Skip to main content

Advertisement

SpringerLink
Log in

Soil enzymes associated with carbon and nitrogen cycling in invaded and native secondary forests of northwestern Argentina

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Alien success has frequently been associated with changes in the concentrations of soil nutrients. We aim to investigate the effects of plant invasion on soil nutrients, potential enzyme activity and litter elemental composition and stoichiometry.

Methods

We compared stands of secondary forest invaded by Ligustrum lucidum and those dominated by natives, and performed litter chemical analyses on 3 native and 2 exotic tree species.

Results

Soils of invaded sites had 20 and 30 % increase in β-glucosidase and alkaline phosphatase activity, higher Olsen-phosphorus (P) and potassium (K) concentrations and lower nitrogen (N) concentration and N:P, N:K and ammonium:Olsen-P ratios. Invaded and non-invaded sites differed in their overall nutrient composition and enzyme activity. Natives and exotics differed in nine of the 16 litter elemental composition and stoichiometry variables analyzed.

Conclusions

The low N:P ratio in litter, the decrease in soil N in invaded stands and the low N concentration of exotics suggest that N is the limiting nutrient and that exotic success is related to higher N uptake and use efficiency. The higher investment in the acquisition of soil resources, higher nutrient uptake and use efficiency of limiting nutrients contribute to the success of exotics in this subtropical forest.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alder PB, Ellner SP, Levine JM (2010) Coexistence of perennial plants: an embarrassment of niches. Ecol Lett 13:1019–1029

    Google Scholar 

  • Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:162–619

    Article  Google Scholar 

  • Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

    Article  CAS  Google Scholar 

  • Aragón R, Morales JM (2003) Species composition and invasion in NW Argentinean secondary forests: Effects of land use history, environment and landscape. J Veg Sci 14:195–204

    Article  Google Scholar 

  • Aragón R, Montti L, Ayup MM, Fernández R (2014) Exotic species as modifiers of ecosystem processes: Litter decomposition in native and invaded secondary forests of NWArgentina. Acta Oecol 54:21–28

    Article  Google Scholar 

  • Ayup MM, Montti L, Aragón R, Grau HR (2014) Invasion of Ligustrum lucidum (Oleaceae) in the southern Yungas: Changes in habitat properties and decline in bird diversity. Acta Oecol 54:72–81

    Article  Google Scholar 

  • Bartolucci G (2011) Descripción de los bosques de Ligustrum lucidum (Oleácea) en la selva de Yungas en la provincia de Tucumán y su influencia sobre la comunidad de renovales. Undergraduate dissertation. University of Tucumán. Argentina

  • Baruch Z, Goldstein G (1999) Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 121:183–192

    Article  Google Scholar 

  • Bianchi AR, Yañez C (1992) Las precipitaciones del Noroeste Argentino. Instituto de Tecnología Agropecuaria, Argentina

    Google Scholar 

  • Biondini ME, Bonham CD, Redente EF (1985) Secondary successional patterns in a sagebrush (Artemisia tridentata) community as they relate to soil disturbance and soil biological activity. Vegetatio 60:25–36

    Article  Google Scholar 

  • Blank RR (2010) Intraspecific and interspecific pair-wise seedling competition between exotic annual grasses and native perennials: plant-soil relationships. Plant Soil 326:331–343

    Article  CAS  Google Scholar 

  • Blank RR, Sforza R (2007) Plant-soil relationships of the invasive annual grass Taeniatherum caput-medusae: a reciprocal transplant experiment. Plant Soil 298:7–19

    Article  CAS  Google Scholar 

  • Bonsall MB, Jansen VAA, Hassell MP (2004) Life history trade-offs assemble ecological guilds. Science 306:111–114

    Article  PubMed  CAS  Google Scholar 

  • Bray SR, Kitayima K, Sylvia DM (2003) Mycorrhizae differentially alter growth physiology, and competitive ability of an invasive shrub. Ecol Appl 13:565–574

    Article  Google Scholar 

  • Brown AD, Grau HR, Malizia LR, Grau A (2001). Argentina. In: Kappelle M and Brown AD (Eds.), Bosques nublados del Neotrópico. Instituto Nacional de Biodiversidad (INBio), Santo Domingo de Heredia, Costa Rica, 623-659

  • Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biol Biochem 58:216–234

    Article  CAS  Google Scholar 

  • Cabrera AL, Willink A (1980) Biogeografía de América Latina. Organización para Estados Americanos (OEA), Washington

    Google Scholar 

  • Castro- Díez P, Godoy O, Alonso A, Gallardo A, Saldaña A (2013) What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A meta-analysis. Ecol Lett. doi:10.1111/ele.12197

    PubMed  Google Scholar 

  • Criquet S, Ferre E, Farnet AM, Le Petit J (2004) Annual dynamics of phosphatase activities in an evergreen oak litter: influence of biotic and abiotic factors. Soil Biol Biochem 36:1111–1118

    Article  CAS  Google Scholar 

  • Davies KF, Harrison S, Safford HD, Viers JH (2007) Productivity alters the scale dependence of the diversity-invasibility relationship. Ecology 88:1940–1947

    Article  PubMed  Google Scholar 

  • Debosz K, Rasmussen PH, Pedersen AR (1999) Temporal variations in microbial biomass C abd cellulolytic enzyme activity in arable soils: effects of organic matter input. Appl Soil Ecol 13:209–218

    Article  Google Scholar 

  • Drenovsky RE, Grewell BJ, D’Antonio CM, Funk JL, James JJ, Molinari N, Parker IM, Richards CM (2012) A functional trait perspective on plant invasion. Ann Bot 110:141–153

    Article  PubMed  PubMed Central  Google Scholar 

  • Dye P, Jarmain C (2004) Water use by black wattle (Acacia mearnsii): implications for the link between removal of invaded trees and catchment streamflow response. S Afr J Sci 100:40–44

    Google Scholar 

  • Easdale TA (2006) Comparative morphologies and life histories amongst montane tree species in North-Western Argentina. PhD Dissertation. University of Wales, Bangor, United Kingdom

  • Easdale TA, Healey JR (2009) Resource-use-related traits correlate with population turnover rates, but not stem diameter growth rates, in 29 subtropical montane tree species. Perspect Plant Ecol Evol Syst 11:203–218

    Article  Google Scholar 

  • Easdale TA, Healey JR, Grau HR, Malizia A (2007) Tree life histories in a montane subtropical forest: species differ independently by shade-tolerance, turnover rate and substrate preference. J Ecol 95:1234–1239

    Article  Google Scholar 

  • Ehrenfeld JG (2003) Effects of Exotic Plant Invasions on Soil Nutrient Cycling Processes. Ecosystems 6:503–523

    Article  CAS  Google Scholar 

  • Ehrenfeld JG, 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 

  • Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943

    Article  Google Scholar 

  • Evans RD, Rimer R, Sperry L, Belnap J (2001) Exotic plant invasion alters nitrogen dynamics In an arid grassland. Ecol Appl 11:1301–1310

    Article  Google Scholar 

  • Feng YL (2008) Photosynthesis, Nitrogen allocation and specific leaf area in invasive Eupatorium adenophorum and native Eupatorium japonicum grown at different irradiances. Physiol Plant 133:318–326

    Article  PubMed  CAS  Google Scholar 

  • Feng YL, Auge H, Ebeling SK (2007) Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 153:501–510

    Article  PubMed  Google Scholar 

  • Feng YL, Li YP, Wang RF, Callaway RM, Valiente-Banuet A, Inderjit (2011) A quicker return energy-use strategy by populations of a subtropical invader in the non-native range: a potential mechanism for the evolution of increased competitive ability. J Ecol 99:1116–1123

    Article  Google Scholar 

  • Fernandez RD (2012) Descomposición de hojarasca en Bosques secundarios de la Sierra de San Javier: efecto de las especies exóticas. Undergraduate dissertation. University of Tucumán. Argentina

  • Fierer N, Bradford MA, Jackson RB (2007) Towards an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  • Flory LS, Clay K (2010) Non-native grass invasion alters native plant composition in experimental communities. Biol Inv 12:1285–1294

    Article  Google Scholar 

  • Funk JL, Vitousek PM (2007) Resource use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081

    Article  PubMed  CAS  Google Scholar 

  • Gerlach Jr. JD (2000) A model experimental system for predicting the invasion success and ecosystem impacts of non-indigenuous summer-flowering annual plants in California’s Central Valley grasslands and oak woodlands. PhD dissertation, University of California, Davis, CA

  • González AL, Kominoski JS, Danger M, Ishida S, Iwai N, Rubach A (2010) Can ecological stoichiometry help explain patterns of biological invasion? Oikos 119:779–790

    Article  Google Scholar 

  • Grau HR, Aide TM (2007) Are Rural–Urban Migration and Sustainable Development Compatible in Mountain Systems? Mt Res Dev 27:119–123

    Article  Google Scholar 

  • Grau HR, Aragón R (2000) Arboles invasores de la Sierra de San Javier. In: Grau HR, Aragón R (eds) Arboles Exóticos de las Yungas Argentinas. LIEY-Universidad Nacional de Tucumán, Tucumán, pp 5–20

    Google Scholar 

  • Grau HR, Brown AD (1995) Patterns of tree species diversity along latitudinal and altitudinal gradients in the Argentinean subtropical montane forests. In: Churchill SP, Balslev H, Forero E, Luteyn J (eds) Biodiversity and conservation of Neotropical montane forest. New York Botanical Garden, Bronx, pp 295–300

    Google Scholar 

  • Grau HR, Arturi MF, Brown AD, Aceñolaza PG (1997) Floristic and structural patterns along a chronosequence of secondary forest succession in Argentinean subtropical montane forests. Forest Ecol Manag 95:161–171

    Article  Google Scholar 

  • Grau HR, Hernández ME, Gutierrez J, Gasparri NI, Casavecchia MC, Flores EE, Paolini L (2008) A peri-urban neotropical forest transition and its consequences for environmental services. Ecol Soc 13(1): 35 [online] URL: http://www.ecologyandsociety.org/vol13/iss1/art35/

  • Harrington RA, Fownes JH, Cassidy TM (2004) Japanese Barberry (Berberis thunbergii) in forest understory: leaf and whole plant reponses to nitrogen availability. Am Midl Nat 151:206–216

    Article  Google Scholar 

  • Hewins DB, Hyatt LA (2010) Flexible N uptake and assimilation mechanisms may assist biological invasion by Alliaria petiolata. Biol Inv 12:2639–2647

    Article  Google Scholar 

  • Holmes PM, Richardson DM, Elser KJ, Witkowski ETF, Fourie S (2005) A decision-making framework for restoring riparian zones degraded by invasive alien plants in South Africa. S Afr J Sci 101:553–564

    Google Scholar 

  • Joanisse GD, Bradley RL, Preston CM, Munson AD (2007) Soil enzyme inhibition by condensed litter tannins may drive ecosystem structure and processes: the case of Kalmia angustifolia. New Phytol 175:535–546

    Article  PubMed  CAS  Google Scholar 

  • Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fert Soils 6:68–72

    Article  CAS  Google Scholar 

  • Kolb A, Alpert P, Enters D, Holzapfe C (2002) Patterns of invasion within a grassland community. J Ecol 90:871–881

    Article  Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Huang WZ (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 

  • Ladd JM, Brisbane PG, Butler JHA (1976) Studies on soil fumigation. 3. Effects on enzyme-actrivities, bacterial numbers and extractable ninhydrin reactive compounds. Soil Biol Biochem 8:255–260

    Article  CAS  Google Scholar 

  • Leffler AJ, Monaco TA, James JJ (2011) Nitrogen acquisition by annual and perennial grass seedlings: testing the roles of performance and plasticity to explain plant invasion. Plant Ecol 212:1601–1611

    Article  Google Scholar 

  • Leishman MR, Haslchurst T, Ares A, Baruch Z (2007) Leaf trait relationships of native and invasive plants: community-and global-scale comparisons. New Phytol 176:635–643

    Article  PubMed  CAS  Google Scholar 

  • Leishman MR, Thomson VP, Cooke J (2010) Native and exotic invasive plants have fundamentally similar carbon capture strategies. J Ecol 98:28–42

    Article  CAS  Google Scholar 

  • Levine JM, HilleRisLambers J (2009) The importance for the maintenance of species diversity. Nature 461:254–U130

    Article  PubMed  CAS  Google Scholar 

  • Levine JM, Vilà M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plants. Proc R Soc Lond B 270:775–781

    Article  Google Scholar 

  • Lichstein JW, Grau HR, Aragón R (2004) Recruitment limitation in secondary forests dominated by an exotic tree. J Veg Sci 15:721–728

    Article  Google Scholar 

  • McCune B, Mefford MJ (1999) PC-ORD Multivariate analysis of ecological data. Version 3. 0. MjM Software Design, Gleneden Beach, OR

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C : N : P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci U S A 98:5446–5451

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mozder TJ, Zieman JC (2010) Ecophysiological differences between genetic lineages facilitate the invasion of non-native Phragmites australis in North American Atlantic coast wetlands. J Ecol 98:451–458

    Article  Google Scholar 

  • Nagel JM, Griffin KL (2001) Construction cost and invasive potential: comparing Lythrum salicaria (Lythraceae) with co-occurring native species along pond banks. Am J Bot 88:2252–2258

    Article  PubMed  CAS  Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA. Cir. n 939

  • Peng RH, Fang CM, Li B, Chen JK (2011) Spartina alterniflora invasion inceases soil inorganic nitrogen pools through interactions with tidal subsides in the Yangtze Estuary, China. Oecologia 165:797–807

    Article  PubMed  Google Scholar 

  • Peñuelas J, Sardans J, Ogaya R, Estiarte M (2008) Nutrient stoichiometric relations and biogeochemical niche in coesxisting plant species: effect of simulated climatic change. Pol J Ecol 56(4):613–622

    Google Scholar 

  • Peñuelas J, Sardans J, Llusia Owen S, Carnicer J, Giambelluca TW, Rezende EL, Waite M, Niinemets Ü (2010) Faster returns on leaf economics and different biogeochemical niche in invasive compared with native plant species. Glob Chang Biol 16:2171–2185

    Article  Google Scholar 

  • Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP (2004) Seasonal sexual segregation in two Thalassarche species: competitive exclusion, reproductive role specialization or foraging niche divergence? Proc R Soc B Biol Sci 271:1283–1291

    Article  CAS  Google Scholar 

  • Sardans J, Peñuelas J (2005) Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biol Biochem 37:455–461

    Article  CAS  Google Scholar 

  • Sardans J, Peñuelas J (2010) Soil enzyme activity in a Mediterranean forest after six Years of drought. Soil Sci Soc Am J 74:838–851

    Article  CAS  Google Scholar 

  • Sardans J, Peñuelas J (2012) The role of plants in the effects of Global Change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiol 160:1741–1761

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sardans J, Peñuelas J (2013) Climate and taxonomy underlie different elemental concentrations and stoichiometries of forest species: the optimum “biogeochemical niche”. Plant Ecol 215:441–455

    Article  Google Scholar 

  • Sardans J, Peñuelas J, Ogaya R (2008) Experimental drought reduced acid and alkaline phosphatase activity and increased organic extractable P in soil in a Quercus ilex Mediterranean forest. Eur J Soil Biol 44:509–520

    Article  CAS  Google Scholar 

  • Schinner F, Ohlinger R, Kandeler E, Margesin R (1996) Methods in Soil Biology. Springer Lab Manual, Berlin

    Book  Google Scholar 

  • Shah MA, Reshi ZA, Khasa DP (2009) Arbuscular mycorryzhas: drivers or passengers of alien plant invasion. Bot Rev 75:397–417

    Article  Google Scholar 

  • Shen XY, Peng SL, Chen BM, Pang JX, Chen LY, Xu HM, Hou YP (2011) Do higher resource capture ability and utilization efficiency facilitate the successful invasion of native plants? Bio Inv 13:869–881

    Article  Google Scholar 

  • Sinsabaugh RL, Antibus RK, Linkins AE, McClaugherty CA, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: Nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:1586–1593

    Article  CAS  Google Scholar 

  • Stege PW, Messina GA, Bianchi G, Olsina RA, Raba J (2010) Determination of b-glucosidase activity in soils with a bioanalytical sensor modified with multiwalled carbon nanotubes. Anal Bioanal Chem 397:1347–1353

    Article  PubMed  CAS  Google Scholar 

  • Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 17:1199–1210

    Article  Google Scholar 

  • Tabatabai MA (1994) Soil enzymes. In: Bottomley PS, Angle JS, Weaver RW (eds) Methods of Soil Analysis: Part 2- Microbiological and Biochemical Properties. Soil Science Society of America, Madison, pp 775–833

    Google Scholar 

  • Tecco P, Diaz S, Cabido M, Urcelay C (2010) Functional traits of alien plants across contrasting climatic and land-use regimes: do aliens join the locals or try harder than them? J Ecol 98:17–27

    Article  Google Scholar 

  • Tharayil N, Alpert P, Bhowmik PC, Gerard P (2013) Phenolic inputs by invasive species could impart seasonal variations in nitrogen pools in the introduced soils: a case study with Polygonum cuspidatum. Soil Biol Bioche 57:858–867

    Article  CAS  Google Scholar 

  • Van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37

    Article  PubMed  Google Scholar 

  • Van Kleunen M, Weber E, Fischer M (2010) A meta‐analysis of trait differences between invasive and non‐invasive plant species. Ecol Lett 13:235–245

    Article  PubMed  Google Scholar 

  • Van Wilgen BW, Reyers B, Le Maitre DC, Richardson DM, Schonegevel L (2008) A biome-scale assessment of the impact of invasive alien plants on ecosystems services in South Africa. J Environ Manag 89:336–349

    Article  Google Scholar 

  • Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106

    Article  CAS  Google Scholar 

  • Xu CY, Griffin KL, Schuster WSF (2007) Leaf phenology and seasonal variation of photosynthesis of invasive Berberis thunbergii (Japanese barberry) and two co-occuring native understory shrubs in a northeastern United States deciduous forest. Oecologia 154:11–21

    Article  PubMed  Google Scholar 

  • Zabinsky CA, Quinn L, Callaway RM (2002) Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Funct Ecol 16:758–765

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the Spanish Government grant CGL2013-48074-P, the Catalan Government project SGR 2014- 274 and the European Research Council Synergy grant ERC-2013-SyG-610028 IMBALANCE-P. R. Aragón’s stay at CREAF was supported by an external grant from CONICET (National Research Council, Argentina).

Author information

Authors and Affiliations

  1. Instituto de Ecología Regional, Universidad Nacional de Tucumán, CC 34 (4107), Tucumán, Argentina

    Roxana Aragón

  2. CSIC, Global Ecology Unit CREAF-CSIC-UAB, Cerdanyola del Vallès, 08193, Barcelona, Catalonia, Spain

    Jordi Sardans & Josep Peñuelas

  3. CREAF, Cerdanyola del Vallès, 08193, Barcelona, Catalonia, Spain

    Jordi Sardans & Josep Peñuelas

Authors
  1. Roxana Aragón
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jordi Sardans
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Josep Peñuelas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roxana Aragón.

Additional information

Responsible Editor: Harry Olde Venterink.

Appendix 1

Appendix 1

Table 4 Elements (±standard error) in leaf litter of the five species in the two forest types: invaded (INV) and native (NAT) forest stands (n = 5). Units as in Table 2. ** indicates significant differences at p < 0.01 for species, forest type (FT) and species and forest-type interaction (Sp*FT)
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aragón, R., Sardans, J. & Peñuelas, J. Soil enzymes associated with carbon and nitrogen cycling in invaded and native secondary forests of northwestern Argentina. Plant Soil 384, 169–183 (2014). https://doi.org/10.1007/s11104-014-2192-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-014-2192-8

Keywords

Search

Navigation