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Rapid Root Decomposition Decouples Root Length from Increased Soil C Following Grassland Invasion

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Abstract

Plant invasion often increases stand biomass, but higher tissue quality (for example, less lignin and more nutrients) in invasive species might accelerate litter decomposition. This mechanism may minimize increases in soil carbon (C) sequestration despite higher production. Our knowledge about invasion and tissue quality is based on shoots, but roots contribute 50–90% of biomass in vegetation types such as semiarid grasslands. Here we investigate root decomposition rates and tissue quality in the widespread invasive grass Agropyron cristatum, which doubles root mass but not soil C in the Great Plains of North America. Root length was significantly greater beneath Agropyron than native grassland 7 years after minirhizotron installation. However, CO2 evolution from decomposing roots was twice as much for Agropyron roots as for native grass roots (P < 0.05). CO2 evolution from decomposing native grass roots was not significantly different from controls with no root tissue added, suggesting that Agropyron invasion can convert grassland soil to a source of CO2 to the atmosphere. Rapid root decomposition was associated with significantly lower lignin content in Agropyron roots than native grass roots, although root N and lignin:N ratios did not differ. We present the first report of root decomposition rates associated with plant invasion. Increases in root length were accompanied by increased root decomposition rates of low-lignin tissue, such that invasion-driven enhanced productivity did not enhance soil C sequestration. Among-species differences in root tissue quality and decomposition rates could influence soil C dynamics during invasions of systems dominated by belowground production, such as tundra, boreal forests, and semiarid grassland.

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References

  • Balogianni VG, Wilson SD, Vaness BM, MacDougall AS, Pinno BD. 2014. Distinct root and shoot responses to mowing and fertility in native and invaded grassland. Rangel Ecol Manag 67:39–45.

    Article  Google Scholar 

  • Belnap J, Phillips SL. 2001. Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol Appl 11:1261–75.

    Article  Google Scholar 

  • Bilbrough CJ, Caldwell MM. 1995. The effects of shading and N status on root proliferation in nutrient patches by the perennial grass Agropyron desertorum in the field. Oecologia 103:10–16.

    Article  Google Scholar 

  • Bilbrough CJ, Caldwell MM. 1997. Exploitation of springtime ephemeral N pulses by six Great Basin plant species. Ecology 78:231–43.

    Google Scholar 

  • Bradford MA, Watts BW, Davies CA. 2009. Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Glob Chang Biol 16:1576–88.

    Article  Google Scholar 

  • Bronick CJ, Lal R. 2005. Soil structure and management: a review. Geoderma 124:3–22.

    Article  CAS  Google Scholar 

  • Carrillo Y, Dijkstra FA, LeCain D, Morgan JA, Blumenthal D, Waldron S, Pendall E. 2014. Disentangling root responses to climate change in a semiarid grassland. Oecologia 175:699.

    Article  PubMed  Google Scholar 

  • Carney KM, Hungate BA, Drake BG, Megonigal JP. 2007. Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci 104:4990–5.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Castro-Diez P, Godoy O, Alonso A, Gallardo A, Saldaña A. 2014. What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A meta-analysis. Ecol Lett 17:1–12.

    Article  CAS  PubMed  Google Scholar 

  • Chapin FSIII, Matson PA, Mooney HA. 2002. Principles of terrestrial ecosystem ecology. New York: Springer.

    Google Scholar 

  • Chapin FSIII, McFarland J, McGuire AD, Euskirchen ES, Ruess RW, Kielland K. 2009. The changing global carbon cycle: linking plant-soil carbon dynamics to global consequences. J Ecol 97:840–50.

    Article  CAS  Google Scholar 

  • Chen J, Stark JM. 2000. Plant species effects and carbon and nitrogen cycling in a sagebrush-crested wheatgrass soil. Soil Biol Biochem 32:47–57.

    Article  CAS  Google Scholar 

  • Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz 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. Ecol Lett 11:1065–71.

    Article  PubMed  Google Scholar 

  • 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? Glob Chang Biol 19:988–95.

    Article  PubMed  Google Scholar 

  • Crow SE, Lajtha K, Filley TR, Swanston CW, Bowden RD, Caldwell BA. 2009. Sources of plant-derived carbon and stability of organic matter in soil: implications for global change. Glob Chang Biol 15:2003–19.

    Article  Google Scholar 

  • Dalias P, Anderson JM, Bottner P, Coûteaux MM. 2001. Temperature responses of carbon mineralization in conifer forest soils from different regional climates incubated under standard laboratory conditions. Glob Chang Biol 7:181–92.

    Article  Google Scholar 

  • Dìaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Marti G, Grime JP, Zarrinkamar F, Asri Y. 2004. The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15:295–304.

    Article  Google Scholar 

  • Dijkstra FA, Hobbie SE, Reich PB. 2006. Soil processes affected by sixteen grassland species grown under different environmental conditions. Soil Sci Soc Am J 70:770–7.

    Article  CAS  Google Scholar 

  • Ehrenfeld JG. 2010. Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80.

    Article  Google Scholar 

  • Ehrenfeld JG. 2003. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–23.

    Article  CAS  Google Scholar 

  • Evans RD, Rimer R, Sperry L, Belnap J. 2001. Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11:1301–10.

    Article  Google Scholar 

  • Fierer N, Schimel JP. 2002. Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem 34:777–87.

    Article  CAS  Google Scholar 

  • Fierer N, Craine JM, McLauchlan K, Schimel JP. 2005. Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–6.

    Article  Google Scholar 

  • Foster BL, Kindscher K, Houseman GR, Murphy CA. 2009. Effects of hay management and native species sowing on grassland community structure, biomass, and restoration. Ecol Appl 19:1884–96.

    Article  PubMed  Google Scholar 

  • Freschet GT, Cornwell WK, Wardle DA, Elumeeva TG, Liu WD, Jackson BG, Onipchenko VG, Soudzilovskaia NA, Tao JP, Cornelissen JHC. 2013. Linking litter decomposition of above- and below-ground organs to plant-soil feedbacks worldwide. J Ecol 101:943–52.

    Article  CAS  Google Scholar 

  • Heidinga L, Wilson SD. 2002. The impact of an invading alien grass (Agropyron cristatum) on species turnover in native prairie. Divers Distrib 8:249–58.

    Article  Google Scholar 

  • Henderson DC, Naeth MA. 2005. Multi-scale impacts of crested wheatgrass invasion in mixed-grass prairie. Biol Invasions 7:639–50.

    Article  Google Scholar 

  • Hendricks JJ, Hendrick RL, Wilson CA, Mitchell RJ, Pecot SD, Guo DL. 2006. Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review. J Ecol 94:40–57.

    Article  Google Scholar 

  • Hendrickson JR, Wienhold BJ, Berdahl JD. 2001. Decomposition rates of native and improved cultivars of grasses in the Northern Great Plains. Arid Land Res Manag 15:347–57.

    Article  CAS  Google Scholar 

  • Hickman JE, Ashton IW, Howe KM, Lerdau MT. 2013. The native–invasive balance: implications for nutrient cycling in ecosystems. Oecologia 173:319–28.

    Article  PubMed  Google Scholar 

  • Hooker TD, Stark JM, Norton U, Leffler AJ, Peek M, Ryel R. 2008. Distribution of ecosystem C and N within contrasting vegetation types in a semiarid rangeland in the Great Basin, USA. Biogeochemistry 90:291–308.

    Article  CAS  Google Scholar 

  • Ivans CY, Leffler AJ, Spaulding U, Stark JM, Ryel RJ, Caldwell MM. 2003. Root responses and nitrogen acquisition by Artemisia tridentata and Agropyron desertorum following small summer rainfall events. Oecologia 134:317–24.

    Article  PubMed  Google Scholar 

  • Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED. 1996. A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411.

    Article  Google Scholar 

  • Jastrow JD, Miller RM. 1997. Soil aggregate stabilization and carbon sequestration: feedbacks through organomineral associations. In: Lal R, Kimble JM, Follett RF, Stewart BA, Eds. Soil processes and the carbon cycle. Boca Raton: CRC Press. p 207–23.

    Google Scholar 

  • Jobbágy EG, Jackson RB. 2000. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–36.

    Article  Google Scholar 

  • Johnson JMF, Barbour NW, Weyers SL. 2007. Chemical composition of crop biomass impacts its decomposition. Soil Sci Soc Am J 71:155–62.

    Article  CAS  Google Scholar 

  • Kitchen DJ, Blair JM, Callaham MA Jr. 2009. Annual fire and mowing alter biomass, depth distribution, and C and N content of roots and soil in tallgrass prairie. Plant Soil 323:235–47.

    Article  CAS  Google Scholar 

  • Köchy M, Wilson SD. 2001. Nitrogen deposition and forest expansion in the northern Great Plains. J Ecol 89:807–17.

    Article  Google Scholar 

  • Krzic M, Boersma K, Thompson DJ, Bomke AA. 2000. Soil properties and species diversity of grazed crested wheatgrass and native rangelands. J Range Manag 53:353–8.

    Article  Google Scholar 

  • Lee JS, Daniels BL, Eberiel DT, Farrell RE. 2000. Polymer mineralization in soils: effects of cold storage on microbial populations and biodegradation potential. J Polym Environ 8:81–9.

    Article  CAS  Google Scholar 

  • Lesica P, DeLuca T. 1996. Long-term harmful effects of crested wheatgrass on Great Plains grassland ecosystems. J Soil Water Conserv 51:408–9.

    Google Scholar 

  • Liao CZ, Peng RH, Luo YQ, Zhou XH, Wu XW, Fang CM, Chen JK, Li B. 2008. Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–14.

    Article  CAS  PubMed  Google Scholar 

  • Loya WM, Johnson LC, Nadelhoffer KJ. 2004. Seasonal dynamics of leaf-and root-derived C in arctic tundra mesocosms. Soil Biol Biochem 36:655–66.

    Article  CAS  Google Scholar 

  • Luyssaert S, Schulze ED, Borner A, Knohl A, Hessenmoller D, Law BE, Ciais P, Grace J. 2008. Old-growth forests as global carbon sinks. Nature 455:213–15.

    Article  CAS  PubMed  Google Scholar 

  • MacDougall AS, Wilson SD. 2011. The invasive grass Agropyron cristatum doubles belowground productivity but not soil carbon. Ecology 92:657–64.

    Article  PubMed  Google Scholar 

  • Maron JL, Auge H, Pearson DE, Korell L, Hensen I, Suding KN, Stein C. 2014. Staged invasions across disparate grasslands: effects of seed provenance, consumers and disturbance on productivity and species richness. Ecol Lett 17:499–507.

    Article  PubMed  Google Scholar 

  • Maron JL, Jeffries RL. 2001. Restoring enriched grasslands: Effects of mowing on species richness, productivity, and nitrogen retention. Ecol Appl 11:1088–100.

    Article  Google Scholar 

  • Meisner A, Hol WHG, de Boer W, Krumins JA, Wardle DA, van der Putten WH 2014. Plant–soil feedbacks of exotic plant species across life forms: a meta-analysis. Biol Invas 1–11 (in press).

  • Milchunas DG. 2009. Estimating root production: comparison of 11 methods in shortgrass steppe and review of biases. Ecosystems 12:1381–402.

    Article  CAS  Google Scholar 

  • Milleret R, Le Bayon RC, Gobat JM. 2009. Root, mycorrhiza and earthworm interactions: their effects on soil structuring processes, plant and soil nutrient concentration and plant biomass. Plant Soil 316:1–12.

    Article  CAS  Google Scholar 

  • Mokany K, Raison RJ, Prokushkin AS. 2006. Critical analysis of root: shoot ratios in terrestrial biomes. Glob Chang Biol 12:84–96.

    Article  Google Scholar 

  • Nave LE, Swanston CW, Mishra U, Nadelhoffer KJ. 2013. Afforestation effects on soil carbon storage in the United States: a synthesis. Soil Sci Soc Am J 77:1035–47.

    Article  CAS  Google Scholar 

  • Parton W, Silver WL, Burke IC, Grassens L, Harmon ME, Currie WS, King JY, Adair EC, Brandt LA, Hart SC, Fasth B. 2007. Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315:361–4.

    Article  CAS  PubMed  Google Scholar 

  • Peek MS, Leffler AJ, Ivans CY, Ryel RJ, Caldwell MM. 2005. Fine root distribution and persistence under field conditions of three co-occurring Great Basin species of different life form. New Phytol 165:171–80.

    Article  PubMed  Google Scholar 

  • Peltzer DA, Bellingham PJ, Kurokawa H, Walker LR, Wardle DA, Yeates GW. 2009. Punching above their weight: low-biomass non-native plant species alter soil properties during primary succession. Oikos 118:1001–14.

    Article  CAS  Google Scholar 

  • Quinn GP, Keough MJ. 2002. Experimental design and data analysis for biologists. New York: Cambridge University Press.

    Book  Google Scholar 

  • Richards JH. 1984. Root growth response to defoliation in two Agropyron bunchgrasses: field observations with an improved root periscope. Oecologia 64:21–5.

    Article  Google Scholar 

  • Saby NPA, Arrouays D, Antoni V, Lemercier B, Follain S, Walter C, Schvartz C. 2008. Changes in soil organic carbon in a mountainous French region, 1990–2004. Soil Use Manag 24:254–62.

    Article  Google Scholar 

  • Scott NA, Saggar S, McIntosh PD. 2001. Biogeochemical impact of Hieracium invasion in New Zealand’s grazed tussock grasslands: sustainability implications. Ecol Appl 11:1311–22.

    Article  Google Scholar 

  • Seabloom EW, Borer ET, Boucher VL, Burton RS, Cottingham KL, Goldwasser L, Gram WK, Kendall BE, Micheli F. 2003. Competition, seed limitation, disturbance, and reestablishment of California native annual forbs. Ecol Appl 13:575–92.

    Article  Google Scholar 

  • Shipley B, Lechowicz MJ, Wright I, Reich PB. 2006. Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87:535–41.

    Article  PubMed  Google Scholar 

  • Steinaker DF, Wilson SD. 2008a. Scale and density dependent relationships among roots, mycorrhizal fungi and collembola in grassland and forest. Oikos 117:703–10.

    Article  Google Scholar 

  • Steinaker DF, Wilson SD. 2008b. Phenology of fine roots and leaves in forest and grassland. J Ecol 96:1222–9.

    Article  Google Scholar 

  • Strand AE, Pritchard SG, McCormack ML, Davis MA, Oren R. 2008. Irreconcilable differences: fine-root life spans and soil carbon persistence. Science 319:456–8.

    Article  CAS  PubMed  Google Scholar 

  • Strickland MS, Devore JL, Maerz JC, Bradford MA. 2010. Grass invasion of a hardwood forest is associated with declines in belowground carbon pools. Glob Chang Biol 16:1338–50.

    Article  Google Scholar 

  • Tamura M, Tharayil N. 2014. Plant litter chemistry and microbial priming regulate the accrual, composition and stability of soil carbon in invaded ecosystems. New Phytol 203:110–24.

    Article  CAS  PubMed  Google Scholar 

  • Taylor BN, Beidler KV, Cooper ER, Strand AE, Pritchard SG. 2013. Sampling volume in root studies: the pitfalls of under-sampling exposed using accumulation curves. Ecol Lett 16:862–9.

    Article  PubMed  Google Scholar 

  • Throop HL, Archer SR. 2008. Shrub (Prosopis velutina) encroachment in a semidesert grassland: spatial–temporal changes in soil organic carbon and nitrogen pools. Glob Chang Biol 14:2420–31.

    Article  Google Scholar 

  • Vila M, Espinar JL, Hejda M, Hulme PE, Jarosik V, Maron JL, Pergl J, Schaffner U, Sun Y, Pysek P. 2011. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–8.

    Article  PubMed  Google Scholar 

  • Weidenhamer JD, Callaway RM. 2010. Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J Chem Ecol 36:59–69.

    Article  CAS  PubMed  Google Scholar 

  • Willms WD, Ellert BH, Janzen HH, Douwes H. 2005. Evaluation of native and introduced grasses for reclamation and production. Rangel Ecol Manag 58:177–83.

    Article  Google Scholar 

  • Wilson GW, Rice CW, Rillig MC, Springer A, Hartnett DC. 2009. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–61.

    Article  PubMed  Google Scholar 

  • Wilson SD, Pärtel M. 2003. Extirpation or coexistence? Management of a persistent introduced grass in a prairie restoration. Restor Ecol 11:410–16.

    Article  Google Scholar 

  • Zhang L, Wang H, Zou J, Rogers WE, Siemann E. 2014. Non-native plant litter enhances soil carbon dioxide emissions in an invaded annual grassland. Plos One 9:e92301.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ziter C, MacDougall AS. 2013. Nutrients and defoliation increase soil carbon inputs in grassland. Ecology 94:106–16.

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Medicine Lake National Wildlife Refuge for access and logistical support. We thank anonymous reviewers and S. Hobbie for helpful comments and the Natural Sciences and Engineering Research Council of Canada for funding.

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Authors and Affiliations

  1. Department of Biology, University of Regina, 3737 Wascana Parkway, Regina, Saskatchewan, S4S 0A2, Canada

    Vasiliki G. Balogianni & Scott D. Wilson

  2. Department of Soil Science, University of Saskatchewan, 5E18 - 51 Campus Drive, Saskatoon, Saskatchewan, S7N 5A8, Canada

    Richard E. Farrell

  3. Department of Integrated Biology, University of Guelph, 50 Stone Road East, Guelph, Ontario, N1G 2W1, Canada

    Andrew S. MacDougall

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  1. Vasiliki G. Balogianni
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  3. Richard E. Farrell
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Correspondence to Vasiliki G. Balogianni.

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Vasiliki G. Balogianni performed research, analyzed data, and contributed in conceiving and designing of the study and writing the paper. Scott D. Wilson contributed in conceiving and designing of the study and writing the paper. Richard E. Farrell contributed in new methods and Andrew S. MacDougall contributed in conceiving and designing of the study.

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Balogianni, V.G., Wilson, S.D., Farrell, R.E. et al. Rapid Root Decomposition Decouples Root Length from Increased Soil C Following Grassland Invasion. Ecosystems 18, 1307–1318 (2015). https://doi.org/10.1007/s10021-015-9900-y

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