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Biological Invasions

, Volume 21, Issue 1, pp 67–83 | Cite as

Enemy of my enemy: evidence for variable soil biota feedbacks of Vincetoxicum rossicum on native plants

  • Angela E. Dukes
  • Akihiro Koyama
  • Kari E. Dunfield
  • Pedro M. AntunesEmail author
Original Paper

Abstract

Interactions between plants and soil biota can be major drivers of plant invasions. The ‘Enemy of my enemy’ hypothesis (EEH) predicts that native plants are more negatively impacted by enemies (e.g. pathogens) that accumulate and spillover from the invader’s rhizosphere than the invaders themselves, thereby facilitating the invasion. We tested EEH using Vincetoxicum rossicum, one of the most invasive plant species in Eastern North America, and a total of eight co-occuring native plant species. Specifically, we predicted that the native species would grow less in presence of soil biota associated with V. rossicum than that from uninvaded soils. Field soils were collected from four V. rossicum invaded and neighboring uninvaded areas for use in two experiments. In Experiment 1, V. rossicum and each of five native plant species were grown in a plant growth chamber for 3 months, either in presence or absence of soil biota from the invaded and uninvaded soils. We found that only one species (Solidago canadensis) supported EEH. In contrast, the legume Desmodium canadense more than doubled its biomass in response to V. rossicum -associated soil biota. In Experiment 2, four native legume species, including D. canadense, were examined for EEH in the same manner as in Experiment 1. Only one species (Lespedeza hirta) supported EEH and, again, V. rossicum-associated soil biota was advantageous to D. canadense. In summary, we found inconsistent support for the EEH between V. rossicum and native co-occurring species in Eastern North America. We conclude that the accumulation of rhizosphere enemies in native plants may not be a major factor in the invasive success of V. rossicum.

Keywords

Vincetoxicum rossicum Enemy of my enemy hypothesis Accumulation of local pathogens Plant-soil feedback Plant invasions Desmodium canadense 

Notes

Acknowledgements

This research was conducted in Robinson-Huron Treaty territory and the traditional territory of the Anishnaabeg, specifically the Garden River and Batchewana First Nations, as well as Métis People. We thank Jamie Davidson (Central Lake Ontario Conservation Authority), Ken Towle (Ganaraska Region Conservation Authority), John Standeven (Orono Crown Lands), Elizabeth Heighington (Toronto Zoo), and Bohdan Kowalyk (Ontario Ministry of Natural Resources) for site information and access; Dr. Hafiz Maherali for advice on phylogenetic analysis; Ontario Forest Research Institute, in particular Darren Derbowka and Kevin Maloney, for technical assistance and infrastructure access; Susan Meades, curator of the Northern Ontario Plant Database, for support with plant identification. Funding was provided by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) and a Canada Research Chair to PMA.

Author contributions

All authors contributed to designing the experiment. A. Dukes conducted the experiments. A. Dukes and A. Koyama analyzed the data. A. Koyama, P.M Antunes and A. Dukes wrote the manuscript. All authors approved the final article.

Funding

This work was funded through an Ontario Graduate Scholarship and bursaries from the University of Guelph to A. Dukes and a NSERC Discovery Grant and a Canada Research Chair awarded to P.M. Antunes.

Supplementary material

10530_2018_1804_MOESM1_ESM.docx (300 kb)
Supplementary material 1 (DOCX 299 kb)

References

  1. Anacker BL, Klironomos JN, Maherali H, Reinhart KO, Strauss SY (2014) Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance. Ecol Lett 17(12):1613–1621.  https://doi.org/10.1111/ele.12378 CrossRefGoogle Scholar
  2. Antunes PM, Rajcan I, Goss MJ (2006) Specific flavonoids as interconnecting signals in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium japonicum (Kirchner) Jordan and soybean (Glycine max (L.) Merr.). Soil Biol Biochem 38(3):533–543.  https://doi.org/10.1016/j.soilbio.2005.06.008 CrossRefGoogle Scholar
  3. Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515(7528):505–511.  https://doi.org/10.1038/nature13855 CrossRefGoogle Scholar
  4. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20(11):634–641.  https://doi.org/10.1016/j.tree.2005.08.005 CrossRefGoogle Scholar
  5. Bongard CL, Navaranjan G, Yan W, Fulthorpe RR (2013) Fungal colonization of the invasive vine Vincetoxicum rossicum and native plants. Plant Ecol Evol 146(1):45–52.  https://doi.org/10.5091/plecevo.2013.739 CrossRefGoogle Scholar
  6. Bradley JD (2013) Southern Ontario vascular plant species list. Ontario Ministry of Natural Resources. Queen’s Printer for Ontario. http://www.forestry.utoronto.ca/Settledlandscapes/VSP/documents/SouthOntPlantList_Scientific.pdf. Accessed 18 Feb 2015
  7. Brandt AJ, Seabloom EW, Hosseini PR (2009) Phylogeny and provenance affect plant-soil feedbacks in invaded California grasslands. Ecology 90(4):1063–1072.  https://doi.org/10.1890/08-0054.1 CrossRefGoogle Scholar
  8. Butchart SHM, Walpole M, Collen B, Van Strien A, Scharlemann JPW, Almond REA, Baillie JEM, Bomhard B, Brown C, Bruno J, Carpenter KE, Carr GM, Chanson J, Chenery AM, Csirke J, Davidson NC, Dentener F, Foster M, Galli A, Galloway JN, Genovesi P, Gregory RD, Hockings M, Kapos V, Lamarque JF, Leverington F, Loh J, Mcgeoch MA, Mcrae L, Minasyan A, Morcillo MH, Oldfield TEE, Pauly D, Quader S, Revenga C, Sauer JR, Skolnik B, Spear D, Stanwell-Smith D, Stuart SN, Symes A, Tierney M, Tyrrell TD, Vié J-C, Watson R (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168.  https://doi.org/10.1126/science.1187512 CrossRefGoogle Scholar
  9. Cahill JF, Cale JA, Karst J, Bao T, Pec GJ, Erbilgin N (2016) No silver bullet: different soil handling techniques are useful for different research questions, exhibit differential type I and II error rates, and are sensitive to sampling intensity. New Phytol 216(1):11–14.  https://doi.org/10.1111/nph.14141 CrossRefGoogle Scholar
  10. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  11. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733.  https://doi.org/10.1038/nature02322 CrossRefGoogle Scholar
  12. Callaway RM, Cipollini D, Barto K et al (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055CrossRefGoogle Scholar
  13. Callaway RM, Montesinos D, Williams K, Maron JL (2013) Native congeners provide biotic resistance to invasive Potentilla through soil biota. Ecology 94(6):1223–1229.  https://doi.org/10.1890/12-1875.1 CrossRefGoogle Scholar
  14. Cappuccino N, Mackay R, Eisner C (2002) Spread of the invasive alien vine Vincetoxicum rossicum: tradeoffs between seed dispersability and seed quality. Am Midl Nat 148(2):263.  https://doi.org/10.1674/0003-0031(2002)148[0263:SOTIAV]2.0.CO;2 CrossRefGoogle Scholar
  15. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67.  https://doi.org/10.1038/nature11148 CrossRefGoogle Scholar
  16. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7(8):721–733.  https://doi.org/10.1111/j.1461-0248.2004.00616.x CrossRefGoogle Scholar
  17. Crins WJ, Gray PA, Uhlig PWC, Wester MC (2009) The ecosystems of Ontario, part 1: ecozones and ecoregions. Technical Report SIB TER IMA TR-01. Ministry of Natural Resources. Ontario Ministry of Natural Resources, Science & Information Branch Inventory, Monitoring and Assessment Section. Technical Report SIB TER IMA TR-01, Peterborough, CanadaGoogle Scholar
  18. Day NJ, Antunes PM, Dunfield KE (2015a) Changes in arbuscular mycorrhizal fungal communities during invasion by an exotic invasive plant. Acta Oecol 67:66–74.  https://doi.org/10.1016/j.actao.2015.06.004 CrossRefGoogle Scholar
  19. Day NJ, Dunfield KE, Antunes PM (2015b) Temporal dynamics of plant-soil feedback and root-associated fungal communities over 100 years of invasion by a non-native plant. J Ecol 103(6):1557–1569.  https://doi.org/10.1111/1365-2745.12459 CrossRefGoogle Scholar
  20. Day NJ, Dunfield KE, Antunes PM (2016) Fungi from a non-native invasive plant increase its growth but have different growth effects on native plants. Biol Invasions 18(1):231–243.  https://doi.org/10.1007/s10530-015-1004-2 CrossRefGoogle Scholar
  21. DiTommaso A, Lawlor FM, Darbyshire SJ (2005) The biology of invasive alien plants in Canada. 2. Cynanchum rossicum (Kleopow) Borhidi [= Vincetoxicum rossicum (Kleopow) Barbar] and Cynanchum louiseae (L.) Kartesz and Gandhi [= Vincetoxicum nigrum (L.) Moench]. Can J Plant Sci 85(1):243–263.  https://doi.org/10.4141/P03-056 CrossRefGoogle Scholar
  22. Early R, Bradley BA, Dukes JS, Lawler JJ, Olden JD, Blumenthal DM, Gonzalez P, Grosholz ED, Ibañez I, Miller LP, Sorte CJB, Tatem AJ (2016) Global threats from invasive alien species in the twenty-first century and national response capacities. Nat Commun.  https://doi.org/10.1038/ncomms12485 Google Scholar
  23. Eppinga MB, Rietkerk M, Dekker SC, De Ruiter PC, van der Putten WH (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114(1):168–176.  https://doi.org/10.1111/j.2006.0030-1299.14625.x CrossRefGoogle Scholar
  24. Ernst CM, Cappuccino N (2005) The effect of an invasive alien vine, Vincetoxicum rossicum (Asclepiadaceae), on arthropod populations in Ontario old fields. Biol Invasions 7(3):417–425.  https://doi.org/10.1007/s10530-004-4062-4 CrossRefGoogle Scholar
  25. Feng Y, van Kleunen M (2016) Phylogenetic and functional mechanisms of direct and indirect interactions among alien and native plants. J Ecol 104(4):1136–1148.  https://doi.org/10.1111/1365-2745.12577 CrossRefGoogle Scholar
  26. Fitzpatrick CR, Gehant L, Kotanen PM, Johnson MTJ (2017) Phylogenetic relatedness, phenotypic similarity and plant-soil feedbacks. J Ecol 105(3):786–800.  https://doi.org/10.1111/1365-2745.12709 CrossRefGoogle Scholar
  27. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446(7139):1079–1081.  https://doi.org/10.1038/nature05719 CrossRefGoogle Scholar
  28. Gilbert B, Levine JM (2013) Plant invasions and extinction debts. Proc Natl Acad Sci USA 110(5):1744–1749.  https://doi.org/10.1073/pnas.1212375110 CrossRefGoogle Scholar
  29. Greipsson S, DiTommaso A (2006) Invasive non-native plants alter the occurrence of arbuscular mycorrhizal fungi and benefit from this association. Ecol Restor 24(4):236–241.  https://doi.org/10.3368/er.24.4.236 CrossRefGoogle Scholar
  30. Gu J, Wang ET, Chen WX (2007) Genetic diversity of rhizobia associated with Desmodium species grown in China. Lett Appl Microbiol 44(3):286–292.  https://doi.org/10.1111/j.1472-765X.2006.02071.x CrossRefGoogle Scholar
  31. Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105.  https://doi.org/10.1038/nature11118 CrossRefGoogle Scholar
  32. Inderjit, van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25(9):512–519.  https://doi.org/10.1016/j.tree.2010.06.006 CrossRefGoogle Scholar
  33. Jordan NR, Larson DL, Huerd SC (2008) Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol Invasions 10(2):177–190CrossRefGoogle Scholar
  34. Karst J, Erbilgin N, Pec GJ, Cigan PW, Najar A, Simard SW, Cahill JF (2015) Ectomycorrhizal fungi mediate indirect effects of a bark beetle outbreak on secondary chemistry and establishment of pine seedlings. New Phytol 208(3):904–914.  https://doi.org/10.1111/nph.13492 CrossRefGoogle Scholar
  35. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  36. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417(6884):67–70.  https://doi.org/10.1038/417067a CrossRefGoogle Scholar
  37. Knevel I, Lans T, Menting FJ, Hertling U, van der Putten WH (2004) Release from native root herbivores and biotic resistance by soil pathogens in a new habitat both affect the alien Ammophila arenaria in South Africa. Oecologia 141:502–510.  https://doi.org/10.1007/s00442-004-1662-8 CrossRefGoogle Scholar
  38. Luque GM, Bellard C, Bertelsmeier C, Bonnaud E, Genovesi P, Simberloff D, Courchamp F (2014) The 100th of the world’s worst invasive alien species. Biol Invasions 16:981–985.  https://doi.org/10.1007/s10530-013-0561-5 CrossRefGoogle Scholar
  39. Magidow LC, DiTommaso A, Ketterings QM, Mohler CL, Milbrath LR (2013) Emergence and performance of two invasive swallowworts (Vincetoxicum spp.) in contrasting soil types and soil pH. Invasive Plant Science and Management 6(2):281–291.  https://doi.org/10.1614/IPSM-D-12-00073.1 CrossRefGoogle Scholar
  40. Malcolm SB, Cockrell BJ, Brower LP (1993) Spring recolonization of eastern North America by the monarch butterfly: successive brood or single sweep migration? In: Biology and conservation of the monarch butterfly. Natural History Museum of Los Angeles County; Science Series, p 38Google Scholar
  41. Mangla S, Inderjit, Callaway RM (2008) Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol 96:58–67.  https://doi.org/10.1111/j.1365-2745.2007.01312.x Google Scholar
  42. Martínez-García LB, Pietrangelo O, Antunes PM (2016) Parent tree distance-dependent recruitment limitation of native and exotic invasive seedlings in urban forests. Urban Ecosyst 19(2):969–981.  https://doi.org/10.1007/s11252-015-0507-z CrossRefGoogle Scholar
  43. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115(3):495–501.  https://doi.org/10.1111/j.1469-8137.1990.tb00476.x CrossRefGoogle Scholar
  44. Mitchell CE (2003) Trophic control of grassland production and biomass by pathogens. Ecol Lett 6(2):147–155.  https://doi.org/10.1046/j.1461-0248.2003.00408.x CrossRefGoogle Scholar
  45. Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248.  https://doi.org/10.1016/j.funeco.2015.06.006 CrossRefGoogle Scholar
  46. Ontario Geological Survey (1991) Bedrock geology of Ontario, Southern sheet; Ontario Geological Survey, Map2544, Scale 1:1 000 000Google Scholar
  47. Padilla FM, Pugnaire FI (2006) The role of nurse plants in the restoration of degraded environments. Front Ecol Environ 4(4):196–202CrossRefGoogle Scholar
  48. Parker MA, Jankowiak JG, Landrigan GK (2015) Diversifying selection by Desmodiinae legume species on Bradyrhizobium symbionts. FEMS Microbiol Ecol.  https://doi.org/10.1093/femsec/fiv075 Google Scholar
  49. Power AG, Mitchell CE (2004) Pathogen spillover in disease epidemics. Am Nat 164(Suppl):S79–S89.  https://doi.org/10.1086/424610 CrossRefGoogle Scholar
  50. R Core Team (2017) R: a language and environment for statistical computing, R version 3.4.3. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 15 Jan 2018
  51. Reinhart KO, Rinella MJ (2016) A common soil handling technique can generate incorrect estimates of soil biota effects on plants. New Phytol 210(3):786–789.  https://doi.org/10.1111/nph.13822 CrossRefGoogle Scholar
  52. Reinhart KO, Packer A, Van der Putten WH et al (2003) Plant–soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol Lett 6:1046–1050CrossRefGoogle Scholar
  53. Sanderson LA, Day NJ, Antunes PM (2015) Edaphic factors and feedback do not limit range expansion of an exotic invasive plant. Plant Ecol 216(1):133–141.  https://doi.org/10.1007/s11258-014-0422-z CrossRefGoogle Scholar
  54. Sanon A, Beguiristain T, Cebron A, Berthelin J, Ndoye I, Leyval C, Sylla S, Duponnois R (2009) Changes in soil diversity and global activities following invasions of the exotic invasive plant, Amaranthus viridis L., decrease the growth of native sahelian Acacia species. FEMS Microbiol Ecol 70(1):118–131CrossRefGoogle Scholar
  55. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682.  https://doi.org/10.1038/nmeth.2019 CrossRefGoogle Scholar
  56. Schnitzer SA, Klironomos JN, HilleRisLambers J, Kinkel LL, Reich PB, Xiao K, Rillig MC, Sikes BA, Callaway RM, Mangan SA, Van Nes EH, Scheffer M (2011) Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92(2):296–303.  https://doi.org/10.1890/10-0773.1 CrossRefGoogle Scholar
  57. Sheeley SE, Raynal DJ (1996) The distribution and status of species of Vincetoxicum in eastern North America. Bull Torrey Bot Club 123:148–156CrossRefGoogle Scholar
  58. Smith LL, DiTommaso A, Lehmann J, Greipsson S (2008) Effects of arbuscular mycorrhizal fungi on the exotic invasive vine pale swallow-wort (Vincetoxicum rossicum). Invasive Plant Science and Management. 1(2):142–152.  https://doi.org/10.1614/IPSM-07-010.1 CrossRefGoogle Scholar
  59. St Denis M, Cappuccino N (2004) Reproductive biology of Vincetoxicum rossicum (Kleo.) Barb. (Asclepiadaceae), an invasive alien in Ontario. J Torrey Bot Soc 131(1):8–15.  https://doi.org/10.2307/4126923 CrossRefGoogle Scholar
  60. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4(5):e140.  https://doi.org/10.1371/journal.pbio.0040140 CrossRefGoogle Scholar
  61. Suding KN, Harpole WS, Fukami T, Kulmatiski A, MacDougall AS, Stein C, van der Putten WH (2013) Consequences of plant–soil feedbacks in invasion. J Ecol 101(2):298–308CrossRefGoogle Scholar
  62. Te Beest M, Stevens N, Olff H, van der Putten WH (2009) Plant-soil feedback induces shifts in biomass allocation in the invasive plant Chromolaena odorata. J Ecol 97(6):1281–1290.  https://doi.org/10.1111/j.1365-2745.2009.01574.x CrossRefGoogle Scholar
  63. Thorpe AS, Thelen GC, Diaconu A et al (2009) Root exudate is allelopathic in invaded community but not in native community: field evidence for the novel weapons hypothesis. J Ecol 97:641–645CrossRefGoogle Scholar
  64. Tlusty B, Grossman JM, Graham PH (2004) Selection of rhizobia for prairie legumes used in restoration and reconstruction programs in Minnesota. Can J Microbiol 50(11):977–983.  https://doi.org/10.1139/w04-084 CrossRefGoogle Scholar
  65. van der Heijden MGA, de Bruin S, Luckerhoff L, van Logtestijn RSP, Schlaeppi K (2015) A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10(2):1–11.  https://doi.org/10.1038/ismej.2015.120 Google Scholar
  66. van der Putten WH (2003) Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84(9):2269–2280.  https://doi.org/10.1890/02-0284 CrossRefGoogle Scholar
  67. van der Putten WH, Bardgett RD, Bever JD et al (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276CrossRefGoogle Scholar
  68. Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Resour 5:181–183.  https://doi.org/10.1111/j.1471-8286.2004.00829.x CrossRefGoogle Scholar
  69. Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100CrossRefGoogle Scholar
  70. Wolfe BE, Rodgers VL, Stinson KA, Pringle A (2008) The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. J Ecol 96(4):777–783.  https://doi.org/10.1111/j.1365-2745.2008.01389.x CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of BiologyAlgoma UniversitySault Ste. MarieCanada
  2. 2.School of Environmental SciencesUniversity of GuelphGuelphCanada

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