Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Belowground competition drives invasive plant impact on native species regardless of nitrogen availability

Abstract

Plant invasions and eutrophication are pervasive drivers of global change that cause biodiversity loss. Yet, how invasive plant impacts on native species, and the mechanisms underpinning these impacts, vary in relation to increasing nitrogen (N) availability remains unclear. Competition is often invoked as a likely mechanism, but the relative importance of the above and belowground components of this is poorly understood, particularly under differing levels of N availability. To help resolve these issues, we quantified the impact of a globally invasive grass species, Agrostis capillaris, on two co-occurring native New Zealand grasses, and vice versa. We explicitly separated above- and belowground interactions amongst these species experimentally and incorporated an N addition treatment. We found that competition with the invader had large negative impacts on native species growth (biomass decreased by half), resource capture (total N content decreased by up to 75%) and even nutrient stoichiometry (native species tissue C:N ratios increased). Surprisingly, these impacts were driven directly and indirectly by belowground competition, regardless of N availability. Higher root biomass likely enhanced the invasive grass’s competitive superiority belowground, indicating that root traits may be useful tools for understanding invasive plant impacts. Our study shows that belowground competition can be more important in driving invasive plant impacts than aboveground competition in both low and high fertility ecosystems, including those experiencing N enrichment due to global change. This can help to improve predictions of how two key drivers of global change, plant species invasions and eutrophication, impact native species diversity.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant–soil feedbacks. J Exp Bot 50:29–37. https://doi.org/10.1093/jexbot/50.330.29

  2. Agrawal A, Kotanen P, Mitchell C et al (2005) Enemy release? An experiment with congeneric plant pairs and diverse above-and belowground enemies. Ecology 86:2979–2989

  3. Barney JN, Tekiela DR, Dollete ESJ, Tomasek BJ (2013) What is the real impact of invasive plant species? Front Ecol Environ 11:322–329. https://doi.org/10.1890/120120

  4. Barney JN, Tekiela DR, Barrios-Garcia MN et al (2015) Global Invader Impact Network (GIIN): toward standardized evaluation of the ecological impacts of invasive plants. Ecol Evol 5:2878–2889. https://doi.org/10.1002/ece3.1551

  5. Besaw LM, Thelen GC, Sutherland S et al (2011) Disturbance, resource pulses and invasion: short-term shifts in competitive effects, not growth responses, favour exotic annuals. J Appl Ecol 48:998–1006. https://doi.org/10.1111/j.1365-2664.2011.01988.x

  6. Blumenthal DM, Jordan NR, Russelle MP (2003) Soil carbon addition controls weeds and facilitates prairie restoration. Ecol Appl 13:605–615

  7. Bobbink R (1991) Effects of nutrient enrichment in Dutch chalk grassland. J Appl Ecol 28:28–41

  8. Borer ET, Seabloom EW, Gruner DS et al (2014) Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508:517–520. https://doi.org/10.1038/nature13144

  9. Broadbent AAD, Orwin KH, Peltzer DA et al (2017) Invasive N-fixer impacts on litter decomposition driven by changes to soil properties not litter quality. Ecosystems 20:1–13. https://doi.org/10.1007/s10021-016-0099-3

  10. CABI (2017) Agrostis capillaris Norbert Maczey. In: Invasive Species Compendium. CAB, Wallingford, UK. https://www.cabi.org/isc/citation/

  11. Cahill JF (1999) Fertilization effects on interactions between above- and belowground competition. Ecology 80:466–480

  12. Cahill JF (2002) Interactions between root and shoot competition vary among species. Oikos 99:101–112. https://doi.org/10.1034/j.1600-0706.2002.990111.x

  13. Cahill JF (2003) Lack of relationship between below-ground competition and allocation to roots in 10 grassland species. J Ecol 91:532–540

  14. Cahill JF, Casper BB (2000) Investigating the relationship between neighbor root biomass and belowground competition: field evidence for symmetric competition belowground. Oikos 90:311–320. https://doi.org/10.1034/j.1600-0706.2000.900211.x

  15. 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

  16. Daehler C (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211

  17. Daly GT (1964) Leaf-surface wax in Poa colensoi. J Exp Bot 15:160–165

  18. Dickie IA, St John MG, Yeates GW et al (2014) Belowground legacies of Pinus contorta invasion and removal result in multiple mechanisms of invasional meltdown. AoB Plants 6:1–15. https://doi.org/10.1093/aobpla/plu056

  19. Dillenburg LR, Whigham DF, Teramura AH, Forseth IN (1993) Effects of below- and aboveground competition from the vines Lonicera japonica and Parthenocissus quinquefolia on the growth of the tree host Liquidambar styraciflua. Oecologia 93:48–54

  20. DiTommaso A, Aarssen LW (1991) Effect of nutrient level on competition intensity in the field for three coexisting grass species. J Veg Sci 2:513–522. https://doi.org/10.2307/3236033

  21. Duncan RP, Webster RJ, Jensen CA (2001) Declining plant species richness in the tussock grasslands of Canterbury and Otago, South Island, New Zealand. NZ J Ecol 2:35–47

  22. Edgar E, Connor H (2000) Flora of New Zealand, 5th edn. Manaaki Whenua Press, Lincoln, New Zealand

  23. Edgar E, Forde MB (1991) Agrostis L. in New Zealand. NZ J Bot 29:139–161. https://doi.org/10.1080/0028825X.1991.10416717

  24. Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. PNAS 100:8916–8920

  25. Fay PA, Prober SM, Harpole WS et al (2015) Grassland productivity limited by multiple nutrients. Nat Plants 1:15080. https://doi.org/10.1038/nplants.2015.80

  26. Firn J, Moore JL, MacDougall AS et al (2011) Abundance of introduced species at home predicts abundance away in herbaceous communities. Ecol Lett 14:274–281

  27. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081. https://doi.org/10.1038/nature05719

  28. Grace JB (1993) The effects of habitat productivity on competition intensity. Trends Ecol Evol 8:229–230. https://doi.org/10.1016/0169-5347(93)90194-T

  29. Harpole WS, Tilman D (2006) Non-neutral patterns of species abundance in grassland communities. Ecol Lett 9:15–23. https://doi.org/10.1111/j.1461-0248.2005.00836.x

  30. Harpole WS, Tilman D (2007) Grassland species loss resulting from reduced niche dimension. Nature 446:791–793. https://doi.org/10.1038/nature05684

  31. Harpole WS, Ngai JT, Cleland EE et al (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862. https://doi.org/10.1111/j.1461-0248.2011.01651.x

  32. Harpole WS, Sullivan LL, Lind EM et al (2016) Addition of multiple limiting resources reduces grassland diversity. Nature 537:1–9. https://doi.org/10.1038/nature19324

  33. Hautier Y, Niklaus P, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–638. https://doi.org/10.1126/science.1169640

  34. Heberling JM, Fridley JD (2016) Invaders do not require high resource levels to maintain physiological advantages in a temperate deciduous forest. Ecology 97:874–884. https://doi.org/10.1890/15-1659.1

  35. Hill MO, Mountford JO, Roy DB, Bunce RGH (1999) Ellenberg’s indicator values for British plants. ECOFACT Volume 2 Technical Annex (ECOFACT, 2a), Institute of Terrestrial Ecology, Huntingdon

  36. Hillerislambers J, Adler PB, Harpole WS et al (2012) Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst 43:227–248

  37. Johnson NC, Rowland DL, Corkidi L, Allen EB (2008) Plant winners and losers during grassland n-eutrophication differ in biomass allocation and mycorrhizas. Ecology 89:2868–2878

  38. Kueffer C, Schumacher E, Fleischmann K et al (2007) Strong below-ground competition shapes tree regeneration in invasive Cinnamomum verum forests. J Ecol 95:273–282

  39. Lai HR, Mayfield MM, Gay-des-combes JM et al (2015) Distinct invasion strategies operating within a natural annual plant system. Ecol Lett 18:336–346

  40. Leishman MR, Thomson VP (2005) Experimental evidence for the effects of additional water, nutrients and physical disturbance on invasive plants in low fertility Hawkesbury Sandstone soils, Sydney, Australia. J Ecol 93:38–49

  41. 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

  42. Leishman MR, Thomson VP, Cooke J (2010) Native and exotic invasive plants have fundamentally similar carbon capture strategies. J Ecol 98:28–42

  43. Levine JM, Vilà M, D’Antonio CM et al (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc B Biol Sci 270:775–781. https://doi.org/10.1098/rspb.2003.2327

  44. MacDougall AS, Gilbert B, Levine JM (2009) Plant invasions and the niche. J Ecol 97:609–615. https://doi.org/10.1111/j.1365-2745.2009.01514.x

  45. Mark AF, McLennan B (2005) The conservation status of New Zealand’s indigenous grasslands. NZ J Bot 43:245–270

  46. Olde Venterink H, Güsewell S (2010) Competitive interactions between two meadow grasses under nitrogen and phosphorus limitation. Funct Ecol 24:877–886

  47. Olde Venterink H, Wassen MJ, Verkroost AWM, De Ruiter PC (2003) Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84:2191–2199. https://doi.org/10.1890/01-0639

  48. Ordonez A, Olff H (2013) Do alien plant species profit more from high resource supply than natives? A trait-based analysis. Glob Ecol Biogeogr 22:648–658

  49. Ordonez A, Wright IJ, Olff H (2010) Functional differences between native and alien species: a global-scale comparison. Funct Ecol 24:1353–1361

  50. Radford IJ, Dickinson KJM, Lord JM (2007) Functional and performance comparisons of invasive Hieracium lepidulum and co-occurring species in New Zealand. Austral Ecol 32:338–354. https://doi.org/10.1111/j.1442-9993.2007.01700.x

  51. Reinhart K, Callaway R (2006) Soil biota and invasive plants. New Phytol 170:445–457

  52. Rose A (1995) Vegetation change over 25 years in a New Zealand short-tussock grassland: effects of sheep grazing and exotic invasions. NZ J Ecol 19(2):163–174

  53. Rose AB, Frampton CM (2007) Rapid short-tussock grassland decline with and without grazing, Marlborough, New Zealand. NZ J Ecol 31:232–244

  54. Rose AB, Suisted PA, Frampton CM (2004) Recovery, invasion, and decline over 37 years in a Marlborough short tussock grassland, New Zealand. NZ J Bot 42:77–87. https://doi.org/10.1080/0028825X.2004.9512891

  55. Scott D (2000) Fertiliser and grazing rejuvenation of fescue tussock grassland. NZ J Ecol Agric Res 43:481–490. https://doi.org/10.1080/00288233.2000.9513444

  56. 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. https://doi.org/10.1073/pnas.1835728100

  57. Seabloom EW, Borer ET, Buckley YM et al (2015) Plant species’ origin predicts dominance and response to nutrient enrichment and herbivores in global grasslands. Nat Commun 6:7710. https://doi.org/10.1038/ncomms8710

  58. Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879. https://doi.org/10.1126/science.1094678

  59. R Core Team (2017) R: A language and environment for statistical computing. Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  60. Thompson VP, Leishman MR (2004) Survival of native plants of Hawkesbury Sandstone communities with additional nutrients: effect of plant age and habitat type. Aust J Bot 52:141–147

  61. Thomsen MA, Corbin JD, D’Antonio CM (2006) The effect of soil nitrogen on competition between native and exotic perennial grasses from northern coastal California. Plant Ecol 186:23–35. https://doi.org/10.1007/s11258-006-9109-4

  62. Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton

  63. Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton

  64. Trinder CJ, Brooker RW, Robinson D (2013) Plant ecology’s guilty little secret: understanding the dynamics of plant competition. Funct Ecol 27:918–929

  65. Turkington R, Klein E, Chanway CP (1993) Interactive effects of nutrients and disturbance: an experimental test of plant strategy theory. Ecology 74:863–878

  66. Tylianakis JM, Didham RK, Bascompte J, Wardle D (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

  67. van der Putten WH, Bradford MA, Pernilla Brinkman E et al (2016) Where, when and how plant-soil feedback matters in a changing world. Funct Ecol 30:1109–1121

  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

  69. Van Kleunen M, Dawson W, Essl F et al (2015) Global exchange and accumulation of non-native plants. Nature 525:100–103. https://doi.org/10.1038/nature14910

  70. Vila M, Weiner J (2004) Are invasive plant species better competitors than native plant species?–evidence from pair-wise experiments. Oikos 105:229–238

  71. Vilà M, Espinar JL, Hejda 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

  72. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science 277:494–499. https://doi.org/10.1126/science.277.5325.494

  73. 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 0478217595

  74. Wilsey BJ, Polley WH (2006) Aboveground productivity and root-shoot allocation differ between native and introduced grass species. Oecologia 150:300–309

  75. Wilson JB (1988) Shoot competition and root competition. J Appl Ecol 25:279–296

  76. Wilson SD, Shay JM (1990) Competition, fire, and nutrients in a mixed-grass prairie. Ecology 71:1959–1967. https://doi.org/10.2307/1937604

  77. Wilson SD, Tilman D (1991) Component of plant competition along an experimental gradient of nitrogen availability. Ecology 72:1050–1065. https://doi.org/10.2307/1940605

Download references

Acknowledgements

We would like to thank Karen Boot, Rowan Buxton and Chris Morse for field and logistical assistance, along with Matthew Clare and Silke Broadbent for help in the greenhouse, and Paul Chambre for experimental advice. AB is funded by a Lancaster University Faculty of Science and Technology studentship.

Author information

AB and CS conceived the experiment; AB conducted the experiment and data analysis; DP coordinated fieldwork; AB, CS, DP, NO and KO designed experiments and wrote the manuscript.

Correspondence to Arthur Broadbent.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Edith B. Allen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 55 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Broadbent, A., Stevens, C.J., Peltzer, D.A. et al. Belowground competition drives invasive plant impact on native species regardless of nitrogen availability. Oecologia 186, 577–587 (2018). https://doi.org/10.1007/s00442-017-4039-5

Download citation

Keywords

  • Global change
  • Grassland
  • Mechanism
  • Non-native
  • Nutrient availability