Belowground impacts of perennial grass cultivation for sustainable biofuel feedstock production in the tropics

Abstract

Perennial grasses can sequester soil organic carbon (SOC) in sustainably managed biofuel systems, directly mitigating atmospheric CO₂ concentrations while simultaneously generating biomass for renewable energy. The objective of this study was to quantify SOC accumulation and identify the primary drivers of belowground C dynamics in a zero-tillage production system of tropical perennial C4 grasses grown for biofuel feedstock in Hawaii. Specifically, the quantity, quality, and fate of soil C inputs were determined for eight grass accessions – four varieties each of napier grass and guinea grass. Carbon fluxes (soil CO₂ efflux, aboveground net primary productivity, litterfall, total belowground carbon flux, root decay constant), C pools (SOC pool and root biomass), and C quality (root chemistry, C and nitrogen concentrations, and ratios) were measured through three harvest cycles following conversion of a fallow field to cultivated perennial grasses. A wide range of SOC accumulation occurred, with both significant species and accession effects. Aboveground biomass yield was greater, and root lignin concentration was lower for napier grass than guinea grass. Structural equation modeling revealed that root lignin concentration was the most important driver of SOC pool: varieties with low root lignin concentration, which was significantly related to rapid root decomposition, accumulated the greatest amount of SOC. Roots with low lignin concentration decomposed rapidly, but the residue and associated microbial biomass/by-products accumulated as SOC. In general, napier grass was better suited for promoting soil C sequestration in this system. Further, high-yielding varieties with low root lignin concentration provided the greatest climate change mitigation potential in a ratoon system. Understanding the factors affecting SOC accumulation and the net greenhouse gas trade-offs within a biofuel production system will aid in crop selection to meet multiple goals toward environmental and economic sustainability.

References Adair EC, Reich PB, Hobbie SE, Knops JMH (2009) Interactive effects of time, CO₂, N, and diversity on total belowground carbon allocation and ecosystem carbon storage in a grassland community. Ecosystems, 12, 1037–1052. Adler PR, Del Grosso SJ, Parton WJ (2007) Life-cycle assessment of net greenhouse-gas flux for bioenergy cropping systems. Ecological Applications, 17, 675–691. Agostini F, Gregory AS, Richter GM (2015) Carbon sequestration by perennial energy crops: is the jury still out? Bioenergy Research, 8, 1057–1080. Al-Kaisi MM, Grote JB (2007) Cropping systems effects on improving soil carbon stocks of exposed subsoil. Soil Science Society of America Journal, 71, 1381–1388. Anderson-Teixeira KJ, Davis SC, Masters MD, DeLucia EH (2009) Changes in soil organic carbon under biofuel crops. GCB Bioenergy, 1, 75–96. Anderson-Teixeira KJ, Snyder PK, Twin TE, Cuadra CV, Costa MH, DeLucia EH (2012) Climate-regulation services of natural and agricultural ecoregions of the Americas. Nature Climate Change, 2, 177–181. Anderson-Teixeira KJ, Masters MD, Black CK, Zeri M, Hussain MZ, Bernacchi CJ, DeLucia EH (2013) Altered belowground carbon cycling following land-use change to perennial bioenergy crops. Ecosystems, 16, 508–520. Bond-Lamberty B, Wang C, Gower ST (2004) A global relationship between the heterotrophic and autotrophic components of soil respiration? Global Change Biology, 10, 1756–1766. Brahim N, Blavet D, Gallali T, Bernoux M (2011) Application of structural equation modeling for assessing relationships between organic carbon and soil properties in semiarid Mediterranean region. International Journal of Environmental Science and Technology, 8, 305–320. Bremer DJ, Ham JM, Owensby CE, Knapp AK (1998) Responses of soil respiration to clipping and grazing in a tallgrass prairie. Journal of Environmental Quality, 27, 1539–1548. Cherubini F, Bird ND, Cowie A, Jungmeier G, Schlamadinger B, Woess-Gallasch S (2009) Energy- and greenhouse gas-based LCA of biofuel and bioenergy systems: key issues, ranges and recommendations. Resources, Conservation and Recycling, 53, 434–447. Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Global Change Biology, 19, 988–995. Cotrufo MF, Soong JL, Horton AJ, Campbell EE, Haddix ML, Wall DH, Parton WJ (2015) Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nature Geoscience, 8, 776–779. Dalal RC, Mayer RJ (1986) Long-term trends in fertility of soils under continuous cultivation and cereal. Cropping in southern Queensland. 2. Total organic carbon and its rate of loss from the soil profile. Australian Journal of Soil Research, 24, 281–292. Davidson E, Ackerman I (1993) Changes in soil carbon inventory following cultivation of previously untilled soils. Biogeochemistry, 20, 161–193. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature, 440, 165–173. Davis SC, Boddey RM, Alves BJR et al. (2013) Management swing potential for bioenergy crops. GCB Bioenergy, 5, 623–638. DeLucia EH (2016) How biofuels can cool our climate and strengthen our ecosystems. Eos, 97, 14–19. Dornbush M, Raich J (2006) Soil temperature, not aboveground plant productivity, best predicts intra-annual variations of soil respiration in central Iowa grasslands. Ecosystems, 9, 909–920. Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB (2012) Global change belowground: impacts of elevated CO₂, nitrogen, and summer drought on soil food webs and biodiversity. Global Change Biology, 18, 435–447. Ellert BH, Bettany JR (1995) Calculation of organic matter and nutrients stored in soils under contrasting management regimes. Canadian Journal of Soil Science, 75, 529–538. Ford CR, Mcgee J, Scandellari F, Hobbie EA, Mitchell RJ (2012) Long- and short-term precipitation effects on soil CO₂ efflux and total belowground carbon allocation. Agricultural and Forest Meteorology, 156, 54–64. Franzluebbers A (2012) Grass roots of soil carbon sequestration. Carbon Management, 3, 9–11. Gelfand I, Sahajpal R, Zhang X, Izaurralde RC, Gross KL, Robertson GP (2013) Sustainable bioenergy production from marginal lands in the US Midwest. Nature, 493, 514–517. Geng Y, Wang Y, Yang K et al. (2012) Soil respiration in Tibetan alpine grasslands: belowground biomass and soil moisture, but not soil temperature, best explain the large-scale patterns. PLoS One, 7, e34968. Giambelluca TW, Chen Q, Frazier AG et al. (2013) Online rainfall atlas of Hawai'i. Bulletin of the American Meteorology Society, 94, 313–316 (and online tool). Giardina CP, Ryan MG (2002) Total belowground carbon allocation in a fast-growing eucalyptus plantation estimated. Ecosystems, 5, 487–499. Gibbs HK, Johnston M, Foley JA, Holloway T, Monfreda C, Ramankutty N, Zaks D (2008) Carbon payback times for crop-based biofuel expansion in the tropics: the effects of changing yield and technology, Environmental Research Letters, 3, 034001. Gifford RM, Roderick ML (2003) Soil carbon stocks and bulk density: spatial or cumulative mass coordinates as a basis of expression? Global Change Biology, 9, 1507–1514. Gomez-Casanovas N, Anderson-Teixeira K, Zeri M, Bernacchi CJ, DeLucia EH (2013) Gap filling strategies and error in estimating annual soil respiration. Global Change Biology, 19, 1941-1952. Grace J (2006) Structural Equation Modeling and Natural Systems. Cambridge University Press, Cambridge. Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Science of the Total Environment, 404, 297–307. Hall MB (2003) Challenges with nonfiber carbohydrate methods. Journal of Animal Science, 81, 3226-3232. Hashimoto A, Arnold J, Ayars J et al. (2012) High-yield tropical biomass for advanced biofuels. Proceedings from Sun Grant National Conference: Science for Biomass Feedstock Production and Utilization, New Orleans, LA. Available at: www.sungrant.tennessee.edu/NatConference/ (accessed 23 June 2016). Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proceedings of the National Academy of Science, 103, 11206–11210. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical Journal, 50, 346–363. Hu LT, Bentler PM (1999) Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Structural Equation Modeling, 6, 1–55. Huang YH, Li YL, Xiao Y et al. (2011) Controls of litter quality on the carbon sink in soils through partitioning the products of decomposing litter in a forest succession series in South China. Forest Ecology and Management, 261, 1170–1177. Jastrow JD, Miller RM (1996) Soil aggregate stabilization and carbon sequestration: feedbacks through organomineral associations. In: Soil Processes and the Carbon Cycle (eds Lal R, Kimble J, Follett R, Stewart BA), pp. 207–223. CRC Press, Boca Raton. Johnson JMF, Barbour NW, Weyers SL (2007) Chemical composition of crop biomass impacts its decomposition. Soil Science Society of America Journal, 71, 155–162. Jonsson M, Wardle DA (2010) Structural equation modelling reveals plant-community drivers of carbon storage in boreal forest ecosystems. Biology Letters, 6, 116–119. Jöreskog KG, Sorbom D (1989) Lisrel 7. A Guide to the Program and Applications, 2nd edn. SPSS Inc., Chicago, IL. Keffer VI, Turn SQ, Kinoshita CM, Evans DE (2009) Ethanol technical potential in Hawaii based on sugarcane, banagrass, Eucalyptus, and Leucaena. Biomass and Bioenergy, 33, 247–254. Khanal SK, Surampalli RY, Zhang TC, Lamsal BP, Tyagi RD, Kao CM (eds.) (2010) Bioenergy and Biofuel from Biowastes and Biomass. American Society of Civil Engineers, Reston, VA. Kindler R, Siemens J, Kaiser K et al. (2011) Dissolved carbon leaching from soil is a crucial component of the net ecosystem carbon balance. Global Change Biology, 17, 1167–1185. Kinoshita C, Ishimura D, Jakeway L, Osgood R (1995) Production of Biomass for Electricity Generation on the Island of Oahu. Hawaii Natural Energy Institute, Honolulu, HI. Kuzyakov Y, Gavrichkova O (2010) Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Global Change Biology, 16, 3386–3406. Lal R (2013) Soil carbon management and climate change. Carbon Management, 4, 439–462. Lal R, Kimble JM (1997) Conservation tillage for carbon sequestration. Nutrient Cycling in Agroecosystems, 49, 243–253. Lehmann J (2012) Keeping carbon down. Carbon Management, 3, 21–22. Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature, 528, 60–68. Lemus R, Lal R (2005) Bioenergy crops and carbon sequestration. Critical Reviews in Plant Sciences, 24, 1–21. Lewandowski I (2013) Soil carbon and biofuels: multifunctionality of ecosystem services. In Ecosystem Services and Carbon Sequestration in the Biosphere (eds Lal R, Lorenz K, Huttl RF, Schneider BU, von Braun J), pp. 333–356. Springer, Dordrecht. Liebig MA, Schmer MR, Vogel KP, Mitchell RB (2008) Soil carbon storage by switchgrass grown for bioenergy. BioEnergy Research, 1, 215–222. Liska AJ, Perrin RK (2009) Indirect land use emission in the life cycle of biofuels: regulations vs. science. Biological Systems Engineering: Papers and Publications, Paper 144. Biofuels, Bioproducts and Biorefining, 3, 318–328. Litton CM, Ryan MG, Raich JW (2007) Carbon allocation in forest ecosystems. Global Change Biology, 13, 2089–2109. Litton CM, Cordell S, Sandquist DR (2008) A non-native invasive grass increases soil carbon flux in a Hawaiian tropical dry forest. Global Change Biology, 14, 726–739. Litton CM, Giardina CP, Albano JK, Long MS, Asner GP (2011) The magnitude and variability of soil-surface CO₂ efflux increase with mean annual temperature in Hawaiian tropical montane wet forests. Soil Biology & Biochemistry, 43, 2315–2323. Ma Z, Wood CW, Bransby DI (2000) Carbon dynamics subsequent to establishment of switchgrass. Biomass and Bioenergy, 18, 93–104. Matias L, Castro J, Zamora R (2012) Effect of simulated climate change on soil respiration in a Mediterranean-type ecosystem: rainfall and habitat type are more important than temperature or the soil carbon pool. Ecosystems, 15, 299–310. Meki MN, Kiniry JR, Behrman KD, Pawlowski MN, Crow SE (2014) The role of simulation models in monitoring soil organic carbon storage and greenhouse gas mitigation potential in bioenergy cropping systems. In: CO₂ Sequestration and Valorization (ed. Esteves V), InTech, Croatia. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology, 63, 621–626. Mochizuki J, Yanagida JF, Kumar D, Takara D, Murthy GF (2014). Life cycle assessment of ethanol production from tropical banagrass (Pennisetum purpureum) using green and dry processing technologies in Hawaii. Journal of Renewable Sustainable Energy, 6, 043128. Murphy BW (2014) Soil Organic Matter and Soil Function – Review of the Literature and Underlying Data. Department of the Environment, Canberra, Australia. Ontl TF, Cambardella CA, Schulte LA, Kolka RK (2015) Factors influencing soil aggregation and particulate organic matter responses to bioenergy crops across a topographic gradient. Geoderma, 255–256, 1–11. Ostertag R (2001) The effects of nitrogen and phosphorus availability on fine root dynamics in Hawaiian montane forests. Ecology, 82, 485–499. Powlson DS, Whitmore AP, Goulding WT (2011) Soil carbon sequestration to mitigate climate change: a critical re-examination to identify the true and the false. European Journal of Soil Science, 62, 42–55. Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry, 101, 133–149. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. Reynoso OR, Garay AH, Da Silva SC et al. (2009) Herbage accumulation, growth and structural characteristics of Mombasa grass (Panicum maximum Jacq.) harvested at different cutting intervals. Acumulación de forraje, crecimiento y características estructurales del pasto Mombaza (Panicum maximum Jacq.) cosechado a diferentes intervalos de corte, 47, 203–213. Richter GM, Agostini F, Redmile-Gordon M, White R, Goulding KWT (2015) Sequestration of C in soils under Miscanthus can be marginal and is affected by genotype-specific root distribution. Agriculture Ecosystems & Environment, 200, 169–177. Ryan MG, Binkley D, Fownes JH, Giardina CP, Senock RS (2004) An experimental test of the causes of forest growth decline with stand age. Ecological Monographs, 74, 393–414. Samson R, Mani S, Boddey R et al. (2005) The potential of C4 perennial grasses for developing a global BIOHEAT industry. Critical Reviews in Plant Sciences, 24, 461–495. Sanderson MA (2008) Upland switchgrass yield, nutritive value, and soil carbon changes under grazing and clipping. Agronomy Journal, 100, 510. Schmidt MWI, Torn MS, Abiven S et al. (2011) Persistence of soil organic matter as an ecosystem property. Nature, 478, 49–56. Seltman HJ (2012) Experimental design and analysis. Available at: http://www.stat.cmu.edu/~hseltman/309/Book/Book.pdf (accessed 1 November 2012). Silver W, Miya R (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia, 129, 407–419. Six J, Jastrow JD (2002) Organic matter turnover. In: Encyclopedia of Soil Science (ed. Lal R), pp. 936–942. Marcel Dekker, Boca Raton, FL. Six J, Elliott ET, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biology & Biochemistry, 32, 2099–2103. Sobel ME (1982) Asymptotic confidence intervals for indirect effects in structural equation models. In: Sociological Methodology (ed. Leinhardt S), pp. 290–312. American Sociological Association, Washington, DC. Stockmann U, Adams MA, Crawford JW et al. (2013) The knowns, known unknowns, and unknowns of sequestration of soil organic carbon. Agriculture, Ecosystems, and Environment, 164, 80–99. Sumiyoshi Y (2011) Belowground impact of napier and Guinea grasses grown for biofuel feedstock production. Master's Thesis submitted to the University of Hawaii Manoa. Tabachnick BG, Fidell LS (2007) Using Multivariate Statistics. Allyn and Bacon, Boston. Tiemann LK, Grandy AS (2015) Mechanisms of soil carbon accrual and storage in bioenergy cropping systems. GCB Bioenergy, 7, 161–174. Tilman D, Socolow R, Foley JA et al. (2009) Beneficial biofuels – the food, energy, and environment trilemma. Science, 325, 270–271. Tran N, Illukpitya P, Yanagida JF, Ogoshi R (2011) Optimizing biofuel production: an economic analysis for selected biofuel feedstock production in Hawaii. Journal of Biomass and Bioenergy, 35, 1756–1764. Tufekcioglu A, Raich JW, Isenhart TM, Schultz RC (2001) Soil respiration within riparian buffers and adjacent crop fields. Plant and Soil, 229, 117–124. Van Soest PJ (1963) Use of detergents in the analysis of fibrous feeds. II. A rapid method for the determination of fiber and lignin. Journal of the Association of Official Agricultural Chemists, 46, 829–835. Van Soest PJ, Wine RH (1968) The determination of lignin and cellulose in acid detergent fiber with permanganate. Journal of the Association of Official Agricultural Chemists, 51, 780–787. Virto I, Barré P, Burlot A, Chenu C (2012) Carbon input differences as the main factor explaining the variability in soil organic C storage in no-tilled compared to inversion tilled agrosystems. Biogeochemistry, 108, 17–26. Vivanco L, Austin A (2006) Intrinsic effects of species on leaf litter and root decomposition: a comparison of temperate grasses from North and South America. Oecologia, 150, 97–107. Werling BP, Dickson TL, Isaacs R et al. (2014) Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes. Proceedings of the National Academy of Sciences, 111, 1652–1657. Wider RK, Lang GE (1982) A critique of the analytical methods used in examining decomposition data obtained from litter bags. Ecology, 63, 1636–1642. Zhang D, Hui D, Luo Y, Zhou G (2008) Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. Journal of Plant Ecology, 1, 85–93.