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Legacy effects overwhelm the short-term effects of exotic plant invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling

  • Community ecology - Original Paper
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Abstract

Plant invasions can have substantial consequences for the soil ecosystem, altering microbial community structure and nutrient cycling. However, relatively little is known about what drives these changes, making it difficult to predict the effects of future invasions. In addition, because most studies compare soils from uninvaded areas to long-established dense invasions, little is known about the temporal dependence of invasion impacts. We experimentally manipulated forest understory vegetation in replicated sites dominated either by exotic Japanese barberry (Berberis thunbergii), native Viburnums, or native Vacciniums, so that each vegetation type was present in each site-type. We compared the short-term effect of vegetation changes to the lingering legacy effects of the previous vegetation type by measuring soil microbial community structure (phospholipid fatty acids) and function (extracellular enzymes and nitrogen mineralization). We also replaced the aboveground litter in half of each plot with an inert substitute to determine if changes in the soil microbial community were driven by aboveground or belowground plant inputs. We found that after 2 years, the microbial community structure and function was largely determined by the legacy effect of the previous vegetation type, and was not affected by the current vegetation. Aboveground litter removal had only weak effects, suggesting that changes in the soil microbial community and nutrient cycling were driven largely by belowground processes. These results suggest that changes in the soil following either invasion or restoration do not occur quickly, but rather exhibit long-lasting legacy effects from previous belowground plant inputs.

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References

  • Brant JB, Myrold DD, Sulzman EW (2006) Root controls on soil microbial community structure in forest soils. Oecologia 148:650–659

    Article  PubMed  Google Scholar 

  • Chapman S, Langley J, Hart SC, Koch G (2006) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169:27–34

    Article  PubMed  CAS  Google Scholar 

  • Coleman HM, Levine JM (2007) Mechanisms underlying the impacts of exotic annual grasses in a coastal California meadow. Biol Invasions 9:65–71

    Article  Google Scholar 

  • Congdon P (2001) Bayesian statistical modelling. Wiley, Chichester

    Google Scholar 

  • Cressie N, Calder CA, Clark JS, Ver Hoef JM, Wikle CK (2009) Accounting for uncertainty in ecological analysis: the strengths and limitations of hierarchical statistical modeling. Ecol Appl 19:553–570

    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 15:2003–2019

    Article  Google Scholar 

  • Dambrine E, Dupouey J-L, Laüt L, Humbert L, Thinon N, Beaufils T, Richard H (2007) Present forest biodiversity patterns in France related to former Roman agriculture. Ecology 88:1430–1439

    Article  PubMed  CAS  Google Scholar 

  • DeGasperis BG, Motzkin G (2007) Windows of opportunity: historical and ecological controls on Berberis thunbergii invasions. Ecology 88:3115–3125

    Article  PubMed  Google Scholar 

  • Ehrenfeld J (1999) Structure and dynamics of populations of Japanese barberry (Berberis thunbergii DC.) in deciduous forests of New Jersey. Biol Invasions 1:203–213

    Article  Google Scholar 

  • Ehrenfeld J (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523

    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, Parsons W, Han X, Parmelee R, Zhu W (1997) Live and dead roots in forest soil horizons: contrasting effects on nitrogen dynamics. Ecology 78:348–362

    Google Scholar 

  • Ehrenfeld J, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300

    Article  Google Scholar 

  • Fahey TJ, Siccama TG, Driscoll CT, Likens GE, Campbell J, Johnson CE, Battles JJ, Aber JD, Cole JJ, Fisk MC, Groffman PM, Hamburg SP, Holmes RT, Schwarz PA, Yanai RD (2005) The biogeochemistry of carbon at Hubbard Brook. Biogeochem 75:109–176

    Article  CAS  Google Scholar 

  • Farrer EC, Goldberg DE (2009) Litter drives ecosystem and plant community changes in cattail invasion. Ecol Appl 19:398–412

    Article  PubMed  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    Article  PubMed  CAS  Google Scholar 

  • Flory SL, Clay K (2006) Invasive shrub distribution varies with distance to roads and stand age in eastern deciduous forests in Indiana, USA. Plant Ecol 184:131–141

    Article  Google Scholar 

  • Hannam KD, Quideau SA, Kishchuck BE (2007) The microbial communities of aspen and spruce forest floors are resistant to changes in litter inputs and microclimate. Appl Soil Ecol 35:635–647

    Article  Google Scholar 

  • Hart SC, Sollins P (1998) Soil carbon and nitrogen pools and processes in an old-growth conifer forest 13 years after trenching. Can J For Res 28:1261–1265

    Article  Google Scholar 

  • Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522

    Article  Google Scholar 

  • Hobbie SE, Oleksyn J, Eissenstat DM, Reich PB (2010) Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia 162:505–513

    Article  PubMed  Google Scholar 

  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

    Article  PubMed  Google Scholar 

  • Holub SM, Lajtha K, Spears JDH, Tóth JA, Crow SE, Caldwell BA, Papp M, Nagy PT (2005) Organic matter manipulations have little effect on gross and net nitrogen transformations in two temperate forest mineral soils in the USA and central Europe. For Ecol Manage 214:320–330

    Article  Google Scholar 

  • Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–2991

    Article  CAS  Google Scholar 

  • Keith AM, Brooker RW, Osler GHR, Chapman SJ, Burslem DFRP, Van Der Wal R (2009) Strong impacts of belowground tree inputs on soil nematode trophic composition. Soil Biol Biochem 41:1060–1065

    Article  CAS  Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Huang WZ (1998) Effects of exotic plant species on soil properties in hardwood forests of New Jersey. Water Air Soil Pollut 105:493–501

    Article  CAS  Google Scholar 

  • Kourtev P, Ehrenfeld J, Huang W (2002) Enzyme activities during litter decomposition of two exotic and two native plant species in hardwood forests of New Jersey. Soil Biol Biochem 34:1207–1218

    Article  CAS  Google Scholar 

  • Kourtev P, Ehrenfeld J, Häggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905

    Article  CAS  Google Scholar 

  • Kulmatiski A, Beard KH, Stark JM (2006) Soil history as a primary control on plant invasion in abandoned agricultural fields. J Appl Ecol 43:868–876

    Article  Google Scholar 

  • Lajtha K, Crow SE, Yano Y, Kaushal SS, Sulzman E, Sollins P, Spears JDH (2005) Detrital controls on soil solution N and dissolved organic matter in soils: a field experiment. Biogeochem 76:261–281

    Article  CAS  Google Scholar 

  • Lauber C, Strickland MS, Bradfored MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415

    Article  CAS  Google Scholar 

  • Liao CZ, Luo YQ, Fang CM, Chen JK, Li B (2008) Litter pool sizes, decomposition, and nitrogen dynamics in Spartina alterniflora-invaded and native coastal marshlands of the Yangtze Estuary. Oecologia 156:589–600

    Article  PubMed  Google Scholar 

  • Lunn DJ, Best TA, Spiegelhalter D (2000) WinBUGS—a Bayesian modeling framework: concepts, structure, and extensibility. Stat Comput 10:325–337

    Article  Google Scholar 

  • Mosher ES, Silander J, Latimer AM (2009) The role of land-use history in major invasions by woody plant species in the northeastern North American landscape. Biol Invasions 11:2317–2328

    Article  Google Scholar 

  • Nilsson MC, Wardle DA, DeLuca TH (2008) Belowground and aboveground consequences of interactions between live plant species mixtures and dead organic substrate mixtures. Oikos 117:439–449

    Article  Google Scholar 

  • O’Donnell AG, Colvan SR, Malosso E, Supaphol S (2005) Twenty years of molecular analysis of bacterial communities in soils and what have we learned about function? In: Bardgett RD, Usher MB, Hopkins DW (eds) Biological diversity and function in soils. Cambridge University Press, Cambridge, pp 44–56

    Chapter  Google Scholar 

  • Olsson P (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310

    Article  CAS  Google Scholar 

  • Parks CG, Radosevich SR, Endress BA, Naylor BJ, Anzinger D, Rew LJ, Maxwell BD, Dwire KA (2005) Natural and land-use history of the Northwest mountain ecoregions (USA) in relation to patterns of plant invasions. Perspect Plant Ecol Evol Syst 7:137–158

    Article  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Plue J, Hermy M, Verheyen K, Thuillier P, Saguez R, Decocq G (2008) Persistent changes in forest vegetation and seed bank 1,600 years after human occupation. Landscape Ecol 23:673–688

    Article  Google Scholar 

  • Plummer M, Best N, Cowles K, Vines K (2009) coda: output analysis and diagnostics for MCMC. R package version 0:13–14

    Google Scholar 

  • Pollierer MM, Langel R, Körner C, Maraun M, Scheu S (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736

    Article  PubMed  Google Scholar 

  • R Development Core Team (2009). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, http://www.R-project.org

  • Sax DF, Stachowicz JJ, Gaines S (2005) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland

  • Sayer EJ, Tanner EVJ, Cheesman AW (2006) Increased litterfall changes fine root distribution in a moist tropical forest. Plant Soil 281:5–13

    Article  CAS  Google Scholar 

  • Siira-Pietikäinen A, Haimi J, Kanninen A, Pietikäinen J, Fritze H (2001) Response of decomposer community to root-isolation and addition of slash. Soil Biol Biochem 33:1993–2004

    Article  Google Scholar 

  • Silander J, Klepeis D (1999) The invasion ecology of Japanese barberry (Berberis thunbergii) in the New England landscape. Biol Invasions 1:189–201

    Article  Google Scholar 

  • Sinsabaugh RL, Reynolds H, Long TM (2000) Rapid assay for amidohydrolase (urease) activity in environmental samples. Soil Biol Biochem 32:2095–2097

    Article  CAS  Google Scholar 

  • Sinsabaugh RL et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    PubMed  Google Scholar 

  • Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A (2002) Bayesian measures of model complexity and fit. J R Stat Soc Series B Stat Methodol 64:583–639

    Article  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451

    Article  PubMed  Google Scholar 

  • Sturtz S, Ligges U, Gelman A (2005) R2WinBUGS: a package for running WinBUGS from R. J Stat Softw 12:1–16

    Google Scholar 

  • Subke J, Hahn V, Battipaglia G, Linder S, Buchmann N, Cotrufo MF (2004) Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia 139:551–559

    Article  PubMed  Google Scholar 

  • Uselman SM, Qualls RG, Lilienfein J (2009) Production of total potentially soluble organic C, N, and P across an ecosystem chronosequence: root versus leaf litter. Ecosystems 12:240–260

    Article  CAS  Google Scholar 

  • van der Putten WH, Kowalchuck GA, Brinkman EP, Doodeman GTA, van der Kaaij RM, Kamp AFD, Menting FBJ, Veenendaal EM (2007) Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecology 88:978–988

    Article  PubMed  Google Scholar 

  • van der Putten WH, Bardgett RD, De Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schädler M, Scherber C, Strauss SY, Vos M, Wardle DA (2009) Empirical and theoretical challenges in aboveground-belowground ecology. Oecologia 161:1–14

    Article  PubMed  Google Scholar 

  • Vilà M, Basnou C, Pysek P, Josefsson M, Genovesi P, Gollash S, Nentwig W, Olenin S, Roques A, Roy D, Hulme PE, DAISIE partners (2010) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front Ecol Environ 8:135–144

    Article  Google Scholar 

  • Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846

    Article  CAS  Google Scholar 

  • Weintraub MN, Scott-Denton LE, Schmidt SK, Monson RK (2007) The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem. Oecologia 154:327–338

    Article  PubMed  Google Scholar 

  • White DC, Ringelberg DB (1998) Signature lipid biomarker analysis. In: Burlage RS, Atlas R, Stahl D, Geesey G, Sayler G (eds) Techniques in microbial ecology. Oxford University Press, Oxford, p 468

  • White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62

    Article  Google Scholar 

  • Withington JM, Reich PB, Oleksyn J, Eissenstat DM (2006) Comparisons of structure and life span in roots and leaves among temperate trees. Ecol Monogr 76:381–397

    Article  Google Scholar 

  • Yokomizo H, Possingham HP, Thomas MB, Buckley YM (2009) Managing the impact of invasive species: the value of knowing the density-impact curve. Ecol Appl 19:376–386

    Article  PubMed  Google Scholar 

  • Zeller M, Liu J, Buchmann N, Richter A (2008) Tree girdling increases soil N mineralisation in two spruce stands. Soil Biol Biochem 40:1155–1166

    Article  CAS  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

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Acknowledgments

We wish to thank Jodi Messina, Michael Murillo, and Dr. Max Häggblom for lab and field help. Ed Green provided essential help with statistics. We thank Ai Wen, Monica Palta, Laura Shappell, Brian Clough, and two anonymous reviewers for helpful comments that improved the manuscript. Funding was provided by a National Science Foundation Graduate Research Fellowship to K.J.E. and a National Science Foundation Grant to J.G.E. (NSF DEB-0309047). All experiments comply with the current laws of the country in which the experiments were performed.

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The authors declare that they have no conflict of interest.

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Correspondence to Kenneth J. Elgersma.

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Communicated by Melinda Smith.

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Elgersma, K.J., Ehrenfeld, J.G., Yu, S. et al. Legacy effects overwhelm the short-term effects of exotic plant invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling. Oecologia 167, 733–745 (2011). https://doi.org/10.1007/s00442-011-2022-0

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