Abstract
A trend of increasing woody plant density, or woody thickening, has been observed across grassland and woodland ecosystems globally. It has been proposed that increasing atmospheric [CO2] is a major driver of broad scale woody thickening, though few field-based experiments have tested this hypothesis. Our study utilises a Free Air CO2 Enrichment experiment to examine the effect of elevated [CO2] (eCO2) on three mechanisms that can cause woody thickening, namely (i) woody plant recruitment, (ii) seedling growth, and (iii) post-disturbance resprouting. The study took place in a eucalypt-dominated temperate grassy woodland. Annual assessments show that juvenile woody plant recruitment occurred over the first 3 years of CO2 fumigation, though eCO2 did not affect rates of recruitment. Manipulative experiments were established to examine the effect of eCO2 on above-ground seedling growth using transplanted Eucalyptus tereticornis (Myrtaceae) and Hakea sericea (Proteaceae) seedlings. There was no positive effect of eCO2 on biomass of either species following 12 months of exposure to treatments. Lignotubers (i.e., resprouting organs) of harvested E. tereticornis seedlings that were retained in situ for an additional year were used to examine resprouting response. The likelihood of resprouting and biomass of resprouts increased with lignotuber volume, which was not itself affected by eCO2. The presence of herbaceous competitors and defoliation by invertebrates and pathogens were found to greatly reduce growth and/or resprouting response of seedlings. Our findings do not support the hypothesis that future increases in atmospheric [CO2] will, by itself, promote woody plant recruitment in eucalypt-dominated temperate grassy woodlands.
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References
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372. https://doi.org/10.1111/j.1469-8137.2004.01224.x
Asner GP, Archer S, Hughes RF, Ansley RJ, Wessman CA (2003) Net changes in regional woody vegetation cover and carbon storage in Texas Drylands, 1937–1999. Glob Change Biol 9:316–335. https://doi.org/10.1046/j.1365-2486.2003.00594.x
Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6 p
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):48. https://doi.org/10.18637/jss.v067.i01
Bloor JMG, Barthes L, Leadley PW (2008) Effects of elevated CO2 and N on tree–grass interactions: an experimental test using Fraxinus excelsior and Dactylis glomerata. Funct Ecol 22:537–546. https://doi.org/10.1111/j.1365-2435.2008.01390.x
Bond WJ, Keeley JE (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol Evol 20:387–394. https://doi.org/10.1016/j.tree.2005.04.025
Bond WJ, Midgley GF (2012) Carbon dioxide and the uneasy interactions of trees and savannah grasses. Philos Transact R Soc Lond B 367:601–612. https://doi.org/10.1098/rstb.2011.0182
Bond WJ, van Wilgen BW (1996) Fire and Plants. Chapman & Hall, London
Bradstock RA (2010) A biogeographic model of fire regimes in Australia: current and future implications. Glob Ecol Biogeogr 19:145–158
Ceulemans R, Janssens IA, Jach ME (1999) Effects of CO2 enrichment on trees and forests: lessons to be learned in view of future ecosystem studies. Ann Bot 84:577–590. https://doi.org/10.1006/anbo.1999.0945
Clarke PJ (2002) Experiments on tree and shrub establishment in temperate grassy woodlands: seedling survival. Austral Ecol 27:606–615. https://doi.org/10.1046/j.1442-9993.2002.01221.x
Clarke PJ et al (2012) Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. New Phytol 197(1):19–35. https://doi.org/10.1111/nph.12001
Clarke PJ, Manea A, Leishman MR (2016) Are fire resprouters more carbon limited than non-resprouters? Effects of elevated CO2 on biomass, storage and allocation of woody species. Plant Ecol 217:763–771. https://doi.org/10.1007/s11258-015-0528-y
Collins L, Bradstock RA, Resco de Dios V, Duursma RA, Velasco S, Boer MM (2018) Understorey productivity in temperate grassy woodland responds to soil water availability but not to elevated [CO2]. Glob Change Biol. https://doi.org/10.1111/gcb.14038
Davis MA, Reich PB, Knoll MJB, Dooley LEE, 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. https://doi.org/10.1111/j.1365-2486.2007.01444.x
Donohue RJ, Roderick ML, McVicar TR, Farquhar GD (2013) Impact of CO2 fertilization on maximum foliage cover across the globe’s warm, arid environments. Geophys Res Lett 40:3031–3035. https://doi.org/10.1002/grl.50563
Drake JE et al (2016) Short-term carbon cycling responses of a mature eucalypt woodland to gradual stepwise enrichment of atmospheric CO2 concentration. Glob Change Biol 22:380–390. https://doi.org/10.1111/gcb.13109
Duursma RA, Gimeno TE, Boer MM, Crous KY, Tjoelker MG, Ellsworth DS (2016) Canopy leaf area of a mature evergreen Eucalyptus woodland does not respond to elevated atmospheric [CO2] but tracks water availability. Glob Change Biol 22:1666–1676. https://doi.org/10.1111/gcb.13151
Eamus D, Palmer AR (2007) Is climate change a possible explanation for woody thickening in arid and semi-arid regions? Res Lett Ecol 2007:5. https://doi.org/10.1155/2007/37364
Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol Lett 14:709–722. https://doi.org/10.1111/j.1461-0248.2011.01630.x
Ellsworth DS et al (2017) Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nat Clim Change 7:279–282. https://doi.org/10.1038/nclimate3235
Facey SL, Ellsworth DS, Staley JT, Wright DJ, Johnson SN (2014) Upsetting the order: how climate and atmospheric change affects herbivore–enemy interactions. Curr Opin Insect Sci 5:66–74. https://doi.org/10.1016/j.cois.2014.09.015
Fensham RJ, Fairfax RJ (2006) Can burning restrict eucalypt invasion on grassy balds? Austral Ecol 31:317–325. https://doi.org/10.1111/j.1442-9993.2006.01560.x
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks CA
Gimeno TE et al (2016) Conserved stomatal behaviour under elevated CO2 and varying water availability in a mature woodland. Funct Ecol 30:700–709. https://doi.org/10.1111/1365-2435.12532
Hasegawa S, Macdonald CA, Power SA (2016) Elevated carbon dioxide increases soil nitrogen and phosphorus availability in a phosphorus-limited Eucalyptus woodland. Glob Change Biol 22:1628–1643. https://doi.org/10.1111/gcb.13147
Hättenschwiler S, Körner C (2003) Does elevated CO2 facilitate naturalization of the non-indigenous Prunus laurocerasus in Swiss temperate forests? Funct Ecol 17:778–785. https://doi.org/10.1111/j.1365-2435.2003.00785.x
Hoffmann AW, Bazzaz AF, Chatterton JN, Harrison AP, Jackson BR (2000) Elevated CO2 enhances resprouting of a tropical savanna tree. Oecologia 123:312–317. https://doi.org/10.1007/s004420051017
Hovenden MJ, Williams AL (2010) The impacts of rising CO2 concentrations on Australian terrestrial species and ecosystems. Austral Ecol 35:665–684. https://doi.org/10.1111/j.1442-9993.2009.02074.x
John JA, Draper NR (1980) An alternative family of transformations. J R Stat Soc 29:190–197. https://doi.org/10.2307/2986305
Katz DSW (2016) The effects of invertebrate herbivores on plant population growth: a meta-regression analysis. Oecologia 182:43–53. https://doi.org/10.1007/s00442-016-3602-9
Kgope BS, Bond WJ, Midgley GF (2010) Growth responses of African savanna trees implicate atmospheric [CO2] as a driver of past and current changes in savanna tree cover. Austral Ecol 35:451–463. https://doi.org/10.1111/j.1442-9993.2009.02046.x
Kim D, Oren R, Qian SS (2016) Response to CO2 enrichment of understory vegetation in the shade of forests. Glob Change Biol 22:944–956. https://doi.org/10.1111/gcb.13126
Klimešová J, Klimeš L (2007) Bud banks and their role in vegetative regeneration – A literature review and proposal for simple classification and assessment. Persp Plant Ecol 8:115–129. https://doi.org/10.1016/j.ppees.2006.10.002
Knox KJE, Clarke PJ (2006) Response of resprouting shrubs to repeated fires in the Dry Sclerophyll Forest of Gibraltar Range National Park. Proc Linn Soc N S W 127:49–56
Lunt ID, Winsemius LM, McDonald SP, Morgan JW, Dehaan RL (2010) How widespread is woody plant encroachment in temperate Australia? Changes in woody vegetation cover in lowland woodland and coastal ecosystems in Victoria from 1989 to 2005. J Biogeogr 37:722–732. https://doi.org/10.1111/j.1365-2699.2009.02255.x
Lunt ID, Prober SM, Morgan JW (2012) How do fire regimes affect ecosystem structure, function and diversity in grasslands and grassy woodlands of southern Australia? In: Bradstock RA, Gill AM, Williams RJ (eds) Flammable Australia: fire regimes, biodiversity and ecosystems in a changing world. CSIRO, Melbourne, pp 253–270
Manea A, Leishman MR (2014) Competitive interactions between established grasses and woody plant seedlings under elevated CO2 levels are mediated by soil water availability. Oecologia 177:499–506. https://doi.org/10.1007/s00442-014-3143-z
Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc 273:2575–2584. https://doi.org/10.1098/rspb.2006.3587
McCarthy HR et al (2010) Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytol 185:514–528. https://doi.org/10.1111/j.1469-8137.2009.03078.x
Mohan JE, Clark JS, Schlesinger WH (2007) Long-term CO2 enrichment of a forest ecosystem: implications for forest regeneration and succession. Ecol Appl 17:1198–1212. https://doi.org/10.1890/05-1690
Morgan JA et al (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140:11–25. https://doi.org/10.1007/s00442-004-1550-2
Morgan JA, Milchunas DG, LeCain DR, West M, Mosier AR (2007) Carbon dioxide enrichment alters plant community structure and accelerates shrub growth in the shortgrass steppe. Proc Natl Acad Sci 104:14724–14729. https://doi.org/10.1073/pnas.0703427104
Ochoa-Hueso R et al (2017) Rhizosphere-driven increase in nitrogen and phosphorus availability under elevated atmospheric CO2 in a mature Eucalyptus woodland. Plant Soil 416:283–295. https://doi.org/10.1007/s11104-017-3212-2
Pathare VS, Crous KY, Cooke J, Creek D, Ghannoum O, Ellsworth DS (2017) Water availability affects seasonal CO2-induced photosynthetic enhancement in herbaceous species in a periodically dry woodland. Glob Change Biol 23:5164–5178. https://doi.org/10.1111/gcb.13778
Polley HW, Mayeux HS, Johnson HB, Tischler CR (1997) Viewpoint: atmospheric CO2, soil water, and shrub/grass ratios on rangelands. J Range Manage 50:278–284. https://doi.org/10.2307/4003730
Poorter H, Navas M-L (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
Robinson EA, Ryan GD, Newman JA (2012) A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336. https://doi.org/10.1111/j.1469-8137.2012.04074.x
Sankaran M, Ratnam J, Hanan N (2008) Woody cover in African savannas: the role of resources, fire and herbivory. Glob Ecol Biogeogr 17:236–245. https://doi.org/10.1111/j.1466-8238.2007.00360.x
Skinner AK, Lunt ID, McIntyre S, Spooner PG, Lavorel S (2010) Eucalyptus recruitment in degraded woodlands: no benefit from elevated soil fertility. Plant Ecol 208:359–370. https://doi.org/10.1007/s11258-009-9712-2
Souza L, Belote RT, Kardol P, Weltzin JF, Norby RJ (2010) CO2 enrichment accelerates successional development of an understory plant community. J Plant Ecol 3(1):31–39. https://doi.org/10.1093/jpe/rtp032
Stevens N, Lehmann CER, Murphy BP, Durigan G (2017) Savanna woody encroachment is widespread across three continents. Glob Change Biol 23:235–244. https://doi.org/10.1111/gcb.13409
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Tian F, Brandt M, Liu YY, Rasmussen K, Fensholt R (2016) Mapping gains and losses in woody vegetation across global tropical drylands. Glob Change Biol 23:1748–1760. https://doi.org/10.1111/gcb.13464
Tjoelker MG, Oleksyn J, Reich PB (1998) Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO2 and temperature. Tree Physiol 18:715–726. https://doi.org/10.1093/treephys/18.11.715
Van Auken OW (2009) Causes and consequences of woody plant encroachment into western North American grasslands. J Environ Manage 90:2931–2942. https://doi.org/10.1016/j.jenvman.2009.04.023
Walters JR, Bell TL, Read S (2005) Intra-specific variation in carbohydrate reserves and sprouting ability in Eucalyptus obliqua seedlings. Aust J Bot 53:195–203. https://doi.org/10.1071/BT04016
Wang D, Heckathorn SA, Wang X, Philpott SM (2011) A meta-analysis of plant physiological and growth responses to temperature and elevated CO2. Oecologia 169:1–13. https://doi.org/10.1007/s00442-011-2172-0
Wigley BJ, Bond WJ, Hoffman MT (2010) Thicket expansion in a South African savanna under divergent land use: local vs. global drivers? Glob Change Biol 16:964–976. https://doi.org/10.1111/j.1365-2486.2009.02030.x
Wright A et al (2013) 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. https://doi.org/10.1007/s00442-012-2420-y
Zavaleta ES (2006) Shrub establishment under experimental global changes in a California grassland. Plant Ecol 184:53–63. https://doi.org/10.1007/s11258-005-9051-x
Acknowledgements
We thank Steven Wohl, Vinod Kumar, Craig Barton, and Craig McNamara for maintaining the Western Sydney University Free Air CO2 Enrichment (EucFACE) facility, as well as several employees at Western Sydney University and volunteers who assisted with routine surveys of understorey vegetation plots and the experimental plantings. The EucFACE experiment is funded by the Australian Government, through the Education Investment Fund, the Department of Industry and Science and the Australian Research Council, and Western Sydney University. The growth and resprouting components of this research were funded by Australian Research Council Discovery Grant number DP130102576. Establishment and continued monitoring of the long-term vegetation plots was funded by the Hawkesbury Institute for the Environment, Western Sydney University. Victor Resco de Dios acknowledges funding from a Ramón y Cajal fellowship (RYC-2012-10970). Raul Ochoa Hueso acknowledges funding from a Juan de la Cierva-Incorporación fellowship (IJCI-2014-21252).
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This study was funded by the Australian Research Council (DP130102576) and the Hawkesbury Institute for the Environment, Western Sydney University.
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LC, MB, RB, VRD, and SP conceived the ideas and designed the experiment; LC, EB, SH, JP, and ROH collected the data; LC analysed the data; LC led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Communicated by Ines Ibanez.
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Collins, L., Boer, M.M., de Dios, V.R. et al. Effects of competition and herbivory over woody seedling growth in a temperate woodland trump the effects of elevated CO2. Oecologia 187, 811–823 (2018). https://doi.org/10.1007/s00442-018-4143-1
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DOI: https://doi.org/10.1007/s00442-018-4143-1