Skip to main content

Advertisement

SpringerLink
Log in

Complex facilitation and competition in a temperate grassland: loss of plant diversity and elevated CO2 have divergent and opposite effects on oak establishment

  • Community ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Encroachment of woody vegetation into grasslands is a widespread phenomenon that alters plant community composition and ecosystem function. Woody encroachment is often the result of fire suppression, but it may also be related to changes in resource availability associated with global environmental change. We tested the relative strength of three important global change factors (CO2 enrichment, nitrogen deposition, and loss of herbaceous plant diversity) on the first 3 years of bur oak (Quercus macrocarpa) seedling performance in a field experiment in central Minnesota, USA. We found that loss of plant diversity decreased initial oak survival but increased overall oak growth. Conversely, elevated CO2 increased initial oak seedling survival and reduced overall growth, especially at low levels of diversity. Nitrogen deposition surprisingly had no net effect on survival or growth. The magnitude of these effects indicates that long-term woody encroachment trends may be most strongly associated with those few individuals that survive, but grow much larger in lower diversity patches. Further, while the CO2 results and the species richness results appear to describe opposing trends, this is due only to the fact that the natural drivers are moving in opposite directions (decreasing species richness and increasing CO2). Interestingly, the mechanisms that underlie both patterns are very similar, increased CO2 and increased species richness both increase herbaceous biomass which (1) increases belowground competition for resources and (2) increases facilitation of early plant survival under a more diverse plant canopy; in other words, both competition and facilitation help determine community composition in these grasslands.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abrams PA (1995) Monotonic or unimodal diversity-productivity gradients: what does competition theory predict? Ecology 76:2019–2027

    Article  Google Scholar 

  • Adair CE, Reich PB, Trost JJ, Hobbie SE (2011) Elevated CO2 stimulates grassland soil respiration by increasing carbon inputs rather than by enhancing soil moisture. Glob Change Biol 17:3546–3563

    Article  Google Scholar 

  • Adler PB, Seabloom EW, Borer ET, Hillebrand H, Hautier Y, Hector A, Harpole WS, O’halloran LR, Grace JB, Anderson TM, Bakker JD, Biederman LA, Brown CS, Buckley YM, Calabrese LB, Chu C-J, Cleland EE, Collins SL, Cottingham KL, Crawley MJ, Damschen EI, Davies KF, Decrappeo NM, Fay PA, Firn J, Frater P, Gasarch EI, Gruner DS, Hagenah N, Hille Ris Lambers J, Humphries H, Jin VL, Kay AD, Kirkman KP, Klein JA, Knops JMH, La Pierre KJ, Lambrinos JG, Li W, Macdougall AS, Mcculley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan JW, Mortensen B, Orrock JL, Prober SM, Pyke DA, Risch AC, Schuetz M, Smith MD, Stevens CJ, Sullivan LL, Wang G, Wragg PD, Wright JP, Yang LH (2011) Productivity is a poor predictor of plant species richness. Science 333:1750–1753. doi:10.1126/science.1204498

    Article  PubMed  CAS  Google Scholar 

  • Archer S (1989) Have southern Texas savannas been converted to woodlands in recent history? Am Nat 134:545–561

    Article  Google Scholar 

  • Archer S, Schimel D, Holland E (1995) Mechanisms of shrubland expansion: land use, climate or CO2? Climatic Change 29:91–99

    Article  Google Scholar 

  • Barger NN, Archer SR, Campbell JL, Huang C-Y, Morton JA, Knapp AK (2011) Woody plant proliferation in North American drylands: a synthesis of impacts on ecosystem carbon balance. J Geophys Res 116:G00K07. doi:10.1029/2010JG001506

    Article  Google Scholar 

  • Bengtsson J, Engelhardt K, Giller P, Hobbie S, Lawrence D, Levine J, Vila M, Wolters V (2002) Slippin’ and slidin’ between the scales: the scaling components of biodiversity–ecosystem functioning relations. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning synthesis and perspectives. Oxford University Press, New York, pp 209–220

    Google Scholar 

  • Bertness M, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193

    Article  PubMed  CAS  Google Scholar 

  • Bolker B, Brooks M, Clark C, Geange S, Poulsen J, Stevens M, White J (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Bond WJ, Midgley GF (2000) A proposed CO2-controlled mechanism of woody plant invasion in grasslands and savannas. Glob Change Biol 6:865–869

    Article  Google Scholar 

  • Brown J, Archer S (1989) Woody plant invasion of grasslands: establishment of honey mesquite (Prosopis glandulosa var. glandulosa) on sites differing in herbaceous biomass and grazing history. Oecologia 80:19–26

    Article  Google Scholar 

  • Brown J, Archer S (1999) Shrub invasion of grassland: recruitment is continuous and not regulated by herbaceous biomass or density. Ecology 80:2385–2396

    Article  Google Scholar 

  • Bruno J, Stachowicz J, Bertness M (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Bulleri F, Bruno J, Benedetti-Cecchi L (2008) Beyond competition: incorporating positive interactions between species to predict ecosystem invasibility. PLoS Biol 6:e162

    Article  PubMed  Google Scholar 

  • Bustamente-Sanchez MA, Armesto JJ, Halpern CB (2011) Biotic and abiotic controls on tree colonization in three early successional communities of Chiloé Island, Chile. J Ecol 99(1):228–299

    Google Scholar 

  • Callaway R (1995) Positive interactions among plants. Bot Rev 61:306–349

    Article  Google Scholar 

  • Callaway R, Walker L (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965

    Article  Google Scholar 

  • Chase JM, Ryberg WA (2004) Connectivity, scale-dependence, and the productivity-diversity relationship. Ecol Lett 7:676–683. doi:10.1111/j.1461-0248.2004.00622.x

    Article  Google Scholar 

  • Classen A, Norby R, Campany C, Sides K (2010) Climate change alters seedling emergence and establishment in an old-field ecosystem. PLoS One e13476:1–8

    Google Scholar 

  • Cuesta B, Villar-Salvador P, Puértolas J, Rey Benayas JM, Michalet R (2010) Facilitation of Quercus ilex in Mediterranean shrubland is explained by both direct and indirect interactions mediated by herbs. J Ecol 98:687–696. doi:10.1111/j.1365-2745.2010.01655.x

    Article  Google Scholar 

  • Davis M, Wrage K, Reich P (1998) Competition between tree seedlings and herbaceous vegetation: support for a theory of resource supply and demand. J Ecol 86:652–661

    Google Scholar 

  • Davis M, Wrage K, Reich P, Tjoelker M, Schaeffer T, Muermann C (1999) Survival, growth, and photosynthesis of tree seedlings competing with herbaceous vegetation along a water-light-nitrogen gradient. Plant Ecol 145:341–350

    Article  Google Scholar 

  • Davis MA, Reich PB, Knoll MJB, Dooley L, Hundtoft M, Attleson I (2007) Elevated atmospheric CO2: a nurse plant substitute for oak seedlings establishing in old fields. Glob Change Biol 13:2308–2316. doi:10.1111/j.1365-2486.2007.01444.x

    Article  Google Scholar 

  • Dickie IA, Schnitzer SA, Reich PB, Hobbie SE (2007) Is oak establishment in old-fields and savanna openings context dependent? J Ecol 95:309–320. doi:10.1111/j.1365-2745.2006.01202.x

    Article  Google Scholar 

  • Dijkstra F, Hobbie S, Reich P, Knops J (2005) Divergent effects of elevated CO2, N fertilization, and plant diversity on soil C and N dynamics in a grassland field experiment. Plant Soil 272:41–52

    Article  CAS  Google Scholar 

  • Fargione JE, Tilman D (2005) Diversity decreases invasion via both sampling and complementarity effects. Ecol Lett 8:604–611. doi:10.1111/j.1461-0248.2005.00753.x

    Article  Google Scholar 

  • Farrer EC, Goldberg DE (2011) Patterns and mechanisms of conspecific and heterospecific interactions in a dry perennial grassland. J Ecol 99(1):265–276

    Google Scholar 

  • Fensham R, Fairfax R, Archer S (2005) Rainfall, land use and woody vegetation cover change in semi-arid Australian savanna. Ecology 93:596–606

    Google Scholar 

  • Hoekstra JM, Boucher TM, Ricketts TH, Roberts C (2004) Confronting a biome crisis: global disparities of habitat loss and protection. Ecol Lett 8:23–29. doi:10.1111/j.1461-0248.2004.00686.x

    Article  Google Scholar 

  • Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, Van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202. doi:10.1038/nature10282

    Article  PubMed  CAS  Google Scholar 

  • Jackson R, Banner J, Jobbágy E, Pockman W, Wall D (2002) Ecosystem carbon loss with woody plant invasion of grasslands. Nature 418:623–626

    Article  PubMed  CAS  Google Scholar 

  • Kennedy T, Naeem S, Howe K, Knops J, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638

    Article  PubMed  CAS  Google Scholar 

  • Kgope BS, Bond WJ, Midgley GF (2009) Growth responses of African savanna trees implicate atmospheric [CO2] as a driver of past and current changes in savanna tree cover. Aust Ecol 35:451–463. doi:10.1111/j.1442-9993.2009.02046.x

    Article  Google Scholar 

  • Knapp AK, Briggs JM, Collins SL, Archer SR, Bret-Harte MS, Ewers BE, Peters DP, Young DR, Shaver GR, Pendall E, Cleary MB (2008) Shrub encroachment in North American grasslands: shifts in growth form dominance rapidly alters control of ecosystem carbon inputs. Glob Change Biol 14:615–623. doi:10.1111/j.1365-2486.2007.01512.x

    Article  Google Scholar 

  • Knops JMH (2006) Fire does not alter vegetation in infertile prairie. Oecologia 150:477–483. doi:10.1007/s00442-006-0535-8

    Article  PubMed  Google Scholar 

  • McCulley R, Archer S, Boutton T, Hons F, Zuberer D (2004) Soil respiration and nutrient cycling in wooded communities developing in grassland. Ecology 85:2804–2817

    Article  Google Scholar 

  • McKinley D, Blair J (2008) Woody plant encroachment by Juniperus virginiana in a mesic native grassland promotes rapid carbon and nitrogen accrual. Ecosystems 11(3):454–468. doi:10.1007/s10021-008-9133-4

    Article  CAS  Google Scholar 

  • Miriti MN (2006) Ontogenetic shift from facilitation to competition in a desert shrub. J Ecol 94:973–979. doi:10.1111/j.1365-2745.2006.01138.x

    Article  Google Scholar 

  • Montgomery RA, Reich PB, Palik BJ (2010) Untangling positive and negative biotic interactions: views from above and below ground in a forest ecosystem. Ecology 91:3641–3655

    Article  PubMed  Google Scholar 

  • Naeem S, Knops J, Tilman D, Howe K, Kennedy T, Gale S (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos:91:97–108

    Google Scholar 

  • Niinemets à (2010) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manage 260:1623–1639. doi:10.1016/j.foreco.2010.07.054

    Article  Google Scholar 

  • Ovington J, MacRae C (1960) The growth of seedlings of Quercus petraea. J Ecol 48:549–555

    Article  Google Scholar 

  • Peterson D, Reich P (2001) Prescribed fire in oak savanna: fire frequency effects on stand structure and dynamics. Ecol Appl 11:914–927

    Article  Google Scholar 

  • Polley WH, Johnson H, Tischler C (2003) Woody invasion of grasslands: evidence that CO2 enrichment indirectly promotes establishment of Prosopis glandulosa. Plant Ecol 164:85–94

    Article  Google Scholar 

  • Post W, Emanuel W, Zinke P, Stangenberger A (1982) Soil carbon pools and world life zones. Nature 298:156–159

    Google Scholar 

  • Reich PB (2009) Elevated CO2 reduces losses of plant diversity caused by nitrogen deposition. Science 326:1399–1402. doi:10.1126/science.1178820

    Article  PubMed  CAS  Google Scholar 

  • Reich P, Knops J, Tilman D, Craine J, Ellsworth D, Tjoelker M, Lee T, Wedin D, Naeem S, Bahauddin D (2001a) Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410:809–810

    Article  PubMed  CAS  Google Scholar 

  • Reich P, Peterson D, Wedin D, Wrage K (2001b) Fire and vegetation effects on productivity and nitrogen cycling across a forest–grassland continuum. Ecology 82:1703–1719

    Google Scholar 

  • Reich P, Tilman D, Craine J, Ellsworth D, Tjoelker M, Knops J, Wedin D, Naeem S, Bahauddin D, Goth J (2001c) Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? A field test with 16 grassland species. New Phytol 150:435–448

    Google Scholar 

  • Reich PB, Frelich LE, Voldseth RA, Bakken P, Adair EC (2012) Understorey diversity in southern boreal forests is regulated by productivity and its indirect impacts on resource availability and heterogeneity. J Ecol 100:539–545. doi:10.1111/j.1365-2745.2011.01922.x

    Article  Google Scholar 

  • Roques K, O’connor T, Watkinson A (2001) Dynamics of shrub encroachment in an African savanna: relative influences of fire, herbivory, rainfall and density dependence. J Appl Ecol 38:268–280

    Google Scholar 

  • Roscher C, Temperton VM, Scherer-Lorenzen M, Schmitz M, Schumacher J, Schmid B, Buchmann N, Weisser WW, Schulze E-D (2005) Overyielding in experimental grassland communities: irrespective of species pool or spatial scale. Ecol Lett 8:419–429. doi:10.1111/j.1461-0248.2005.00736.x

    Article  Google Scholar 

  • Schnitzer S, Klironomos J, HilleRisLambers J, Kinkel L, Reich P, Xiao K, Rillig M, Sikes B, Callaway R, Mangan S (2011) Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92:296–303

    Article  PubMed  Google Scholar 

  • Silva J, Zambrano A, Fariñas M (2001) Increase in the woody component of seasonal savannas under different fire regimes in Calabozo, Venezuela. J Biogeogr 28:977–983

    Google Scholar 

  • Staver AC, Archibald S, Levin SA (2011) The global extent and determinants of savanna and forest as alternative biome states. Science 334:230–232. doi:10.1126/science.1210465

    Article  PubMed  CAS  Google Scholar 

  • Tilman D (1987) Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57:189–214

    Article  Google Scholar 

  • Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997a) The influence of functional diversity and composition on ecosystem processes. Science 277:1300

    Article  CAS  Google Scholar 

  • Tilman D, Lehman C, Thomson K (1997b) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861

    Article  PubMed  CAS  Google Scholar 

  • Tilman D, Reich P, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845

    Article  PubMed  CAS  Google Scholar 

  • Van Auken O (2000) Shrub invasions of North American semiarid grasslands. Annu Rev Ecol Syst 31:197–215

    Article  Google Scholar 

  • Van Auken O, Bush J (1997) Growth of Prosopis glandulosa in response to changes in aboveground and belowground interference. Ecology 78:1222–1229

    Article  Google Scholar 

  • van Ruijven J, Berendse F (2003) Positive effects of plant species diversity on productivity in the absence of legumes. Ecol Lett 6:170–175

    Article  Google Scholar 

  • Vitousek P, Mooney H, Lubchenco J, Melillo J (1997) Human domination of earth’s ecosystems. Science 277:494

    Article  CAS  Google Scholar 

  • Zhang Y, Chen HYH, Reich PB (2012) Forest productivity increases with evenness, species richness and trait variation: a global meta-analysis. J Ecology. doi:10.1111/j.1365-2745.2011.01944.x

Download references

Acknowledgments

This research was supported by the Department of Energy Program for Ecological Research Grant DE-FG02-96ER62291, the National Science Foundation Long-term Ecological Research Grant DEB-0080382, the NSF Long-term Research in Environmental Biology DEB-0716587, the University of Minnesota, the University of Wisconsin–Milwaukee (UWM) AOP program, the UWM Department of Biological Sciences, and the NSF Graduate Research Fellowship Program. IAD was additionally supported by the New Zealand Ministry of Science and Innovation (Ecosystem Resilience OBI). We thank Sarah Christman and all other Cedar Creek interns for field assistance, and Joe Mascaro and Ramesh Laungani for helpful comments during the writing process. The authors declare that they have no conflict of interest and that all experiments were conducted in compliance with U.S. law.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Wisconsin–Milwaukee, Lapham Hall, 3209 N. Maryland Ave., Milwaukee, WI, 53211, USA

    Alexandra Wright, Stefan A. Schnitzer & Scott A. Mangan

  2. Landcare Research, Lincoln, New Zealand

    Ian A. Dickie

  3. Biology Department, Duke University, Durham, NC, USA

    Alex R. Gunderson

  4. Department of Mathematical Sciences, University of Wisconsin–Milwaukee, Milwaukee, USA

    Gabriella A. Pinter

  5. Department of Forest Resources, University of Minnesota, St. Paul, MN, USA

    Peter B. Reich

  6. Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, NSW, 2751, Australia

    Peter B. Reich

Authors
  1. Alexandra Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan A. Schnitzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ian A. Dickie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alex R. Gunderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gabriella A. Pinter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Scott A. Mangan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Peter B. Reich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexandra Wright.

Additional information

Communicated by Scott Collins.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 89 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wright, A., Schnitzer, S.A., Dickie, I.A. et al. Complex facilitation and competition in a temperate grassland: loss of plant diversity and elevated CO2 have divergent and opposite effects on oak establishment. Oecologia 171, 449–458 (2013). https://doi.org/10.1007/s00442-012-2420-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-012-2420-y

Keywords

Search

Navigation