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Soil recovery after removal of the N2-fixing invasive Acacia longifolia: consequences for ecosystem restoration

Abstract

Invasion by Acacia longifolia alters soil characteristics and processes. The present study was conducted to determine if the changes in soil C and N pools and processes induced by A. longifolia persist after its removal, at the São Jacinto Dunes Nature Reserve (Portugal). Some areas had been invaded for a long time (>20 years) and others more recently (<10 years). For each type of invasion, (i.e., long-invaded and recently invaded), three treatments were used: (1) A. longifolia left intact; (2) A. longifolia was removed; and (3) both A. longifolia and litter layer were removed. Soil samples were collected once a year for four and half years and analysed for chemical and microbial properties. In general, microbial parameters responded faster than C and N pools. In long-invaded areas, two and half years after removal of plants and litter, basal respiration and microbial biomass had already decreased >30%, β-glucosaminidase activity (N mineralization index) >60% and potential nitrification >95%. Removal of plants and litter resulted in a >35% decrease in C and N content after four and half years. In recently invaded areas, β-glucosaminidase activity and potential nitrification showed a marked decrease (>54% and >95%, respectively) after removal of both A. longifolia and litter. Our results suggest that after removal of an N2-fixing invasive tree that changes ecosystem-level processes, it takes several years before soil nutrients and processes return to pre-invasion levels, but this legacy slowly diminish, suggesting that the susceptibility of native areas to (re)invasion is a function of the time elapsed since removal. Removal of the N-rich litter layer facilitates ecosystem recovery.

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Abbreviations

LI:

Areas long-invaded by A. longifolia (>20 years)

LIA:

Areas long-invaded where A. longifolia was left intact

LIAR:

Areas long-invaded where only A. longifolia was removed

LIALR:

Areas long-invaded where both A. longifolia and the litter layer were removed

RI:

Areas recently invaded by A. longifolia (<10 years)

RIA:

Areas recently invaded where A. longifolia was left intact

RIAR:

Areas recently invaded where only A. longifolia was removed

RIALR:

Areas recently invaded where both A. longifolia and the litter layer were removed

References

  • Aaronson S (1970) Experimental microbial ecology. Academic Press, New York, p 236

    Google Scholar 

  • Allison M, Ausden M (2006) Effects of removing the litter and humic layers on heathland establishment following plantation removal. Biol Conserv 127:177–182. doi:10.1016/j.biocon.2005.08.008

    Article  Google Scholar 

  • Alpert P, Maron JL (2000) Carbon addition as a countermeasure against biological invasion by plants. Biol Invasions 2:33–40. doi:10.1023/A:1010063611473

    Article  Google Scholar 

  • Alves JMS, Santo MDE, Costa JC, Gonçalves JHC, Lousã MF (1998) Habitats Naturais e Seminaturais de Portugal Continental. Instituto da Conservação da Natureza, Lisbon Portugal, 55 pp

  • Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221. doi:10.1016/0038-0717(78)90099-8

    Article  CAS  Google Scholar 

  • Andersson M, Kjøller A, Struwe S (2004) Microbial enzyme activities in leaf litter, humus and mineral soil layers of European forests. Soil Biol Biochem 36:1527–1537. doi:10.1016/j.soilbio.2004.07.018

    Article  CAS  Google Scholar 

  • Blumenthal D (2005) Interrelated causes of plant invasion. Science 310:243–244. doi:10.1126/science.1114851

    PubMed  Article  CAS  Google Scholar 

  • Blumenthal DM, Jordan NR, Russelle MP (2003) Soil carbon addition controls weeds and facilitates prairie restoration. Ecol Appl 13:605–615. doi:10.1890/1051-0761(2003)013[0605:SCACWA]2.0.CO;2

    Article  Google Scholar 

  • Bremner JM (1965) Total nitrogen. In: Black CA (ed) Methods of soil analysis. Part 2: chemical and microbiological properties. American Society of Agronomy, Inc. Publisher, Madison USA, pp 1149–1176

    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. doi:10.1007/s10530-006-9008-6

    Article  Google Scholar 

  • Corbin JD, D’Antonio CM (2004) Effects of exotic species on soil nitrogen cycling: implications for restoration. Weed Technol 18:1464–1467

    Article  CAS  Google Scholar 

  • D’Antonio C, Meyerson LA (2002) Exotic plant species as problems and solutions in ecological restoration: a synthesis. Restor Ecol 10:703–713. doi:10.1046/j.1526-100X.2002.01051.x

    Article  Google Scholar 

  • Davis MA, Pelsor M (2001) Experimental support for a resource-based mechanistic model of invasibility. Ecol Lett 4:421–428. doi:10.1046/j.1461-0248.2001.00246.x

    Article  Google Scholar 

  • Echeverría SR, Crisóstomo JA, Nabais C, Freitas H (2008) Belowground mutualists and the invasive ability of Acacia longifolia in coastal dunes of Portugal. Biol Invasions. doi:10.1007/s10530-008-9280-8

    Google Scholar 

  • Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems (N Y, Print) 6:503–523. doi:10.1007/s10021-002-0151-3

    Article  CAS  Google Scholar 

  • Ekenler M, Tabatabai MA (2004) β-glucosaminidase activity as an index of nitrogen mineralization in soils. Commun Soil Sci Plann 35:1081–1094. doi:10.1081/CSS-120030588

    Article  CAS  Google Scholar 

  • Gordon DR (1998) Effects of invasive, non-indigenous plant species on ecosystem processes: lessons from Florida. Ecol Appl 8:975–989. doi:10.1890/1051-0761(1998)008[0975:EOINIP]2.0.CO;2

    Article  Google Scholar 

  • Gross KL, Mittelbach GG, Reynolds HL (2005) Grassland invasibility and diversity: responses to nutrients, seed input, and disturbance. Ecology 86:476–486. doi:10.1890/04-0122

    Article  Google Scholar 

  • Haubensak KA, D’Antonio CM, Alexander J (2004) Effects of nitrogen-fixing shrubs in Washington and coastal California. Weed Technol 18:1475–1479

    Article  Google Scholar 

  • Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985. doi:10.1111/j.1461-0248.2005.00802.x

    Article  Google Scholar 

  • Heneghan L, Fatemi F, Umek L, Grady K, Fagen K, Workman M (2006) The invasive shrub European buckthorn (Rhamnus cathartica L.) alters soil properties in Midwestern US woodlands. Appl Soil Ecol 32:142–148. doi:10.1016/j.apsoil.2005.03.009

    Article  Google Scholar 

  • Hobbs RJ, Humphries SE (1995) An integrated approach to the ecology and management of plant invasions. Conserv Biol 9:761–770. doi:10.1046/j.1523-1739.1995.09040761.x

    Article  Google Scholar 

  • Hulme PE (2006) Beyond control: wider implications for the management of biological invasions. J Appl Ecol 43:835–847. doi:10.1111/j.1365-2664.2006.01227.x

    Article  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. doi:10.1111/j.1365-2664.2006.01192.x

    Article  Google Scholar 

  • Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. P R Soc Lond B Bio 270:775–781. doi:10.1098/rspb.2003.2327

    Article  Google Scholar 

  • Marchante H (2001) Invasão dos ecossistemas dunares portugueses por Acacia: uma ameaça para a biodiversidade nativa. Master thesis, Faculty of Sciences and Technology, University of Coimbra, Coimbra

  • Marchante H, Marchante E, Freitas H (2003) Invasion of the Portuguese dune ecosystems by the exotic species Acacia longifolia (Andrews) Willd.: effects at the community level. In: Child LE, Brock JH, Brundu G, Prach K, Pyšek P, Wade PM, Williamson M (eds) Plant invasion: ecological threats and management solutions. Backhuys Publishers, Leiden, The Netherlands, pp 75–85

    Google Scholar 

  • Marchante HS, Marchante EM, Buscardo E, Maia J, Freitas H (2004) Recovery potential of dune ecosystems invaded by an exotic Acacia species (Acacia longifolia). Weed Technol 18:1427–1433

    Article  Google Scholar 

  • Marchante E, Kjøller A, Struwe S, Freitas H (2007) Soil microbial activity in dune ecosystems in Portugal invaded by Acacia longifolia. In: Tokarska-Guzik B, Brock JH, Brundu G, Child L, Daehler CC, Pyšek P (eds) Plant invasions: human perception, ecological impacts and management. Backhuys Publishers, Leiden, The Netherlands, pp 247–257

    Google Scholar 

  • Marchante E, Kjøller A, Struwe S, Freitas H (2008) Short and long-term impacts of Acacia longifolia invasion on the belowground processes of a Mediterranean coastal dune ecosystem. Appl Soil Ecol. doi:10.1016/j.apsoil.2008.04.004

    Google Scholar 

  • Maron JL, Connors PG (1996) A native nitrogen-fixing shrub facilitates weed invasion. Oecologia 105:302–312. doi:10.1007/BF00328732

    Article  Google Scholar 

  • Maron JL, Jefferies RL (1999) Bush lupine mortality, altered resource availability, and alternative vegetation states. Ecology 80:443–454

    Article  Google Scholar 

  • Maron JL, Jefferies RL (2001) Restoring enriched grasslands: Effects of mowing on species richness, productivity, and nitrogen retention. Ecol Appl 11:1088–1100. doi:10.1890/1051-0761(2001)011[1088:REGEOM]2.0.CO;2

    Article  Google Scholar 

  • Miller M, Palojarvi A, Rangger A, Reeslev M, Kjoller A (1998) The use of fluorogenic substrates to measure fungal presence and activity in soil. Appl Environ Microbiol 64:613–617

    PubMed  CAS  Google Scholar 

  • Mitchell RJ, Marrs RH, Le Duc MG, Auld MHD (1999) A study of the restoration of heathland on successional sites: changes in vegetation and soil chemical properties. J Appl Ecol 36:770–783. doi:10.1046/j.1365-2664.1999.00443.x

    Article  Google Scholar 

  • Olff H, Huisman J, Van Tooren BF (1993) Species dynamics and nutrient accumulation during early primary succession in coastal sand dunes. J Ecol 81:693–706. doi:10.2307/2261667

    Article  Google Scholar 

  • Peperkorn R, Werner C, Beyschlag W (2005) Phenotypic plasticity of an invasive acacia versus two native Mediterranean species. Funct Plant Biol 32:933–944. doi:10.1071/FP04197

    Article  Google Scholar 

  • Perry LG, Galatowitsch SM, Rosen CJ (2004) Competitive control of invasive vegetation: a native wetland sedge suppresses Phalaris arundinacea in carbon-enriched soil. J Appl Ecol 41:151–162. doi:10.1111/j.1365-2664.2004.00871.x

    Article  CAS  Google Scholar 

  • Pickart AJ, Miller LM, Duebendorfer TE (1998) Yellow bush lupine invasion in Northern California coastal dunes I. Ecological impacts and manual restoration techniques. Restor Ecol 6:59–68. doi:10.1046/j.1526-100x.1998.00618.x

    Article  Google Scholar 

  • Prober SM, Thiele KR, Lunt ID, Koen TB (2005) Restoring ecological function in temperate grassy woodlands: manipulating soil nutrients, exotic annuals and native perennial grasses through carbon supplements and spring burns. J Appl Ecol 42:1073–1085. doi:10.1111/j.1365-2664.2005.01095.x

    Article  CAS  Google Scholar 

  • Sayer EJ (2006) Using experimental manipulation to assess the roles of leaf litter in the functioning of forest ecosystems. Biol Rev Camb Philos Soc 81:1–31. doi:10.1017/S1464793105006846

    PubMed  Google Scholar 

  • Silva R (1977) Sector Fertilidade do Solo. Laboratório Químico-Agrícola. Ministério da Agricultura e Pescas, Lisbon

  • Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651. doi:10.1016/j.tree.2006.07.007

    PubMed  Article  Google Scholar 

  • van den Berg LJL, Tomassen HBM, Roelofs JGM, Bobbink R (2005) Effects of nitrogen enrichment on coastal dune grassland: a mesocosm study. Environ Pollut 138:77–85. doi:10.1016/j.envpol.2005.02.024

    PubMed  Article  CAS  Google Scholar 

  • van der Putten WH, Peters BAM (1995) Possibilities for management of coastal foredunes with deteriorated stands of Ammophila arenaria (marram grass). J Coast Conserv 1:29–39

    Article  Google Scholar 

  • Vinton MA, Burke IC (1995) Interactions between individual plant species and soil nutrient status in shortgrass steppe. Ecology 76:1116–1133. doi:10.2307/1940920

    Article  Google Scholar 

  • Vinton MA, Goergen EM (2006) Plant-soil feedbacks contribute to the persistence of Bromus inermis in tallgrass prairie. Ecosystems (N Y, Print) 9:967–976. doi:10.1007/s10021-005-0107-5

    Article  CAS  Google Scholar 

  • Wittenberg R, Cock MJW (2005) Best practices for the prevention and management of invasive alien species. In: Mooney HA, Mack RN, McNeely JA, Neville LE, Schei PJ, Waage JK (eds) Invasive alien species. A new systhesis. Island Press, Washington, p 368

    Google Scholar 

  • Yelenik SG, Stock WD, Richardson DM (2004) Ecosystem level impacts of invasive Acacia saligna in the South African fynbos. Restor Ecol 12:44–51. doi:10.1111/j.1061-2971.2004.00289.x

    Article  Google Scholar 

  • Yelenik SG, Stock WD, Richardson DM (2007) Functional group identity does not predict invader impacts: differential effects of nitrogen-fixing exotic plants on ecosystem function. Biol Invasions 9:117–125. doi:10.1007/s10530-006-0008-3

    Article  Google Scholar 

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Acknowledgements

Special thanks to Hélia Marchante, John Hoffmann, and Susana Echeverría for valuable discussions and checking of English grammar. Three anonymous reviewers provided helpful comments, which greatly improved a previous version of the manuscript. We are also grateful to Karin Vestberg for technical assistance. This research was supported by FCT-MCTES (Portuguese Foundation for Science and Technology) and European fund FEDER, project POCTI/BSE/42335/2001 & POCI(PPCDT)/AMB/61387/2004. E.M. was supported by a FCT-MCTES grant.

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Correspondence to Elizabete Marchante.

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Marchante, E., Kjøller, A., Struwe, S. et al. Soil recovery after removal of the N2-fixing invasive Acacia longifolia: consequences for ecosystem restoration. Biol Invasions 11, 813–823 (2009). https://doi.org/10.1007/s10530-008-9295-1

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  • DOI: https://doi.org/10.1007/s10530-008-9295-1

Keywords

  • Ecosystem processes
  • Microbial activity and biomass
  • C and N-cycling
  • Potential nitrification
  • Soil ecology
  • β-glucosaminidase activity