Skip to main content

Advertisement

Log in

Nitrogen addition, not heterogeneity, alters the relationship between invasion and native decline in California grasslands

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The presence of invasive species reduces the growth and performance of native species; however, the linear or non-linear relationships between invasive abundance and native population declines are less often studied. We examine how the amount and spatial distribution of experimental N deposition influences the relationship between non-native, invasive annual grass abundance (Bromus hordeaceus and Bromus diandrus) and a dominant, native perennial grass species (Stipa pulchra) in California. We hypothesized that native populations would decline as invasion increased, and that high nitrogen availability would cause native species to decline at lower invasion levels. We predicted that the rate of population decline would be slower in heterogeneous, compared to homogeneous, environments. We employed a field experiment that manipulated the amount and spatial heterogeneity of N addition across a range of invasive/native-dominated communities. There were strong negative and non-linear associations between level of invasion and S. pulchra proportional change (PC). Stipa pulchra PC was more negative and seedling survival was lower when N was added, and the negative effects of N addition on PC became larger in the final year of the study when S. pulchra had the largest declines. There was not strong evidence showing reduced competition in heterogeneous, compared to homogeneous, N treatments. Soil moisture was similar between S. pulchra and B. hordeaceus plots under ambient N, but B. hordeaceus under added N reduced soil moisture. Under N addition, Bromus spp. take up N earlier, reduce soil moisture, and create dry conditions in which S. pulchra declines.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of data and material

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Code availability

N/A.

References

  • Abraham JK, Corbin JD, D’Antonio CM (2009) California native and exotic perennial grasses differ in their response to soil nitrogen, exotic annual grass density, and order of emergence. Plant Ecol 201:445–456

    Google Scholar 

  • Angers DA, Caron J (1998) Plant-induced changes in soil structure: processes and feedbacks. Biogeochemistry (Dordr) 42:55–72

    Google Scholar 

  • Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Google Scholar 

  • Bobbink R et al (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59

    CAS  PubMed  Google Scholar 

  • Brook BW, Sodhi NS, Brandshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460

    PubMed  Google Scholar 

  • Chen B-M, D’Antonio CM, Molinari NA, Peng S-L (2017) Mechanisms of influence of invasive grass litter on germination and growth of coexisting species in California. Biol Invasions 20:1881–1897

    Google Scholar 

  • Cleland EE, Harpole WS (2010) Nitrogen enrichment and plant communities. Ann NY Acad Sci 1195:46–61

    CAS  PubMed  Google Scholar 

  • Corbin JD, D’Antonio CM (2004) Competition between native perennial and exotic annual grasses: implications for an historical invasion. Ecology 85:1273-1283. https://doi.org/10.1890/02-0744

    Article  Google Scholar 

  • D’Antonio CM, Chambers JC (2006) Using ecological theory to manage or restore ecosystems affected by invsive plant species. In: Falk DA, Palmer MA, Zedler JB (eds) Foundations of restoration ecology. Island Press, Washington, DC, pp 260–279

    Google Scholar 

  • D’Antonio CM, Mahall BE (1991) Root profiles and competition between the invasive, exotic perennial, Carpobrotus edulis, and 2 native shrub species in California coastal scrub. Am J Bot 78:885–894

    Google Scholar 

  • D’Antonio CM, Malmstrom C, Reynolds SA, Gerlach J (2007) Ecology of invasive non-native species in California grassland. In: Stromberg MR, Corbin JD, D’Antonio CM (eds) California grasslands: ecology and management. University of California Press, Berkeley

    Google Scholar 

  • Diffenbaugh NS, Swain DL, Touma D (2015) Anthropogenic warming has increased drought risk in California. Proc Natl Acad Sci 112:3931–3936

    CAS  PubMed  PubMed Central  Google Scholar 

  • Downey PO, Richardson DM (2016) Alien plant invasions and native plant extinctions: a six-threshold framework. AoB Plants. https://doi.org/10.1093/aobpla/plw047

    Article  PubMed  PubMed Central  Google Scholar 

  • Dyer AR, Rice KJ (1997) Intraspecific and diffuse competition: the response of Nassella pulchra in a California grassland. Ecol Appl 7:484-492

    Google Scholar 

  • Dyer AR, Rice KJ (1999) Effects of compeition on resource availability and growth of a California bunchgrass. Ecology 80:2697–2710

    Google Scholar 

  • Ehrenfeld JG (2003) Effect of exotic plant invasion on soil nutrient cycling processes. Ecosystems 6:503-523

    CAS  Google Scholar 

  • Eilts JA, Mittelbach GG, Reynolds HL, Gross KL (2011) Resource heterogeneity, soil fertility, and species diveristy: effects of clonal species on plant communities. Am Nat 177:574–588

    PubMed  Google Scholar 

  • Everard K, Seabloom EW, Harpole WS, de Mazancourt C (2010) Plant water use affects competition for nitrogen: why drought favors invasive species in California. Am Nat 175:85–97

    PubMed  Google Scholar 

  • Fagan WF, Holmes EE (2006) Quantifying the extinction vortex. Ecol Lett 9:51–60

    PubMed  Google Scholar 

  • Fenn ME et al (2003) Nitrogen emissions, deposition, and monitoring in the western United States. Bioscience 53:391–403

    Google Scholar 

  • Fenn ME et al (2010) Nitrogen critical loads and management alternatives for N-impacted ecosystems in California. J Environ Manag 91:2404–2423

    CAS  Google Scholar 

  • Fitch RL (2017) The effects of nitrogen, water, and topography on the distribution of Stipa pulchra. M.S., California State Polytechnic University, Pomona, Pomona, CA

  • Fitch RL, Questad EJ, Bobich EG (2019) Soil resource availability and its effect on the ecophysiology and establishment of Stipa pulchra. Plant Ecol. https://doi.org/10.1093/jpe/rty055 (Early View)

    Article  Google Scholar 

  • García-Palacios P, Maestre FT, Bardgett RD, de Kroon H (2012) Plant responses to soil heterogeneity and global environmental change. J Ecol 100:1303–1314

    PubMed  PubMed Central  Google Scholar 

  • Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–1191

    CAS  Google Scholar 

  • Gilliam FS, Walter CA, Adams MB, Peterjohn WT (2018) Nitrogen (N) dynamics in the mineral soil of a central Appalachian hardwood forest during a quarter century of whole-watershed N additions. Ecosystems 21:1489–1504

    CAS  Google Scholar 

  • Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of extinction. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 19–34

    Google Scholar 

  • Griffin D, Anchukaitis KJ (2014) How unusual is the 2012–2014 California drought? Geophys Res Lett 41:9017–9023

    Google Scholar 

  • Hamilton JG, Holzapfel C, Mahall BE (1999) Coexistence and interference between a native perennial grass and non-native annual grasses in California. Oecologia (Berl) 121:518–526

    CAS  Google Scholar 

  • Harpole WS, Goldstein L, Aicher R (2007) Resource limitation. In: Stromberg MR, Corbin JD, D’Antonio CM (eds) California grasslands: ecology and management. University of California Press, Berkeley

    Google Scholar 

  • Hernández E, Questad EJ, Meyer WM III, Suding KN (2018) The effects of nitrogen deposition and invasion on litter fuel quality and decomposition in a Stipa pulchra grassland. J Arid Environ 162:35–44

    Google Scholar 

  • HilleRisLambers J, Yelenik SG, Colman BP, Levine JM (2010) California annual grass invaders: the drivers or passengers of change? J Ecol 98:1147–1156. https://doi.org/10.1111/j.1365-2745.2010.01706.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Holmes TH, Rice KJ (1996) Patterns of growth and soil-water utilization in some exotic annuals and native perennial bunchgrasses of California. Ann Bot 78:233–243

    Google Scholar 

  • Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293

    CAS  Google Scholar 

  • Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478–491

    Google Scholar 

  • Hulvey KB, Teller BJ (2018) Site conditions determine a key native plant’s contribution to invasion resistance in grasslands. Ecology 99:1257–1264

    PubMed  Google Scholar 

  • Hulvey KB, Zavaleta ES (2012) Abundance declines of a native forb have nonlinear impacts on grassland invasion resistance. Ecology 93:378–388

    PubMed  Google Scholar 

  • Jackson LE (1985) Ecological origins of California’s Mediterranean grasses. J Biogeogr 12:349–361

    Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-3.2

  • Larios L, Suding KN (2013) Restoration within protected areas: when and how to intervene to manage plant invasions? In: Foxcroft LC, Pyšek P, Richardson DM, Genovesi P (eds) Plant invasions in protected areas, vol 7. Springer, Dordrecht

    Google Scholar 

  • Leibold MA et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613

    Google Scholar 

  • Lenth RV (2021) emmeans: estimated marginal means, aka least-squares means. R package version 1.6.3

  • Levine JM, Vila M, D'Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B Biol Sci 270:775–781. https://doi.org/10.1098/rspb.2003.2327

    Article  Google Scholar 

  • Lombardo K, Fehmi JS, Rice KJ, Laca EA (2007) Nassella pulchra survival and water relations depend more on site productivity than on small-scale disturbance. Restor Ecol 15:177–178

    Google Scholar 

  • MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55

    Google Scholar 

  • Mack MC, D’Antonio CM, Ley RE (2001) Alteration of ecosystem nitrogen dynamics by exotic plants: a case study of C-4 grasses in Hawaii. Ecol Appl 11:1323–1335

    Google Scholar 

  • Marty JT, Collinge SK, Rice KJ (2005) Responses of a remnant California native bunchgrass population to grazing, burning and climatic variation. Plant Ecol 181:101-112. https://doi.org/10.1007/s11258-005-3797-z

    Article  Google Scholar 

  • Mazerolle MJ (2019) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c), vol. R package version 2.2-2

  • Molinari NA, D’Antonio CM (2020) Where have all the wildflowers gone? The role of exotic grass thatch. Biol Invasions 22:957–968

    Google Scholar 

  • Mordecai EA, Molinari NA, Stahlheber KA, Gross K, D’Antonio C (2015) Controls over native perennial grass exclusion and persistence in California grasslands invaded by annuals. Ecology 96:2643–2652. https://doi.org/10.1890/14-2023.1.sm

    Article  PubMed  Google Scholar 

  • Questad EJ, Thaxton JM, Cordell S (2012) Patterns and consequences of re-invasion into a Hawaiian dry forest restoration. Biol Invasions 14:2573–2586

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rao LE, Allen EB (2010) Combined effects of precipitation and nitrogen deposition on native and invasive winter annual production in California deserts. Oecologia (Berl) 162:1035–1046

    Google Scholar 

  • Reynolds HL, Mittelbach GG, Darcy-Hall TL, Houseman GR, Gross KL (2007) No effect of varying soil resource heterogeneity on plant species richness in a low fertility grassland. J Ecol 95:723–733

    Google Scholar 

  • Robeson SM (2015) Revisiting the recent California drought as an extreme value. Geophys Res Lett 42:6771–6779

    Google Scholar 

  • Schellenberg F, Irvine IC, Witter MS, Nielsen AT, Raulund-Rasmussen K (2020) Effects of drought and fire on native Stipa pulchra (poaceae) recovery in southern California grasslands. Madrono 67:9–18. https://doi.org/10.3120/0024-9637-67.1.9

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stromberg MR, D’Antonio CM, Young TP, Wirka J, Kephart P (2007) California grassland restoration. In: Stromberg MR, Corbin JD, D’Antonio C (eds) California grasslands: ecology and management. University of California Press, Berkeley

    Google Scholar 

  • Suding KN, Hobbs RJ (2009) Threshold models in restoration and conservation: a developing framework. Trends Ecol Evol 24:271–279

    PubMed  Google Scholar 

  • Tamme R, Hiiesalu I, Laanisto L, Szava-Kovats R, Pärtel M (2010) Environmental heterogeneity, species diversity and co-existence at different spatial scales. J Veg Sci 21:796–801

    Google Scholar 

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

    Google Scholar 

  • Tonnesen G, Wang Z, Omary M, Chien C (2007) Assessment of N deposition: modeling and habitat assessment. California Energy Commission, PIER Energy-Related Environmental Research CEC-500-2005-032

  • Vallano DM, Selmants PC, Zavaleta ES (2012) Simulated nitrogen deposition enhances the performance of an exotic grass relative to native serpentine grassland competitors. Plant Ecol 213:1015–1026

    Google Scholar 

  • Vaughn KJ et al (2011) California perennial grasses are physiologically distinct from both Mediterranean annual and perennial grasses. Plant Soil 345:37–46. https://doi.org/10.1007/s11104-011-0757-3

    Article  CAS  Google Scholar 

  • Wacker L, Baudois O, Eichenberger-Glinz S, Schmid B (2008) Environmental heterogeneity increases complementarity in experimental grassland communities. Basic Appl Ecol 9:467–474

    Google Scholar 

  • Weiss SB (1999) Cars, cows, and checkerspot butterflies: nitrogen deposition and management of nutrient-poor grasslands for a threatened species. Conserv Biol 13:1476–1486

    Google Scholar 

  • Williams AP, Seager R, Abatzoglou JT, Cook BI, Smerdon JE, Cook ER (2015) Contribution of anthropogenic warming to California drought during 2012–2014. Geophys Res Lett 42:6819–6828

    Google Scholar 

  • Zavaleta ES et al (2003) Grassland responses to three years of elevated temperature, CO(2), precipitation, and N deposition. Ecol Monogr 73:585–604

    Google Scholar 

  • Zuur AF, Ieno EN (2016) Beginner’s guide to zero-inflated models with R. Highland Statistics Ltd, Newburgh, UK

    Google Scholar 

Download references

Acknowledgements

The University of California Agriculture and Natural Resources Division (Research Agreement No. 201013829-22) and National Science Foundation (DEB-0614168) provided funding for the experiment. We thank J. Watkins and the staff of South Coast REC for logistical support, and C. Stein and L. Larios for support with experimental planting and manipulations. H. Jones, R. Marks, B. Myers, M. Hubbell, G. Morrison, and L. Quon assisted with data collection and analysis.

Funding

The University of California Agriculture and Natural Resources Division (Research Agreement No. 201013829-22) and National Science Foundation (DEB-0614168) provided funding for the experiment.

Author information

Authors and Affiliations

Authors

Contributions

EJQ and KNS conceived and designed the experiments. All authors performed the experiments. EJQ and RLF analyzed the data. EJQ wrote the manuscript; all other authors provided editorial advice.

Corresponding author

Correspondence to Erin J. Questad.

Ethics declarations

Conflict of interest

The authors do not have any conflicts of interest to disclose.

Ethics approval

Ethics approval was not required for this study.

Consent to participate

N/A.

Consent for publication

N/A.

Additional information

Communicated by Jennifer Funk.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 88 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Questad, E.J., Fitch, R.L., Paolini, J. et al. Nitrogen addition, not heterogeneity, alters the relationship between invasion and native decline in California grasslands. Oecologia 197, 651–660 (2021). https://doi.org/10.1007/s00442-021-05049-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-021-05049-9

Keywords

Navigation