Effects of elevated CO2 on competition between native and invasive grasses

Abstract

Elevated atmospheric CO2 concentration increases the performance of invasive plants relative to natives when grown in monoculture, but it is unclear how that will affect the relative competitive abilities per se of invasive and native grasses grown together. We tested competitive outcomes for four native and four invasive perennial C3 and C4 grasses under ambient (390 ppm) and elevated (700 or 1000 ppm) CO2 concentrations in the greenhouse with non-limiting water and nutrients. We predicted that elevated CO2 would increase the competitive suppression of native grasses by invasive grasses. To test this, we determined the relative interaction intensity of biomass allocation for natives grown alone vs. those grown in native–invasive species pairs. We also measured photosynthetic traits that contribute to plant invasiveness and may be affected by elevated CO2 concentrations for species pairs in mixture to determine native–invasive relative performance. We found no effect of CO2 for the aboveground biomass and tiller production measures of interaction intensity or for relative performance for most of the measured photosynthetic traits. In competition, the invaders nearly always outperform natives in biomass and tiller production, regardless of CO2 level. The results suggest that increasing CO2 concentration alone has little effect on grass competitive outcomes under controlled conditions.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Ackerly DD, Bazzaz FA (1995) Plant growth and reproduction along CO2 gradients: non-linear responses and implications for community change. Glob Change Biol 1:199–207. https://doi.org/10.1111/j.1365-2486.1995.tb00021.x

    Article  Google Scholar 

  2. Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686. https://doi.org/10.1890/03-0650

    Article  Google Scholar 

  3. Arp WJ (1991) Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14:869–875. https://doi.org/10.1111/j.1365-3040.1991.tb01450.x

    CAS  Article  Google Scholar 

  4. Aschehoug ET, Callaway RM (2015) Diversity increases indirect interactions, attenuates the intensity of competition, and promotes coexistence. Am Nat 186:452–459. https://doi.org/10.1086/682901

    Article  PubMed  Google Scholar 

  5. Aspinwall MJ, Fay PA, Hawkes CV, Lowry DB, Khasanova A, Bonnette J, Whitaker BK, Johnson N, Juenger TE (2017) Intraspecific variation in precipitation responses of a widespread C-4 grass depends on site water limitation. J Plant Ecol 10:310–321. https://doi.org/10.1093/jpe/rtw040

    Article  Google Scholar 

  6. Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895. https://doi.org/10.1111/j.1461-0248.2006.00934.x

    Article  PubMed  Google Scholar 

  7. Blumenthal DM, Resco V, Morgan JA, Williams DG, LeCain DR, Hardy EM, Pendall E, Bladyka E (2013) Invasive forb benefits from water savings by native plants and carbon fertilization under elevated CO2 and warming. New Phytol 200:1156–1165. https://doi.org/10.1111/nph.12459

    CAS  Article  PubMed  Google Scholar 

  8. Blumenthal DM, Kray JA, Ortmans W, Ziska LH, Pendall E (2016) Cheatgrass is favored by warming but not CO2 enrichment in a semi-arid grassland. Glob Change Biol 22:3026–3038. https://doi.org/10.1111/gcb.13278

    Article  Google Scholar 

  9. Bradford MA, Schumacher HB, Catovsky S, Eggers T, Newingtion JE, Tordoff GM (2007) Impacts of invasive plant species on riparian plant assemblages: interactions with elevated atmospheric carbon dioxide and nitrogen deposition. Oecologia 152:791–803. https://doi.org/10.1007/s0042-007-0697-z

    Article  PubMed  Google Scholar 

  10. Brooker RW (2006) Plant–plant interactions and environmental change. New Phytol 171:271–284. https://doi.org/10.1111/j.1469-8137.2006.01752.x

    Article  PubMed  Google Scholar 

  11. Carrara F, Giometto A, Seymour M, Rinaldo A, Altermatt F (2015) Inferring species interactions in ecological communities: a comparison of methods at different levels of complexity. Methods Ecol Evol 6:895–906. https://doi.org/10.1111/2041-210X.12363

    Article  Google Scholar 

  12. Cheplick GP (2003) Evolutionary significance of genotypic variation in developmental reaction norms for a perennial grass under competitive stress. Evol Ecol 17:175–196. https://doi.org/10.1023/A:1023057024776

    Article  Google Scholar 

  13. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. https://doi.org/10.1046/j.1365-2745.2000.00473.x

    Article  Google Scholar 

  14. Dieleman WIJ, Vicca S, Dijkstra FA, Hagedorn F, Hovenden MJ, Larsen KS, Morgan JA, Volder A, Beier C, Dukes JS, King J, Leuzinger S, Linder S, Luo Y, Oren R, De Angelis P, Tingey D, Hoosbeek MR, Janssens IA (2012) Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Glob Change Biol 18:2681–2693. https://doi.org/10.1111/j.1365-2486.2012.02745.x

    Article  Google Scholar 

  15. Dukes JS (2000) Will the increasing atmospheric CO2 concentration affect the success of invasive species? In: Mooney HA, Hobbs RJ (eds) Invasive species in a changing world. Island Press, Washington, DC, pp 95–113

    Google Scholar 

  16. Dukes JS (2002) Comparison of the effect of elevated CO2 on an invasive species (Centaurea solstitialis) in monoculture and community settings. Plant Ecol 160:225–234. https://doi.org/10.1023/A:1015813919850

    Article  Google Scholar 

  17. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139. https://doi.org/10.1016/S0169-5347(98)01554-7

    CAS  Article  PubMed  Google Scholar 

  18. Dukes JS, Chiariello NR, Loarie SR, Field CB (2011) Strong response of an invasive plant species (Centaurea solstitialis L.) to global environmental changes. Ecol Appl 21:1887–1894. https://doi.org/10.1890/11-0111.1

    Article  PubMed  Google Scholar 

  19. Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol 221:32–49. https://doi.org/10.1111/nph.15283

    CAS  Article  PubMed  Google Scholar 

  20. Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl Acad Sci USA 106:10343–10347. https://doi.org/10.1073/pnas.0904209106

    Article  PubMed  Google Scholar 

  21. Fusco EJ, Finn JT, Balch JK, Nagy RC, Bradley BA (2019) Invasive grasses increase fire occurrence and frequency across US ecoregions. Proc Natl Acad Sci USA 116:23594–23599. https://doi.org/10.1073/pnas.1908253116

    CAS  Article  PubMed  Google Scholar 

  22. Goldberg DE (1990) Components of resource competition in plant communities. In: Grace JB, Tilman D (eds) Perspectives on plant competition. Academic Press, San Diego, pp 27–49

    Google Scholar 

  23. Goldberg DE, Landa K (1991) Competitive effect and response: hierarchies and correlated traits in the early stages of competition. J Ecol 79:1013–1030. https://doi.org/10.2307/2261095

    Article  Google Scholar 

  24. Grass Phylogeny Working Group II (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193:304–312. https://doi.org/10.1111/j.1469-8137.2011.03972.x

    Article  Google Scholar 

  25. Grodzinski B, Schmidt JM, Watts B, Taylor J, Bates S, Dixon MA, Staines H (1999) Regulating plant/insect interactions using CO2 enrichment in model ecosystems. Adv Space Res 24:281–291. https://doi.org/10.1016/S0273-1177(99)00315-4

    CAS  Article  PubMed  Google Scholar 

  26. Hager HA (2004) Competitive effect versus competitive response of invasive and native wetland plant species. Oecologia 139:140–149. https://doi.org/10.1007/s00442-004-1494-6

    Article  PubMed  Google Scholar 

  27. Hager HA, Newman JA (2019) Methodology I: detecting and predicting grassland change. In: Gibson DJ, Newman JA (eds) Grasslands and climate change. Cambridge University Press, Cambridge, pp 19–39

    Google Scholar 

  28. Hager HA, Quinn LD, Barney JN, Voigt TB, Newman JA (2015a) Germination and establishment of bioenergy grasses outside cultivation: a multi-region seed addition experiment. Plant Ecol 216:1385–1399. https://doi.org/10.1007/s11258-015-0516-2

    Article  Google Scholar 

  29. Hager HA, Rupert R, Quinn LD, Newman JA (2015b) Escaped Miscanthus sacchariflorus reduces the richness and diversity of vegetation and the soil seed bank. Biol Invasions 17:1833–1847. https://doi.org/10.1007/s10530-014-0839-2

    Article  Google Scholar 

  30. Hager HA, Ryan GD, Kovacs HM, Newman JA (2016a) Effects of elevated CO2 on photosynthetic traits of native and invasive C3 and C4 grasses. BMC Ecol 16:28. https://doi.org/10.1186/s12898-016-0082-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Hager HA, Ryan GD, Kovacs HM, Newman JA (2016b) Effects of elevated CO2 on photosynthetic traits of native and invasive C3 and C4 grasses 2012 to 2013 [South-central Ontario, Canada]. Sch Portal Dataverse. https://doi.org/10.5887/AERDR/10864/TZBTY

    Article  Google Scholar 

  32. Hager HA, Ryan GD, Newman JA (2020) Effects of elevated CO2 on competition between native and invasive grasses. Scholars Portal Dataverse. https://doi.org/10.5683/SP2/GJ94P8

    Article  Google Scholar 

  33. He L, Kong J, Li G, Meng G, Chen K (2018) Similar responses in morphology, growth, biomass allocation, and photosynthesis in invasive Wedelia trilobata and native congeners to CO2 enrichment. Plant Ecol 219:145–157. https://doi.org/10.1007/s11258-017-0784-0

    Article  Google Scholar 

  34. Hely SEL, Roxburgh SH (2005) The interactive effects of elevated CO2, temperature and initial size on growth and competition between a native C3 and an invasive C3 grass. Plant Ecol 177:85–98. https://doi.org/10.1007/s11258-005-2247-2

    Article  Google Scholar 

  35. Hillebrand H, Gurevitch J (2016) Meta‐analysis and systematic reviews in ecology. In: eLS. Wiley. https://doi.org/10.1002/9780470015902.a0003272.pub2

  36. Holohan AD, Müller C, McElwain J (2019) Heritable changes in physiological gas exchange traits in response to long-term, moderate free-air carbon dioxide enrichment. Front Plant Sci 10:1210. https://doi.org/10.3389/fpls.2019.01210

    Article  PubMed  PubMed Central  Google Scholar 

  37. IPCC (Intergovernmental Panel on Climate Change) (2013) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

  38. Khan N, George D, Shabbir A, Hanif Z, Adkins SW (2015) Rising CO2 can alter fodder-weed interactions and suppression of Parthenium hysterophorus. Weed Res 55:113–117. https://doi.org/10.1111/wre.12127

    CAS  Article  Google Scholar 

  39. Koteen LE, Baldocchi DD, Harte J (2011) Invasion of non-native grasses causes a drop in soil carbon storage in California grasslands. Environ Res Lett 6:044001. https://doi.org/10.1088/1748-9326/6/4/044001

    CAS  Article  Google Scholar 

  40. Lambers H, Chapin FS III, Pons TL (1998) Plant physiological ecology. Springer, New York

    Google Scholar 

  41. Larson CD, Lehnhoff EA, Noffsinger C, Rew LJ (2018) Competition between cheatgrass and bluebunch wheatgrass is altered by temperature, resource availability, and atmospheric CO2 concentration. Oecologia 186:855–868. https://doi.org/10.1007/s00442-017-4046-6

    Article  PubMed  Google Scholar 

  42. Linder HP, Lehmann CER, Archibald S, Osborne CP, Richardson DM (2018) Global grass (Poaceae) success underpinned by traits facilitating colonization, persistence and habitat transformation. Biol Rev 93:1125–1144. https://doi.org/10.1111/brv.12388

    CAS  Article  PubMed  Google Scholar 

  43. Liu Y, Oduor AMO, Zhang Z, Manea A, Tooth IM, Leishman MR, Xu X, Van Kleunen M (2017) Do invasive alien plants benefit more from global environmental change than native plants? Glob Change Biol 23:3363–3370. https://doi.org/10.1111/gcb.13579

    Article  Google Scholar 

  44. Louda SM, Potvin MA (1995) Effect of inflorescence-feeding insects on the demography and lifetime fitness of a native plant. Ecology 76:229–245. https://doi.org/10.2307/1940645

    Article  Google Scholar 

  45. Manea A, Leishman MR (2011) Competitive interactions between native and invasive exotic plant species are altered under elevated carbon dioxide. Oecologia 165:735–744. https://doi.org/10.1007/s00442-010-1765-3

    Article  PubMed  Google Scholar 

  46. Manea A, Leishman MR (2014) Leaf area index drives soil water availability and extreme drought-related mortality under elevated CO2 in a temperate grassland model system. PLoS ONE 9:e91046. https://doi.org/10.1371/journal.pone.0091046

    Article  PubMed  PubMed Central  Google Scholar 

  47. Manea A, Sloane DR, Leishman MR (2016) Reductions in native grass biomass associated with drought facilitates the invasion of an exotic grass into a model grassland system. Oecologia 181:175–183. https://doi.org/10.1007/s00442-016-3553-1

    Article  PubMed  Google Scholar 

  48. Marshall VM, Lewis MM, Ostendorf B (2012) Buffel grass (Cenchrus ciliaris) as an invader and threat to biodiversity in arid environments: a review. J Arid Environ 78:1–12. https://doi.org/10.1016/j.jaridenv.2011.11.005

    Article  Google Scholar 

  49. Muir CD (2015) Making pore choices: repeated regime shifts in stomatal ratio. Proc R Soc B 282:20151498. https://doi.org/10.1098/rspb.2015.1498

    Article  PubMed  Google Scholar 

  50. Nagel JM, Huxman TE, Griffin KL, Smith SD (2004) Co-2 enrichment reduces the energetic cost of biomass construction in an invasive desert grass. Ecology 85:100–106. https://doi.org/10.1890/02-3005

    Article  Google Scholar 

  51. Navas ML (1998) Individual species performance and response of multispecific communities to elevated CO2: a review. Funct Ecol 12:721–727. https://doi.org/10.1046/j.1365-2435.1998.00260.x

    Article  Google Scholar 

  52. Newman J, Bergelson J, Grafen A (1997) Blocking factors and hypothesis tests in ecology: is your statistics text wrong? Ecology 78:1312–1320. https://doi.org/10.1890/0012-9658(1997)078[1312:BFAHTI]2.0.CO;2

    Article  Google Scholar 

  53. Ordonez A, Wright IJ, Olff H (2010) Functional differences between native and alien species: a global-scale comparison. Funct Ecol 24:1353–1361. https://doi.org/10.1111/j.1365-2435.2010.01739.x

    Article  Google Scholar 

  54. Owensby CE, Coyne PI, Ham JM, Auen LM, Knapp AK (1993) Biomass production in a tallgrass prairie ecosystem exposed to ambient and elevated CO2. Ecol Appl 3:644–653. https://doi.org/10.2307/1942097

    Article  PubMed  Google Scholar 

  55. Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198. https://doi.org/10.1046/j.1469-8137.2003.00680.x

    Article  Google Scholar 

  56. Poorter H, Bühler J, van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850. https://doi.org/10.1071/FP12049

    Article  Google Scholar 

  57. Pritchard SG, Rogers HH, Prior SA, Peterson CM (1999) Elevated CO2 and plant structure: a review. Glob Change Biol 5:807–837. https://doi.org/10.1046/j.1365-2486.1999.00268.x

    Article  Google Scholar 

  58. Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 97–125

    Google Scholar 

  59. Quinn LD, Allen DJ, Stewart JR (2010) Invasiveness potential of Miscanthus sinensis: implications for bioenergy production in the United States. Glob Change Biol Bioenergy 2:310–320. https://doi.org/10.1111/j.1757-1707.2010.01062.x

    Article  Google Scholar 

  60. Reekie EG (1996) The effect of elevated CO2 on developmental processes and its implications for plant–plant interactions. In: Körner C, Bazzaz FA (eds) Carbon dioxide, populations, and communities. Academic Press, San Diego, pp 333–346

    Google Scholar 

  61. Reichmann LG, Schwinning S, Polley HW, Fay PA (2016) Traits of an invasive grass conferring an early growth advantage over native grasses. J Plant Ecol 9:672–681. https://doi.org/10.1093/jpe/rtw014

    Article  Google Scholar 

  62. Reynolds HL (1996) Effects of elevated CO2 on plants grown in competition. In: Körner C, Bazzaz FA (eds) Carbon dioxide, populations, and communities. Academic Press, San Diego, California, pp 273–286

    Google Scholar 

  63. Sher AA, Hyatt LA (1999) The disturbed resource-flux invasion matrix: a new framework for patterns of plant invasion. Biol Invasions 1:107–114. https://doi.org/10.1023/A:1010050420466

    Article  Google Scholar 

  64. Sorte CJB, Ibanez I, Blumenthal DM, Molinari NA, Miller LP, Grosholz ED, Diez JM, D’Antonio CM, Olden JD, Jones SJ, Dukes JS (2013) Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance. Ecol Lett 16:261–270. https://doi.org/10.1111/ele.12017

    Article  PubMed  Google Scholar 

  65. Sun W, Ubierna N, Ma J-Y, Walker BJ, Kramer DM, Cousins AB (2014) The coordination of C4 photosynthesis and the CO2-concentrating mechanism in maize and Miscanthus × giganteus in response to transient changes in light quality. Plant Physiol 164:1283–1292. https://doi.org/10.1104/pp.113.224683

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. Swope SM, Parker IM (2010) Trait-mediated interactions and lifetime fitness of the invasive plant Centaurea solstitialis. Ecology 91:2284–2293. https://doi.org/10.1890/09-0855.1

    Article  PubMed  Google Scholar 

  67. Taylor SH, Hulme SP, Rees M, Ripley BS, Woodward FI, Osborne CP (2010) Ecophysiological traits in C-3 and C-4 grasses: a phylogenetically controlled screening experiment. New Phytol 185:780–791. https://doi.org/10.1111/j.1469-8137.2009.03102.x

    CAS  Article  PubMed  Google Scholar 

  68. Tipping C, Murray DR (1999) Effects of elevated atmospheric CO2 concentration on leaf anatomy and morphology in Panicum species representing different photosynthetic modes. Int J Plant Sci 160:1063–1073. https://doi.org/10.1086/314201

    CAS  Article  PubMed  Google Scholar 

  69. Tooth IM, Leishman MR (2014) Elevated carbon dioxide and fire reduce biomass of native grass species when grown in competition with invasive exotic grasses in a savanna experimental system. Biol Invasions 16:257–268. https://doi.org/10.1007/s10530-013-0448-5

    Article  Google Scholar 

  70. Urban O (2003) Physiological impacts of elevated CO2 concentration ranging from molecular to whole plant responses. Photosynthetica 41:9–20. https://doi.org/10.1023/A:1025891825050

    CAS  Article  Google Scholar 

  71. 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. https://doi.org/10.1111/j.1461-0248.2009.01418.x

    Article  PubMed  Google Scholar 

  72. Wand SJE, Midgley GF, Jones MH, Curtis PS (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Glob Change Biol 5:723–741. https://doi.org/10.1046/j.1365-2486.1999.00265.x

    Article  Google Scholar 

  73. Wang P, Stieglitz T, Zhou DW, Cahill JF Jr (2010) Are competitive effect and response two sides of the same coin, or fundamentally different? Funct Ecol 24:196–207. https://doi.org/10.1111/j.1365-2435.2009.01612.x

    Article  Google Scholar 

  74. West NM, Matlaga DP, Davis AS (2014) Quantifying targets to manage invasion risk: light gradients dominate the early regeneration niche of naturalized and pre-commercial Miscanthus populations. Biol Invasions 16:1991–2001. https://doi.org/10.1007/s10530-014-0643-z

    Article  Google Scholar 

  75. Williams AL, Wills KE, Janes JK, Schoor JKV, Newton PCD, Hovenden MJ (2007) Warming and free-air CO2 enrichment alter demographics in four co-occurring grassland species. New Phytol 176:365–374. https://doi.org/10.1111/j.1469-8137.2007.02170.x

    Article  PubMed  Google Scholar 

  76. Wilsey BJ, Martin LM, Kaul AD (2018) Phenology differences between native and novel exotic-dominated grasslands rival the effects of climate change. J Appl Ecol 55:863–873. https://doi.org/10.1111/1365-2664.12971

    Article  Google Scholar 

  77. Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327. https://doi.org/10.1111/j.1469-8137.1995.tb03067.x

    Article  Google Scholar 

  78. Ziska LH, George K (2004) Rising carbon dioxide and invasive, noxious plants: potential threats and consequences. World Resour Rev 16:427–447

    Google Scholar 

Download references

Acknowledgements

We thank A. Patchett, K. Shukla, M. Melkic, K. Bolton, S. McGee, E. Staples, and J. Dale for help with the experiment; Y. Zheng, E. Lyons, H. Earl, and G. Otis for providing equipment; R. Dutton for managing the greenhouse, W. McCloskey for providing buffelgrass seed, C. Breton for data archiving assistance, and two anonymous reviewers for comments. This research was funded by Mitacs (HAH); Ontario Ministry of Agriculture, Food and Rural Affairs (all authors); Natural Sciences and Engineering Research Council of Canada (JAN); and J.D. Webster Postdoctoral Fellowship (GDR).

Author information

Affiliations

Authors

Contributions

HAH and GDR designed and executed the study. HAH analysed the data and wrote the manuscript. JAN advised on experimental design and statistics. HAH, GDR, and JAN edited the manuscript.

Corresponding author

Correspondence to Heather A. Hager.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Communicated by Yanjie Liu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 611 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hager, H.A., Ryan, G.D. & Newman, J.A. Effects of elevated CO2 on competition between native and invasive grasses. Oecologia 192, 1099–1110 (2020). https://doi.org/10.1007/s00442-020-04636-6

Download citation

Keywords

  • Climate change
  • Grassland
  • Invasion traits
  • Photosynthesis
  • Relative interaction intensity