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International Journal of Wildland Fire International Journal of Wildland Fire Society
Journal of the International Association of Wildland Fire
RESEARCH ARTICLE

Leaf flammability and fuel load increase under elevated CO2 levels in a model grassland

Anthony Manea A B , Saskia Grootemaat A and Michelle R. Leishman A
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia.

B Corresponding author. Email: anthony.manea@students.mq.edu.au

International Journal of Wildland Fire 24(6) 819-827 https://doi.org/10.1071/WF14201
Submitted: 6 November 2014  Accepted: 8 April 2015   Published: 18 May 2015

Abstract

Fire is a common process that shapes the structure of grasslands globally. Rising atmospheric CO2 concentration may have a profound influence on grassland fire regimes. In this study, we asked (1) does CO2 and soil P availability alter leaf flammability (ignitibility and fire sustainability); (2) are leaf tissue chemistry traits drivers of leaf flammability, and are they modified by CO2 and soil P availability?; (3) does CO2 and soil P availability alter fuel load accumulation in grasslands; and (4) does CO2 and soil P availability alter the resprouting ability of grassland species? We found that leaf flammability increased under elevated CO2 levels owing to decreased leaf moisture content and foliar N, whereas fuel load accumulation increased owing to decreased foliar N (slower decomposition rates) and increased aboveground biomass production. These plant responses to elevated CO2 levels were not modified by soil P availability. The increase in leaf flammability and fuel load accumulation under elevated CO2 levels may alter grassland fire regimes by facilitating fire ignition as well as shorter fire intervals. However, the increased root biomass of grasses under elevated CO2 levels may enhance their resprouting capacity relative to woody plants, resulting in a shift in the vegetation structure of grasslands.

Additional keywords: biomass production, climate change, fire ecology, ignitibility, leaf trait, litter decomposition, persistence, sustainability, woodland.


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 Phytologist 165, 351–372.
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.Crossref | GoogleScholarGoogle Scholar | 15720649PubMed |

Anderson HE (1970) Forest fuel ignitibility. Fire Technology 6, 312–319.
Forest fuel ignitibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXhsVent7g%3D&md5=defa65dc0f812daee680e7458da072fcCAS |

Anderson LJ, Derner JD, Polley WH, Gordon WS, Eissenstat DM, Jackson RB (2010) Root responses along a subambient to elevated CO2 gradient in a C3–C4 grassland. Global Change Biology 16, 454–468.
Root responses along a subambient to elevated CO2 gradient in a C3–C4 grassland.Crossref | GoogleScholarGoogle Scholar |

Billings SA, Zitzer SF, Weatherly H, Schaeffer SM, Charlet T, Arnone JA, Evans RD (2003) Effects of elevated carbon dioxide on green leaf tissue and leaf litter quality in an intact Mojave Desert ecosystem. Global Change Biology 9, 729–735.
Effects of elevated carbon dioxide on green leaf tissue and leaf litter quality in an intact Mojave Desert ecosystem.Crossref | GoogleScholarGoogle Scholar |

Bond WJ (2008) What limits trees in C4 grasslands and savannas? Annual Review of Ecology Evolution and Systematics 39, 641–659.
What limits trees in C4 grasslands and savannas?Crossref | GoogleScholarGoogle Scholar |

Bond WJ, Midgley GF (2012) Carbon dioxide and the uneasy interactions of trees and savannah grasses. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 601–612.
Carbon dioxide and the uneasy interactions of trees and savannah grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltV2rtbc%3D&md5=3d37e2476fe14887fbc83f2c0f880d05CAS | 22232770PubMed |

Bond WJ, Woodward FI, Midgley GF (2005) The global distribution of ecosystems in a world without fire. New Phytologist 165, 525–538.
The global distribution of ecosystems in a world without fire.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2Fpt1OktQ%3D%3D&md5=e841393c065742821621e1b15ab1c8a2CAS | 15720663PubMed |

Bowman DMJS, Balch JK, Artaxo P, Bond WJ, Carlson JM, Cochrane MA, D’Antonio CM, DeFries RS, Doyle JC, Harrison SP, Johnston FH, Keeley JE, Krawchuk MA, Kull CA, Marston JB, Moritz MA, Prentice IC, Roos CI, Scott AC, Swetnam TW, van der Werf GR, Pyne SJ (2009) Fire in the earth system. Science 324, 481–484.
Fire in the earth system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvVGmtb8%3D&md5=acf0f16875fe2576863ea8a4f6d043c7CAS |

Cary GJ, Bradstock RA, Gill AM, Williams RJ (2012) Global change and fire regimes in Australia. In ‘Flammable Australia: fire regimes, biodiversity and ecosystems in a changing world’. (Eds RA Bradstock, AM Gill, RJ Williams), pp. 149–170. (CSIRO Publishing: Melbourne)

Clarke PJ, Lawes MJ, Midgley JJ, Lamont BB, Ojeda F, Burrows GE, Enright NJ, Knox KJE (2013) Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. New Phytologist 197, 19–35.
Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s%2FptlGmsw%3D%3D&md5=d41be5aee6e7ef8a0ec89f9081346e69CAS | 23110592PubMed |

Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, Van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Díaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters 11, 1065–1071.
Plant species traits are the predominant control on litter decomposition rates within biomes worldwide.Crossref | GoogleScholarGoogle Scholar | 18627410PubMed |

Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biology 4, 43–54.
Elevated CO2 reduces the nitrogen concentration of plant tissues.Crossref | GoogleScholarGoogle Scholar |

Craine JM, Jackson RD (2010) Plant nitrogen and phosphorus limitation in 98 North American grassland soils. Plant and Soil 334, 73–84.
Plant nitrogen and phosphorus limitation in 98 North American grassland soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqur%2FM&md5=79065d16d48dfbb4d08da012dc4adf05CAS |

Curtis PS, Wang X (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113, 299–313.
A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology.Crossref | GoogleScholarGoogle Scholar |

De Lillis M, Bianco PM, Loreto F (2009) The influence of leaf water content and isoprenoids on flammability of some Mediterranean woody species. International Journal of Wildland Fire 18, 203–212.
The influence of leaf water content and isoprenoids on flammability of some Mediterranean woody species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvFOiur0%3D&md5=6d64a09aca5d0f6d57b27d1c1b1b228dCAS |

Dijkstra FA, Blumenthal D, Morgan JA, LeCain DR, Follett RF (2010) Elevated CO2 effects on semi-arid grassland plants in relation to water availability and competition. Functional Ecology 24, 1152–1161.
Elevated CO2 effects on semi-arid grassland plants in relation to water availability and competition.Crossref | GoogleScholarGoogle Scholar |

Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.
More efficient plants: a consequence of rising atmospheric CO2?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1eltbY%3D&md5=d825f7844d64a3c651fe9342060d8b24CAS | 15012276PubMed |

Duval B, Blankinship J, Dijkstra P, Hungate B (2012) CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: a meta-analysis. Plant Ecology 213, 505–521.
CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10, 1135–1142.
Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar | 17922835PubMed |

Engber EA, Varner JM (2012) Patterns of flammability of the California oaks: the role of leaf traits. Canadian Journal of Forest Research 42, 1965–1975.
Patterns of flammability of the California oaks: the role of leaf traits.Crossref | GoogleScholarGoogle Scholar |

Engber EA, Varner J, Arguello L, Sugihara NG (2011) The effects of conifer encroachment and overstorey structure on fuels and fire in an oak woodland landscape. Fire Ecology 7, 32–50.
The effects of conifer encroachment and overstorey structure on fuels and fire in an oak woodland landscape.Crossref | GoogleScholarGoogle Scholar |

Gifford R, Barrett D, Lutze J (2000) The effects of elevated [CO2] on the C : N and C : P mass ratios of plant tissues. Plant and Soil 224, 1–14.
The effects of elevated [CO2] on the C : N and C : P mass ratios of plant tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVejsb8%3D&md5=f41b312ca5eb0ee6b2735544a86b7df9CAS |

Gill AM, Moore PHR (1996) ‘Ignitability of leaves of Australian plants.’ (CSIRO: Canberra)

Gill AM, Zylstra P (2005) Flammability of Australian Forests. Australian Forestry 68, 87–93.
Flammability of Australian Forests.Crossref | GoogleScholarGoogle Scholar |

Grunzweig JM, Korner C (2003) Differential phosphorus and nitrogen effects drive species and community responses to elevated CO2 in semi-arid grassland. Functional Ecology 17, 766–777.
Differential phosphorus and nitrogen effects drive species and community responses to elevated CO2 in semi-arid grassland.Crossref | GoogleScholarGoogle Scholar |

Hall MC, Stiling P, Moon DC, Drake BG, Hunter MD (2005) Effects of elevated CO2 on foliar quality and herbivore damage in a scrub oak ecosystem. Journal of Chemical Ecology 31, 267–286.
Effects of elevated CO2 on foliar quality and herbivore damage in a scrub oak ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvF2qsL8%3D&md5=46df0be912ef2544af743cf85400087fCAS | 15856783PubMed |

Higgins SI, Scheiter S, Sankaran M (2010) The stability of African savannas: insights from the indirect estimation of the parameters of a dynamic model. Ecology 91, 1682–1692.
The stability of African savannas: insights from the indirect estimation of the parameters of a dynamic model.Crossref | GoogleScholarGoogle Scholar | 20583710PubMed |

Hill SJ, Tung PJ, Leishman MR (2005) Relationships between anthropogenic disturbance, soil properties and plant invasion in endangered Cumberland Plain Woodland, Australia. Austral Ecology 30, 775–788.
Relationships between anthropogenic disturbance, soil properties and plant invasion in endangered Cumberland Plain Woodland, Australia.Crossref | GoogleScholarGoogle Scholar |

Hoffmann WA, Bazzaz FA, Chatterton NJ, Harrison PA, Jackson RB (2000) Elevated CO2 enhances resprouting of a tropical savanna tree. Oecologia 123, 312–317.
Elevated CO2 enhances resprouting of a tropical savanna tree.Crossref | GoogleScholarGoogle Scholar |

Intergovernmental Panel on Climate Change (IPCC) (2011) Managing the risks of extreme events and disasters to advance climate change adaptation. In ‘Summary for policymakers’. (Eds CB Field, V Barros, TF Stocker, D Qin, D Dokken, KL Ebi, MD Mastrandrea, KJ Mach, G-K Plattner, SK Allen, M Tignor, PM Midgley) p. 3. (Cambridge University Press: Cambridge, MA).

IPCC (2013) Climate change 2013: a physical science basis. In ‘Working Group I Contribution to the IPCC Fifth Assessment Report’. (Eds S Joussaume, J Penner, F Tangang) p. 12. (Cambridge University Press: Cambridge, MA).

Keith DA (2012) Functional traits: their roles in understanding and predicting biotic responses to fire regimes from individuals to landscapes. In ‘Flammable Australia: fire regimes, biodiversity and ecosystems in a changing world’. (Eds RA Bradstock, AM Gill, RJ Williams), pp. 97–126. (CSIRO Publishing: Melbourne)

Knicker H, Hilscher A, Gonzalez-Vila FJ, Almendros G (2008) A new conceptual model for the structural properties of char produced during vegetation fires. Organic Geochemistry 39, 935–939.
A new conceptual model for the structural properties of char produced during vegetation fires.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFOltL4%3D&md5=04052c4e689dfd2bcc91560e01c9eea7CAS |

Knox KJE, Clarke PJ (2005) Nutrient availability induces contrasting allocation and starch formation in resprouting and obligate seeding shrubs. Functional Ecology 19, 690–698.
Nutrient availability induces contrasting allocation and starch formation in resprouting and obligate seeding shrubs.Crossref | GoogleScholarGoogle Scholar |

Lawes M, Clarke P (2011) Ecology of plant resprouting: populations to community responses in fire-prone ecosystems. Plant Ecology 212, 1937–1943.
Ecology of plant resprouting: populations to community responses in fire-prone ecosystems.Crossref | GoogleScholarGoogle Scholar |

Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Annals of Botany 89, 871–885.
Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVeitLk%3D&md5=ef7af27cee9ca65f30876ef90cfba62eCAS | 12102513PubMed |

Leakey A, Ainsworth E, Bernacchi C, Rogers A, Long S, Ort D (2009) Elevated CO2 effects on plant carbon, nitrogen and water relations: six important lessons from FACE. Journal of Experimental Botany 60, 2859–2876.
Elevated CO2 effects on plant carbon, nitrogen and water relations: six important lessons from FACE.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFWjtLc%3D&md5=f003753351152472c6221291bff902a2CAS | 19401412PubMed |

LeCain DR, Morgan JA, Milchunas DG, Mosier AR, Nelson JA, Smith DP (2006) Root biomass of individual species, and root size characteristics after five years of CO2 enrichment on native shortgrass steppe. Plant and Soil 279, 219–228.
Root biomass of individual species, and root size characteristics after five years of CO2 enrichment on native shortgrass steppe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsVaqsr4%3D&md5=43de9b938268194baa49685244aaaa0cCAS |

Leigh A, Sevanto S, Ball MC, Close JD, Ellsworth DS, Knight CA, Nicotra AB, Vogel S (2012) Do thick leaves avoid thermal damage in critically low wind speeds? New Phytologist 194, 477–487.
Do thick leaves avoid thermal damage in critically low wind speeds?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vhslagtQ%3D%3D&md5=ae26ee1814435412b62d3051002f979aCAS | 22296328PubMed |

Lenihan J, Bachelet D, Neilson R, Drapek R (2008) Response of vegetation distribution, ecosystem productivity, and fire to climate change scenarios for California. Climatic Change 87, 215–230.
Response of vegetation distribution, ecosystem productivity, and fire to climate change scenarios for California.Crossref | GoogleScholarGoogle Scholar |

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 ‘Flammable Australia: fire regimes, biodiversity and ecosystems in a changing world’. (Eds RA Bradstock, AM Gill and RJ Williams), pp. 253–270. (CSIRO Publishing: Melbourne)

Morgan JA, LeCain DR, Mosier AR, Milchunas DG (2001) Elevated CO2 enhances water relations and productivity and affects gas exchange in C3 and C4 grasses of the Colorado shortgrass steppe. Global Change Biology 7, 451–466.
Elevated CO2 enhances water relations and productivity and affects gas exchange in C3 and C4 grasses of the Colorado shortgrass steppe.Crossref | GoogleScholarGoogle Scholar |

Murray BR, Hardstaff LK, Phillips ML (2013) Differences in leaf flammability, leaf traits and flammability – trait relationships between native and exotic plant species of dry sclerophyll forest. PLoS One 8, e79205
Differences in leaf flammability, leaf traits and flammability – trait relationships between native and exotic plant species of dry sclerophyll forest.Crossref | GoogleScholarGoogle Scholar | 24260169PubMed |

Pausas JG, Ribeiro E (2013) The global fire–productivity relationship. Global Ecology and Biogeography 22, 728–736.
The global fire–productivity relationship.Crossref | GoogleScholarGoogle Scholar |

Pickett BM, Isackson C, Wunder R, Fletcher TH, Butler BW, Weise DR (2009) Flame interactions and burning characteristics of two live leaf samples. International Journal of Wildland Fire 18, 865–874.
Flame interactions and burning characteristics of two live leaf samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlWht7fN&md5=c7b9f43ec8f42b27d8fab0e82f773471CAS |

Ross DJ, Tate KR, Newton PCD, Clark H (2002) Decomposability of C3 and C4 grass litter sampled under different concentrations of atmospheric carbon dioxide at a natural CO2 spring. Plant and Soil 240, 275–286.
Decomposability of C3 and C4 grass litter sampled under different concentrations of atmospheric carbon dioxide at a natural CO2 spring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlOmsr0%3D&md5=a5b8fc7b0771f1d502381cbfbcd6594bCAS |

Scarff FR, Westoby M (2006) Leaf litter flammability in some semi-arid Australian woodlands. Functional Ecology 20, 745–752.
Leaf litter flammability in some semi-arid Australian woodlands.Crossref | GoogleScholarGoogle Scholar |

Scarff FR, Westoby M (2008) The influence of tissue phosphate on plant flammability: a kinetic study. Polymer Degradation & Stability 93, 1930–1934.
The influence of tissue phosphate on plant flammability: a kinetic study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtF2kurvP&md5=08dae240e2302454331dda14f8449103CAS |

Scarff FR, Gray BF, Westoby M (2012) Exploring phosphate effects on leaf flammability using a physical chemistry model. International Journal of Wildland Fire 21, 1042–1051.
Exploring phosphate effects on leaf flammability using a physical chemistry model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKrsbbF&md5=13bd218cdc0390a0ff2276729740604eCAS |

Schwilk DW, Caprio AC (2011) Scaling from leaf traits to fire behaviour: community composition predicts fire severity in a temperate forest. Journal of Ecology 99, 970–980.
Scaling from leaf traits to fire behaviour: community composition predicts fire severity in a temperate forest.Crossref | GoogleScholarGoogle Scholar |

Shaw MR, Zavaleta ES, Chiariello NR, Cleland EE, Mooney HA, Field CB (2002) Grassland responses to global environmental changes suppressed by elevated CO2. Science 298, 1987–1990.
Grassland responses to global environmental changes suppressed by elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1WisLo%3D&md5=3892dd83b271d0cd7f9d62f580faa2c4CAS | 12471257PubMed |

Stocklin J, Schweizer K, Korner C (1998) Effects of elevated CO2 and phosphorus addition on productivity and community composition of intact monoliths from calcareous grassland. Oecologia 116, 50–56.
Effects of elevated CO2 and phosphorus addition on productivity and community composition of intact monoliths from calcareous grassland.Crossref | GoogleScholarGoogle Scholar |

Taylor BR, Parkinson D, Parsons WFJ (1989) Nitrogen and lignin content as predictors of litter decay rates: a microcosm test. Ecology 70, 97–104.
Nitrogen and lignin content as predictors of litter decay rates: a microcosm test.Crossref | GoogleScholarGoogle Scholar |

Tissue DT, Lewis JD (2010) Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO2] vary with phosphorus supply. Tree Physiology 30, 1361–1372.
Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO2] vary with phosphorus supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFygsrjI&md5=6a4719543f0a4f1c05edce9408f8d7acCAS | 20884610PubMed |

Tooth IM, Leishman MR (2013) Post-fire resprouting responses of native and exotic grasses from Cumberland Plain Woodland (Sydney, Australia) under elevated carbon dioxide. Austral Ecology 38, 1–10.
Post-fire resprouting responses of native and exotic grasses from Cumberland Plain Woodland (Sydney, Australia) under elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar |

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. Biological Invasions 16, 257–268.
Elevated carbon dioxide and fire reduce biomass of native grass species when grown in competition with invasive exotic grasses in a savanna experimental system.Crossref | GoogleScholarGoogle Scholar |

Vitousek PM (1998) Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems 1, 401–407.
Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptFensg%3D%3D&md5=4259d8b185541dfbef6697f9a72697d4CAS |

Ward JK, Strain BR (1999) Elevated CO2 studies: past, present and future. Tree Physiology 19, 211–220.
Elevated CO2 studies: past, present and future.Crossref | GoogleScholarGoogle Scholar | 12651563PubMed |

Wardle DA, Bonner KI, Barker GM (2002) Linkages between plant litter decomposition, litter quality, and vegetation responses to herbivores. Functional Ecology 16, 585–595.
Linkages between plant litter decomposition, litter quality, and vegetation responses to herbivores.Crossref | GoogleScholarGoogle Scholar |