, Volume 186, Issue 3, pp 611–620 | Cite as

Biogeographic differences in soil biota promote invasive grass response to nutrient addition relative to co-occurring species despite lack of belowground enemy release

  • Arthur A. D. BroadbentEmail author
  • Carly J. Stevens
  • Nicholas J. Ostle
  • Kate H. Orwin
Highlighted Student Research


Multiple plant species invasions and increases in nutrient availability are pervasive drivers of global environmental change that often co-occur. Many plant invasion studies, however, focus on single-species or single-mechanism invasions, risking an oversimplification of a multifaceted process. Here, we test how biogeographic differences in soil biota, such as belowground enemy release, interact with increases in nutrient availability to influence invasive plant growth. We conducted a greenhouse experiment using three co-occurring invasive grasses and one native grass. We grew species in live and sterilized soil from the invader’s native (United Kingdom) and introduced (New Zealand) ranges with a nutrient addition treatment. We found no evidence for belowground enemy release. However, species’ responses to nutrients varied, and this depended on soil origin and sterilization. In live soil from the introduced range, the invasive species Lolium perenne L. responded more positively to nutrient addition than co-occurring invasive and native species. In contrast, in live soil from the native range and in sterilized soils, there were no differences in species’ responses to nutrients. This suggests that the presence of soil biota from the introduced range allowed L. perenne to capture additional nutrients better than co-occurring species. Considering the globally widespread nature of anthropogenic nutrient additions to ecosystems, this effect could be contributing to a global homogenization of flora and the associated losses in native species diversity.


Belowground Enemy release Invasive species Nutrient availability Soil biota 



We would like to thank Duane Peltzer for lending equipment and advice, along with Silke Broadbent, Carmen Zwahlen, Lotus Emam, Annette Ryan, Karen Boot, Isabel Rogers, Lucas Gent and Simon Broadbent for help in the field, laboratory and greenhouse. We are also grateful to the Department of Conservation (NZ) for land access. AB was funded by a PhD studentship from the Faculty of Science and Technology at Lancaster University.

Author contribution statement

AB conceived of and conducted the experiments, including fieldwork and analysis of the data; all authors designed experiments and wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2018_4081_MOESM1_ESM.docx (158 kb)
Supplementary material 1 (DOCX 157 kb)


  1. Agrawal A, Kotanen P, Mitchell C, Power A, Godsoe W, Klironomos J (2005) Enemy release? An experiment with congeneric plant pairs and diverse above-and belowground enemies. Ecology 86:2979–2989CrossRefGoogle Scholar
  2. Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699. CrossRefPubMedGoogle Scholar
  3. Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T (2005) Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspect Plant Ecol Evol Syst 7:27–49. CrossRefGoogle Scholar
  4. Baxendale C, Orwin KH, Poly F, Pommier T, Bardgett RD (2014) Are plant–soil feedback responses explained by plant traits? New Phytol 204:408–423. CrossRefPubMedGoogle Scholar
  5. Bennett AE, Strauss SY (2012) Response to soil biota by native, introduced non-pest, and pest grass species: is responsiveness a mechanism for invasion? Biol Invasions 15:1343–1353. CrossRefGoogle Scholar
  6. Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant–soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184. CrossRefPubMedGoogle Scholar
  7. Blumenthal D (2005) Interrelated causes of plant invasion. Science 310:243–244CrossRefPubMedGoogle Scholar
  8. Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895. CrossRefPubMedGoogle Scholar
  9. Blumenthal D, Mitchell CE, Pysek P, Jarosík V (2009) Synergy between pathogen release and resource availability in plant invasion. Proc Natl Acad Sci USA 106:7899–7904. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bradley BA, Blumenthal DM, Wilcove DS, Ziska LH (2010) Predicting plant invasions in an era of global change. Trends Ecol Evol 25:310–318. CrossRefPubMedGoogle Scholar
  11. Broadbent A, Stevens CJ, Peltzer DA, Ostle NJ, Orwin KH (2017) Belowground competition drives invasive plant impact on native species regardless of nitrogen availability. Oecologia. PubMedGoogle Scholar
  12. CABI (2017) Agrostis capillaris Norbert Maczey; Lolium perenne and Anthoxanthum odoratum Ian Popay. In: Invasive Species Compendium. CAB, Wallingford, UK Invasive Species Compendium. In: CAB International, Wallingford.
  13. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40. CrossRefGoogle Scholar
  14. Chun YJ, van Kleunen M, Dawson W (2010) The role of enemy release, tolerance and resistance in plant invasions: linking damage to performance. Ecol Lett 13:937–946. PubMedGoogle Scholar
  15. Cliquet JB, Murray PJ, Boucaud J (1997) Effect of the arbuscular mycorrhizal fungus Glornus nitrogen fasciculaturn on by Loliurn the uptake of amino perenne. New Phytol 137:345–349CrossRefGoogle Scholar
  16. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899. CrossRefPubMedGoogle Scholar
  17. Craine JM, Lee WG (2003) Covariation in leaf and root traits for native and non-native grasses along an altitudinal gradient in New Zealand. Oecologia 134:471–478. CrossRefPubMedGoogle Scholar
  18. Craine JM, Fargione J, Sugita S (2005) Supply pre-emption, not concentration reduction, is the mechanism of competition for nutrients. New Phytol 166:933–940. CrossRefPubMedGoogle Scholar
  19. Davis MA, Pelsor M (2001) Experimental support for a resource-based mechanistic model of invasibility. Ecol Lett 4:421–428. CrossRefGoogle Scholar
  20. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. CrossRefGoogle Scholar
  21. Dickie IA, St John MG, Yeates GW, Morse CW, Bonner KI, Orwin K, Peltzer DA (2014) Belowground legacies of Pinus contorta invasion and removal result in multiple mechanisms of invasional meltdown. AoB Plants 6:1–15. CrossRefGoogle Scholar
  22. Dickie IA, Bufford JL, Cobb RC, Desprez-Loustau ML, Grelet G, Hulme PE, Klironomos J, Makiola A, Nunez MA, Pringle A, Thrall PH, Tourtellot SG, Waller L, Williams NM (2017) The emerging science of linked plant-fungal invasions. New Phytol 215:1314–1332. CrossRefPubMedGoogle Scholar
  23. Diez JM, Dickie I, Edwards G, Hulme PE, Sullivan JJ, Duncan RP (2010) Negative soil feedbacks accumulate over time for non-native plant species. Ecol Lett 13:803–809. CrossRefPubMedGoogle Scholar
  24. Duncan RP, Webster RJ, Jensen CA (2001) Declining plant species richness in the tussock grasslands of Canterbury and Otago, South Island, New Zealand. N Z J Ecol 25:35–47Google Scholar
  25. Faure S, Cliquet J-B, Thephany G, Boucaud J (1998) Nitrogen assimilation in Lolium perenne colonized by the arbuscular mycorrhizal fungus Glomus fasciculatum. New Phytol 138:411–417. CrossRefGoogle Scholar
  26. Firn J, Moore JL, MacDougall AS, Borer ET, Seabloom EW, HilleRisLambers J, Harpole WS, Cleland EE, Brown CS, Knops JMH, Prober SM, Pyke DA, Farrell KA, Bakker JD, O’Halloran LR, Adler PB, Collins SL, D’Antonio CM, Crawley MJ, Wolkovich EM, La Pierre KJ, Melbourne BA, Hautier Y, Morgan JW, Leakey ADB, Kay A, McCulley R, Davies KF, Stevens CJ, Chu CJ, Holl KD, Klein JA, Fay PA, Hagenah N, Kirkman KP, Buckley YM (2011) Abundance of introduced species at home predicts abundance away in herbaceous communities. Ecol Lett 14:274–281. CrossRefPubMedGoogle Scholar
  27. Fox J, Weisberg S (2011) An R companion to applied regression. Sage publications, Inc., Thousand OaksGoogle Scholar
  28. Gross N, Börger L, Duncan RP, Hulme PE (2013) Functional differences between alien and native species: do biotic interactions determine the functional structure of highly invaded grasslands? Funct Ecol 27:1262–1272. CrossRefGoogle Scholar
  29. Gundale M, Kardol P, Nilsson M, Nilsson U, Lucas RW, Wardle DA (2014) Interactions with soil biota shift from negative to positive when a tree species is moved outside its native range. New Phytol 202:415–421. CrossRefPubMedGoogle Scholar
  30. Gurevitch J, Fox GA, Wardle GM, Inderjit Taub D (2011) Emergent insights from the synthesis of conceptual frameworks for biological invasions. Ecol Lett 14:407–418. CrossRefPubMedGoogle Scholar
  31. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–32. Scholar
  32. Kardol P, De Long JR, Sundqvist MK (2012) Crossing the threshold: the power of multi-level experiments in identifying global change responses. New Phytol 196:323–326. CrossRefPubMedGoogle Scholar
  33. Keane R, Crawley M (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  34. King WM, Wilson JB (2006) Differentiation between native and exotic plant species from a dry grassland: fundamental responses to resource availability, and growth rates. Austral Ecol 31:996–1004. CrossRefGoogle Scholar
  35. Klironomos J (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. CrossRefGoogle Scholar
  36. Kuebbing SE, Nuñez MA, Simberloff D (2013) Current mismatch between research and conservation efforts: the need to study co-occurring invasive plant species. Biol Conserv 160:121–129. CrossRefGoogle Scholar
  37. Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant–soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992. CrossRefPubMedGoogle Scholar
  38. Leishman MR, Haslehurst T, Ares A, Baruch Z (2007) Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytol 176:635–643. CrossRefPubMedGoogle Scholar
  39. Leishman MR, Cooke J, Richardson DM (2014) Evidence for shifts to faster growth strategies in the new ranges of invasive alien plants. J Ecol 102:1451–1461. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Mark AF, McLennan B (2005) The conservation status of New Zealand’s indigenous grasslands. N Z J Bot 43:245–270. CrossRefGoogle Scholar
  41. Maron JL, Waller LP, Hahn MA, Diaconu A, Pal RW, Müller-Schärer H, Klironomos JN, Callaway RM (2013) Effects of soil fungi, disturbance and propagule pressure on exotic plant recruitment and establishment at home and abroad. J Ecol 101:924–932. CrossRefGoogle Scholar
  42. Maron JL, Klironomos J, Waller L, Callaway RM (2014) Invasive plants escape from suppressive soil biota at regional scales. J Ecol 102:19–27. CrossRefGoogle Scholar
  43. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627. CrossRefPubMedGoogle Scholar
  44. Moora M, Berger S, Davison J, Öpik M, Bommarco R, Bruelheide H, Kühn I, Kunin WE, Metsis M, Rortais A, Vanatoa A, Vanatoa E, Stout JC, Truusa M, Westphal C, Zobel M, Walther GR (2011) Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeogr 38:1305–1317. CrossRefGoogle Scholar
  45. New Zealand Plant Conservation Network (2016) Agrostis capillaris; Anthoxanthum odoratum and Lolium perenne. In: New Zealand plant conservation network.
  46. Niu S, Classen AT, Dukes JS, Kardol P, Liu L, Luo Y, Rustad L, Sun J, Tang J, Templer PH, Thomas RQ, Tian D, Vicca S, Wang YP, Xia J, Zaehle S (2016) Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. Ecol Lett 19:697–709. CrossRefPubMedGoogle Scholar
  47. Ordonez A, Wright IJ, Olff H (2010) Functional differences between native and alien species: a global-scale comparison. Funct Ecol 24:1353–1361. CrossRefGoogle Scholar
  48. Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504. CrossRefPubMedGoogle Scholar
  49. Pérez-Harguindeguy N, Díaz S, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardized measurement of plant functional traits worldwide. Aust J Bot 23:167–234. CrossRefGoogle Scholar
  50. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288. CrossRefGoogle Scholar
  51. R Core Team (2016) R: a language and environment for statistical computing. Foundation for Statistical Computing, Vienna, Austria.
  52. Reinhart K, Callaway R (2004) Soil biota facilitate exotic Acer invasions in Europe and North America. Ecol Appl 14:1737–1745CrossRefGoogle Scholar
  53. Reinhart K, Callaway R (2006) Soil biota and invasive plants. New Phytol 170:445–457CrossRefPubMedGoogle Scholar
  54. Reinhart KO, Rinella MJ (2016) A common soil handling technique can generate incorrect estimates of soil biota effects on plants. New Phytol 210:786–789. CrossRefPubMedGoogle Scholar
  55. Richardson DM, Pysek P (2008) Fifty years of invasion ecology—the legacy of Charles Elton. Divers Distrib 14:161–168. CrossRefGoogle Scholar
  56. Rose AB, Frampton CM (2007) Rapid short-tussock grassland decline with and without grazing, Marlborough, New Zealand. N Z J Ecol 31:232–244Google Scholar
  57. Rose AB, Suisted PA, Frampton CM (2004) Recovery, invasion, and decline over 37 years in a Marlborough short tussock grassland, New Zealand. N Z J Bot 42:77–87. CrossRefGoogle Scholar
  58. Sala OE (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. CrossRefPubMedGoogle Scholar
  59. Scott D (2000) Fertiliser and grazing rejuvenation of fescue tussock grassland. N Z J Agric Res 43:481–490. CrossRefGoogle Scholar
  60. Seabloom EW, Harpole WS, Reichman OJ, Tilman D (2003) Invasion, competitive dominance, and resource use by exotic and native California grassland species. Proc Natl Acad Sci USA 100:13384–13389. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Seabloom EW, Borer ET, Buckley YM, Cleland EE, Davies KF, Firn J, Harpole WS, Hautier Y, Lind EM, MacDougall AS, Orrock JL, Prober SM, Adler PB, Anderson TM, Bakker JD, Biederman LA, Blumenthal DM, Brown CS, Brudvig LA, Cadotte M, Chu C, Cottingham KL, Crawley MJ, Damschen EI, Dantonio CM, DeCrappeo NM, Du G, Fay PA, Frater P, Gruner DS, Hagenah N, Hector A, Hillebrand H, Hofmockel KS, Humphries HC, Jin VL, Kay A, Kirkman KP, Klein JA, Knops JMH, La Pierre KJ, Ladwig L, Lambrinos JG, Li Q, Li W, Marushia R, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan J, Mortensen B, O’Halloran LR, Pyke DA, Risch AC, Sankaran M, Schuetz M, Simonsen A, Smith MD, Stevens CJ, Sullivan L, Wolkovich E, Wragg PD, Wright J, Yang L (2015) Plant species’ origin predicts dominance and response to nutrient enrichment and herbivores in global grasslands. Nat Commun 6:7710. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55CrossRefPubMedGoogle Scholar
  63. Sun Y, Müller-Schärer H, Schaffner U (2014) Plant neighbours rather than soil biota determine impact of an alien plant invader. Funct Ecol 28:1545–1555. CrossRefGoogle Scholar
  64. Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberté E (2017) Plant–soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355:173–176. CrossRefPubMedGoogle Scholar
  65. Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273. CrossRefPubMedGoogle Scholar
  66. Torrecillas E, del Mar Alguacil M, Roldan A, Diaz G, Montesinos-Navarro A, Torres MP (2014) Modularity reveals the tendency of arbuscular mycorrhizal fungi to interact differently with generalist and specialist plant species in gypsum soils. Appl Environ Microbiol 80:5457–5466. CrossRefPubMedPubMedCentralGoogle Scholar
  67. van Der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community. Ecology 79:2082–2091.[2082:DAMFSA]2.0.CO;2Google Scholar
  68. van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. CrossRefPubMedGoogle Scholar
  69. Van Kleunen M, Dawson W, Essl F, Pergl J, Winter M, Weber E, Kreft H, Weigelt P, Kartesz J, Nishino M, Antonova LA, Barcelona JF, Cabezas FJ, Morozova O, Moser D, Nickrent DL, Patzelt A, Pelser PB, Baptiste MP, Poopath M, Schulze M, Seebens H, Shu WS, Thomas J, Velayos M, Wieringa JJ (2015) Global exchange and accumulation of non-native plants. Nature 525:100–103. CrossRefPubMedGoogle Scholar
  70. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708. CrossRefPubMedGoogle Scholar
  71. Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16Google Scholar
  72. Williams PA (1998) Response of broom (Cytisus scoparius) to control measures. Science for conservation, vol 97. Department of Conservation, New Zealand, pp 1173–2946. ISBN 0478217595Google Scholar
  73. Zhu Q, Riley WJ, Tang J, Koven CD (2016) Multiple soil nutrient competition between plants, microbes, and mineral surfaces: model development, parameterization, and example applications in several tropical forests. Biogeosciences 13:341–363. CrossRefGoogle Scholar
  74. Zhu Q, Riley WJ, Tang J (2017) A new theory of plant-microbe nutrient competition resolves inconsistencies between observations and model predictions. Ecol Appl 27:875–886. CrossRefPubMedGoogle Scholar
  75. Zuppinger-Dingley D, Schmid B, Chen Y, Brandl H, van der Heijden MGA, Joshi J (2011) In their native range, invasive plants are held in check by negative soil-feedbacks. Ecosphere 2:1–12. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Lancaster Environment CentreLancaster UniversityLancasterUK
  2. 2.Landcare ResearchLincolnNew Zealand

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