Chan R et al (2012) Alternanthera philoxeroides (Martius) Grisebach-alligator weed.  In: Julien M, McFadyen R, Cullen J (eds) Biological Control of Weeds in Australia. CSIRO Publishing, Australia, pp 43–51

  • Kumaran N, Lockett C, Dhileepan K (2018) Effect of simulated herbivory on bellyache bush (Jatropha gossypiifolia L.) growth and implications for biological control. Weed Biol Manag 18:151–159

    Google Scholar 

  • Lehtilä K, Boalt E (2004) The use and usefulness of artificial herbivory in plant-herbivore studies. In: Weisser WW, Siemann E (eds) Ecological studies, vol. 173: insects and ecosystem function. Springer, Berlin, pp 257–275

    Google Scholar 

  • Leroux O (2012) Collenchyma: a versatile mechanical tissue with dynamic cell walls. Ann Bot 110:1083–1098

    PubMed  PubMed Central  Google Scholar 

  • Li B, Tomoko S, Yasuhiro Y et al (2001) Interclonal differences, plasticity and trade-offs of life history traits of Cyperus esculentus in relation to water availability. Plant Species Biol 16:193–207

    Google Scholar 

  • Li JM, Jin ZX, Zhu XY (2007) Comparison of the total tannin in different organs of Calycanthus chinensis. Guihaia 27:944–947

    CAS  Google Scholar 

  • Louda SM, Pemberton RW, Johnson MT et al (2003) Nontarget effects—the Achilles’ heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu Rev Entomol 48:365–396

    CAS  PubMed  Google Scholar 

  • Lu X, Siemann E, Shao X et al (2013) Climate warming affects biological invasions by shifting interactions of plants and herbivores. Glob Change Biol 19:2339–2347

    Google Scholar 

  • Lu X, Siemann E, He M et al (2015) Climate warming increases biological control agent impact on a non-target species. Ecol Lett 18:48–56

    PubMed  Google Scholar 

  • Lu X, He M, Tang S et al (2019) Herbivory may promote a non-native plant invasion at low but not high latitudes. Ann Bot 124:819–827

    PubMed  PubMed Central  Google Scholar 

  • Ma R, Ding J, Wang R (2003) Population adaptability of Agasicles hygrophila on different ecotypes alligaorweed. Chin J Biol Control 19:54–58

    Google Scholar 

  • Mukherjee A, Jones JW, Cuda JP et al (2012) Effect of simulated herbivory on growth of the invasive weed Hygrophila polysperma: experimental and predictive approaches. Biol Control 60:271–279

    Google Scholar 

  • Müller-Schärer H, Schaffner U (2008) Classical biological control: exploiting enemy escape to manage plant invasions. Biol Invasions 10:859–874

    Google Scholar 

  • Nault BA, Kennedy GG (1998) Limitations of using regression and mean separation analyses for describing the response of crop yield to defoliation: a case study of the Colorado potato beetle (Coleoptera: Chrysomelidae) on potato. J Econ Entomol 91:7–20

    Google Scholar 

  • Pan X, Geng Y, Zhang W et al (2006) The influence of abiotic stress and phenotypic plasticity on the distribution of invasive Alternanthera philoxeroides along a riparian zone. Acta Oecol 30:341

    Google Scholar 

  • Raghu S, Dhileepan K (2005) The value of simulating herbivory in selecting effective weed biological control agents. Biol Control 34:265–273

    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

    Google Scholar 

  • Schwarzlander M, Hinz HL, Winston RL et al (2018) Biological control of weeds: an analysis of introductions, rates of establishment and estimates of success, worldwide. Biocontrol 63:319–331

    Google Scholar 

  • Sun Y, Ding J, Ren M (2009) Effects of simulated herbivory and resource availability on the invasive plant, Alternanthera philoxeroides in different habitats. Biol Control 48:287–293

    Google Scholar 

  • Sutton GF, Klein H, Paterson ID (2018) Evaluating the efficacy of Hypogeococcus sp as a biological control agent of the cactaceous weed Cereus jamacaru in South Africa. Biocontrol 63:493–503

    Google Scholar 

  • Thomas MB, Reid AM (2007) Are exotic natural enemies an effective way of controlling invasive plants? Trends Ecol Evol 22:447–453

    PubMed  Google Scholar 

  • Tong W, Hu J, Wang R et al (2018) Tolerance and resistance facilitate the invasion success of Alternanthera philoxeroides in disturbed habitats: a reconsideration of the disturbance hypothesis in the light of phenotypic variation. Environ Exp Bot 153:135–142

    Google Scholar 

  • TrumbleKolodny-Hirsch JTDM, Ting IP (2003) Plant compensation for arthropod herbivory. Annu Rev Entomol 38:93–120

    Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL et al (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Wan JL, Huang B, Yu H et al (2019) Reassociation of an invasive plant with its specialist herbivore provides a test of the shifting defence hypothesis. J Ecol 107:361–371

    Google Scholar 

  • Wang N, Yu FH, Li PX et al (2009) Clonal integration supports the expansion from terrestrial to aquatic environments of the amphibious stoloniferous herb Alternanthera philoxeroides. Plant Biol 11:483–489

    CAS  PubMed  Google Scholar 

  • Wei H, Lu X, Ding J (2015) Direct and indirect impacts of different water regimes on the invasive plant, alligator weed (Alternanthera philoxeroides), and its biological control agent, Agasicles hygrophila. Weed Biol Manag 15:1–10

    Google Scholar 

  • Williams DG, Mack RN, Black RA (1995) Ecophysiology of introduced Pennisetum setaceum on Hawaii: the role of phenotypic plasticity. Ecology 76:1569–1580

    Google Scholar 

  • Williamson M (1996) Biological Invasions. In: Usher MB, Deangelis DL, Manly BJF (eds) Population and Community Biology Series 15. Chapman & Hall, London, pp 1–244

  • Xiong S, Zuo X, Zhu Y (2005) Determination of cellulose, hemicellulose and lignin in rice husk. Cereal Feed Ind 5:40–41

  • Yu H, Fan S (2018) Differences in physiological traits and resistances of Alternanthera philoxeroides after herbivory by generalists and specialists. Aquat Ecol 52:323–332

    CAS  Google Scholar 

  • Zhen S, Ruihai Z, Guoliang Z et al (2018) The effect of Agasicles hygrophila release on the control of Alternanthera philoxeroides. Ecol Environ Sci 28:2033–2038

    Google Scholar 

  • Zong N, Shi P (2019) Nitrogen addition stimulated compensatory growth responses to clipping defoliation in a Northern Tibetan alpine meadow. Grassl Sci 65:60–68

    CAS  Google Scholar 

  • Zuo SP, Ma YQ, Shinobu I (2012) Differences in ecological and allelopathic traits among Alternanthera philoxeroides populations. Weed Biol Manag 12:123–130

    Google Scholar 

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Acknowledgements

This study was financially supported by the Ten Thousand Talent Program of Zhejiang Province (2019R52043), the National Key Research and Development Program of China (No. 2016YFC1201100) and the National Natural Science Foundation of China (No. 31270461).

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JL directed the research. SG conducted the experiments. YY analyzed data. JL, MY and YY prepared the manuscript.

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Correspondence to Junmin Li.

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Yuan, Y., Guo, S., Yan, M. et al. Multi-generational effects of simulated herbivory and habitat types on the invasive weed Alternanthera philoxeroides: implications for biological control. Biol Invasions 23, 2109–2123 (2021). https://doi.org/10.1007/s10530-021-02491-x

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