Advertisement

Arthropod-Plant Interactions

, Volume 12, Issue 5, pp 691–700 | Cite as

Strong effects of hydrologic environment and weak effects of elevated CO2 on the invasive weed Alternanthera philoxeroides and the biocontrol beetle Agasicles hygrophila

  • James W. Henriksen
  • Dana S. Lim
  • Xinmin Lu
  • Jianqing Ding
  • Evan Siemann
Original Paper
  • 43 Downloads

Abstract

Global change, such as elevated CO2, may alter interactions between invasive plants and biocontrol agents, impacting biocontrol efficacy. Here, we conducted four experiments in Texas, USA to test how elevated CO2 influences an invasive plant (Alternanthera philoxeroides) and its interactions with an introduced biocontrol beetle (Agasicles hygrophila) in terrestrial (well-watered) and flooded environments. We grew plants for 9 months in ambient or elevated CO2 (800 ppm) chambers in continuously flooded or well-watered conditions. In no-choice trials, flooding increased leaf toughness and decreased beetle consumption but beetles only oviposited on ambient CO2 leaves. In choice trials, beetles preferred to feed and oviposit on terrestrial plants but were also less likely to damage elevated CO2 leaves. Caged beetle populations were larger in terrestrial conditions than aquatic conditions for a second set of plants grown in the chambers. With a third set of plants grown in the ambient or elevated CO2 chambers, damage for plants placed in the field (aquatic setting) was higher for plants grown in terrestrial conditions vs. flooded conditions at ambient CO2. Our results suggest that elevated CO2 will have minor effects on the efficacy of this biocontrol agent by decreasing oviposition and number of leaves damaged, and hydrologic environment may affect invasive plant performance by altering herbivore oviposition and feeding preferences. A broader understanding of the effects of global change on biocontrol will help prevent and manage future spread of invasive plants.

Keywords

Alligator weed Alligator weed flea beetle Biocontrol Carbon dioxide Climate change 

Notes

Acknowledgements

We would like to thank Stephen Truch, Kate Snyder, and Hong Wang for their help in field and lab work and financial support from NSF-China (NSF-C 31370547 & 31570540) and a Spurlino Fellowship.

References

  1. Agrell J, McDonald EP, Lindroth RL (2000) Effects of CO2 and light on tree phytochemistry and insect performance. Oikos 88:259–272.  https://doi.org/10.1034/j.1600-0706.2000.880204.x CrossRefGoogle Scholar
  2. Aguilar-Fenollosa E, Jacas JA (2014) Can we forecast the effects of climate change on entomophagous biological control agents? Pest Manag Sci 70:853–859.  https://doi.org/10.1002/ps.3678 CrossRefPubMedGoogle Scholar
  3. Block A, Vaughan MM, Christensen SA, Alborn HT, Tumlinson JH (2017) Elevated carbon dioxide reduces emission of herbivore-induced volatiles in Zea mays. Plant Cell Environ 40:1725–1734.  https://doi.org/10.1111/pce.12976 CrossRefPubMedGoogle Scholar
  4. Boullis A, Francis F, Verheggen FJ (2015) Climate change and tritrophic interactions: will modifications to greenhouse gas emissions increase the vulnerability of herbivorous insects to natural enemies? Environ Entomol 44:277–286.  https://doi.org/10.1093/ee/nvu019 CrossRefPubMedGoogle Scholar
  5. Caplan JS, Hager RN, Megonigal JP, Mozdzer TJ (2015) Global change accelerates carbon assimilation by a wetland ecosystem engineer. Environ Res Lett 10:12.  https://doi.org/10.1088/1748-9326/10/11/115006 CrossRefGoogle Scholar
  6. Carson WP, Hovick SM, Baumert AJ, Bunker DE, Pendergast TH (2008) Evaluating the post-release efficacy of invasive plant biocontrol by insects: a comprehensive approach. Arthropod Plant Interact 2:77–86.  https://doi.org/10.1007/s11829-008-9036-5 CrossRefGoogle Scholar
  7. Clewley GD, Eschen R, Shaw RH, Wright DJ (2012) The effectiveness of classical biological control of invasive plants. J Appl Ecol 49:1287–1295.  https://doi.org/10.1111/j.1365-2664.2012.02209.x CrossRefGoogle Scholar
  8. Dader B, Fereres A, Moreno A, Trebicki P (2016) Elevated CO2 impacts bell pepper growth with consequences to Myzus persicae life history, feeding behaviour and virus transmission ability. Sci Rep.  https://doi.org/10.1038/srep19120 CrossRefPubMedPubMedCentralGoogle Scholar
  9. de Graaff M-A, van Groenigen K-J, Six J, Hungate B, van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Change Biol 12:2077–2091.  https://doi.org/10.1111/j.1365-2486.2006.01240.x CrossRefGoogle Scholar
  10. DeLucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant-insect interactions. Plant Physiol 160:1677–1685.  https://doi.org/10.1104/pp.112.204750 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Facey SL, Ellsworth DS, Staley JT, Wright DJ, Johnson SN (2014) Upsetting the order: how climate and atmospheric change affects herbivore-enemy interactions. Curr Opin Insect Sci 5:66–74.  https://doi.org/10.1016/j.cois.2014.09.015 CrossRefGoogle Scholar
  12. Fernandez PC, Meiners T, Bjorkman C, Hilker M (2007) Electrophysiological responses of the blue willow leaf beetle, Phratora vulgatissima, to volatiles of different Salix viminalis genotypes. Entomol Exp Appl 125:157–164.  https://doi.org/10.1111/j.1570-7458.2007.00611.x CrossRefGoogle Scholar
  13. Fleming JP, Dibble ED (2015) Ecological mechanisms of invasion success in aquatic macrophytes. Hydrobiol 746:23–37.  https://doi.org/10.1007/s10750-014-2026-y CrossRefGoogle Scholar
  14. Gherlenda AN, Moore BD, Haigh AM, Johnson SN, Riegler M (2016) Insect herbivory in a mature Eucalyptus woodland canopy depends on leaf phenology but not CO2 enrichment. BMC Ecol.  https://doi.org/10.1186/s12898-016-0102-z CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hammack L (1996) Corn volatiles as attractants for northern and western corn rootworm beetles (Coleoptera: Chrysomelidae: Diabrotica spp). J Chem Ecol 22:1237–1253.  https://doi.org/10.1007/bf02266963 CrossRefPubMedGoogle Scholar
  16. Himanen SJ, Nerg A-M, Nissinen A, Pinto DM, Stewart CN Jr, Poppy GM, Holopainen JK (2009) Effects of elevated carbon dioxide and ozone on volatile terpenoid emissions and multitrophic communication of transgenic insecticidal oilseed rape (Brassica napus). New Phytol 181:174–186.  https://doi.org/10.1111/j.1469-8137.2008.02646.x CrossRefPubMedGoogle Scholar
  17. Hulme PE (2015) Invasion pathways at a crossroad: policy and research challenges for managing alien species introductions. J Appl Ecol 52:1418–1424.  https://doi.org/10.1111/1365-2664.12470 CrossRefGoogle Scholar
  18. Jablonski LM, Wang XZ, Curtis PS (2002) Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytol 156:9–26.  https://doi.org/10.1046/j.1469-8137.2002.00494.x CrossRefGoogle Scholar
  19. Jamieson MA, Burkle LA, Manson JS, Runyon JB, Trowbridge AM, Zientek J (2017) Global change effects on plant-insect interactions: the role of phytochemistry. Curr Opin Insect Sci 23:70–80.  https://doi.org/10.1016/j.cois.2017.07.009 CrossRefPubMedGoogle Scholar
  20. Jasoni R et al (2004) Altered leaf and root emissions from onion (Allium cepa L.) grown under elevated CO2 conditions. Environ Exp Bot 51:273–280.  https://doi.org/10.1016/j.envexpbot.2003.11.006 CrossRefGoogle Scholar
  21. Julien MH, Skarratt B, Maywald GF (1995) Potential geographical distribution of alligator weed and its biological control by Agasicles hygrophila. J Aquat Plant Manag 33:55–60Google Scholar
  22. Khelfane-Goucem K, Medjdoub-Bensaad F, Leppik E, Frerot B (2014) Dry bean volatile organic compounds mediating host choice in Acanthoscelides obtectus Say (Coleoptera: Chrysomelidae: Bruchinae). Ann Soc Entomol Fr 50:167–176.  https://doi.org/10.1080/00379271.2014.938547 CrossRefGoogle Scholar
  23. Landosky JM, Karowe DN (2014) Will chemical defenses become more effective against specialist herbivores under elevated CO2? Glob Change Biol 20:3159–3176.  https://doi.org/10.1111/gcb.12633 CrossRefGoogle Scholar
  24. Li N, Li S, Ge J, Schuman MC, Wei JN, Ma RY (2017) Manipulating two olfactory cues causes a biological control beetle to shift to non-target plant species. J Ecol 105:1534–1546.  https://doi.org/10.1111/1365-2745.12778 CrossRefGoogle Scholar
  25. Liu JP, Huang WK, Chi H, Wang CH, Hua HX, Wu G (2017) Effects of elevated CO2 on the fitness and potential population damage of Helicoverpa armigera based on two-sex life table. Sci Rep.  https://doi.org/10.1038/s41598-017-01257-7 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lu X, Siemann E, Shao X, Wei H, Ding J (2013) Climate warming affects biological invasions by shifting interactions of plants and herbivores. Global Change Biol 19:2339–2347.  https://doi.org/10.1111/gcb.12244 CrossRefGoogle Scholar
  27. Lu X, Siemann E, He M, Wei H, Shao X, Ding J (2015) Climate warming increases biological control agent impact on a non-target species. Ecol Lett 18:48–56.  https://doi.org/10.1111/ele.12391 CrossRefPubMedGoogle Scholar
  28. Ma R-Y, Jia X-Y, Liu W-Z, Laushman RH, Zhao L-L, Jia D, Wang R (2013) Sequential loss of genetic variation in flea beetle Agasicles hygrophila (Coleoptera: Chrysomelidae) following introduction into China. Insect Sci 20:655–661.  https://doi.org/10.1111/1744-7917.12025 CrossRefPubMedGoogle Scholar
  29. Mroczek A (2015) Phytochemistry and bioactivity of triterpene saponins from Amaranthaceae family. Phytochem Rev 14:577–605.  https://doi.org/10.1007/s11101-015-9394-4 CrossRefGoogle Scholar
  30. Pan X, Geng Y, Zhang W, Li B, Chen J (2006) The influence of abiotic stress and phenotypic plasticity on the distribution of invasive Alternanthera philoxeroides along a riparian zone. Acta Oecol 30:333–341.  https://doi.org/10.1016/j.actao.2006.03.003 CrossRefGoogle Scholar
  31. Reeves JL, Blumenthal DM, Kray JA, Derner JD (2015) Increased seed consumption by biological control weevil tempers positive CO2 effect on invasive plant (Centaurea diffusa) fitness. Biol Control 84:36–43.  https://doi.org/10.1016/j.biocontrol.2015.02.005 CrossRefGoogle Scholar
  32. Robinson EA, Ryan GD, Newman JA (2012) A meta-analytical review of the effects of elevated CO2 on plant-arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336.  https://doi.org/10.1111/j.1469-8137.2012.04074.x CrossRefPubMedGoogle Scholar
  33. Sage RF, Sage TL, Pearcy RW, Borsch T (2007) The taxonomic distribution of C4 photosynthesis in Amaranthaceae sensu stricto. Am J Bot 94:1992–2003.  https://doi.org/10.3732/ajb.94.12.1992 CrossRefPubMedGoogle Scholar
  34. SAS (2012) SAS Institute Inc., Cary, NC, USAGoogle Scholar
  35. Sharma HC, War AR, Pathania M, Sharma SP, Akbar SM, Munghate RS (2016) Elevated CO2 influences host plant defense response in chickpea against Helicoverpa armigera. Arthropod Plant Interact 10:171–181.  https://doi.org/10.1007/s11829-016-9422-3 CrossRefGoogle Scholar
  36. Spencer NR, Coulson JR (1976) The biological control of alligator-weed, Alternanthera philoxeroides, in the United States of America. Aquat Bot 2:177–190.  https://doi.org/10.1016/0304-3770(76)90019-x CrossRefGoogle Scholar
  37. Terrer C et al (2018) Ecosystem responses to elevated CO2 governed by plant-soil interactions and the cost of nitrogen acquisition. New Phytol 217:507–522.  https://doi.org/10.1111/nph.14872 CrossRefPubMedGoogle Scholar
  38. Thomas MB, Reid AM (2007) Are exotic natural enemies an effective way of controlling invasive plants? Trends Ecol Evol 22:447–453.  https://doi.org/10.1016/j.tree.2007.03.003 CrossRefPubMedGoogle Scholar
  39. Vila M et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708.  https://doi.org/10.1111/j.1461-0248.2011.01628.x CrossRefPubMedGoogle Scholar
  40. Wang BR, Li WG, Wang JB (2005) Genetic diversity of Alternanthera philoxeroides in China. Aquat Bot 81:277–283.  https://doi.org/10.1016/j.aquabot.2005.01.004 CrossRefGoogle Scholar
  41. Wei H, Lu XM, Ding JQ (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 Manage 15:1–10.  https://doi.org/10.1111/wbm.12055 CrossRefGoogle Scholar
  42. Wolf VC, Gassmann A, Muller C (2012) Choice behaviour and performance of Cassida stigmatica on various chemotypes of Tanacetum vulgare and implications for biocontrol. Entomol Exp Appl 144:78–85.  https://doi.org/10.1111/j.1570-7458.2012.01242.x CrossRefGoogle Scholar
  43. Wu H, Carrillo J, Ding JQ (2017) Species diversity and environmental determinants of aquatic and terrestrial communities invaded by Alternanthera philoxeroides. Sci Total Environ 581:666–675.  https://doi.org/10.1016/j.scitotenv.2016.12.177 CrossRefPubMedGoogle Scholar
  44. Wundrow EJ, Carrillo J, Gabler CA, Horn KC, Siemann E (2012) Facilitation and competition among invasive plants: a field experiment with alligatorweed and water hyacinth. PLoS ONE.  https://doi.org/10.1371/journal.pone.0048444 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Xie HC, Zhao L, Yang QF, Wang ZY, He KL (2015) Direct effects of elevated CO2 levels on the fitness performance of Asian corn borer (Lepidoptera: Crambidae) for multigenerations. Environ Entomol 44:1250–1257.  https://doi.org/10.1093/ee/nvv102 CrossRefPubMedGoogle Scholar
  46. Xu C-Y et al (2009) The growth response of Alternanthera philoxeroides in a simulated post-combustion emission with ultrahigh CO2 and acidic pollutants. Environ Pollut 157:2118–2125.  https://doi.org/10.1016/j.envpol.2009.02.013 CrossRefPubMedGoogle Scholar
  47. Yuan JS, Himanen SJ, Holopainen JK, Chen F, Stewart CN Jr (2009) Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol Evol 24:323–331.  https://doi.org/10.1016/j.tree.2009.01.012 CrossRefPubMedGoogle Scholar
  48. Zavala JA, Nabity PD, DeLucia EH (2013) An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu Rev Entomol 58:79–97.  https://doi.org/10.1146/annurev-ento-120811-153544 CrossRefPubMedGoogle Scholar
  49. Zavala JA, Gog L, Giacometti R (2017) Anthropogenic increase in carbon dioxide modifies plant-insect interactions. Ann Appl Biol 170:68–77.  https://doi.org/10.1111/aab.12319 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • James W. Henriksen
    • 1
  • Dana S. Lim
    • 1
  • Xinmin Lu
    • 1
    • 2
    • 3
  • Jianqing Ding
    • 2
    • 4
  • Evan Siemann
    • 1
  1. 1.Biosciences DepartmentRice UniversityHoustonUSA
  2. 2.Key Laboratory of Aquatic Botany and Watershed Ecology Wuhan Botanical Institute/Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  3. 3.School of Life SciencesCentral China Normal UniversityWuhanChina
  4. 4.School of Life SciencesHenan UniversityKaifengChina

Personalised recommendations