Antonie van Leeuwenhoek

, Volume 110, Issue 9, pp 1207–1218 | Cite as

Fungal decomposers of leaf litter from an invaded and native mountain forest of NW Argentina

  • Romina Daiana FernandezEmail author
  • Natalia Bulacio
  • Analía Álvarez
  • Hipólito Pajot
  • Roxana Aragón
Original Paper


The impact of plant species invasions on the abundance, composition and activity of fungal decomposers of leaf litter is poorly understood. In this study, we isolated and compared the relative abundance of ligninocellulolytic fungi of leaf litter mixtures from a native forest and a forest invaded by Ligustrum lucidum in a lower mountain forest of Tucuman, Argentina. In addition, we evaluated the relationship between the relative abundance of ligninocellulolytic fungi and properties of the soil of both forest types. Finally, we identified lignin degrading fungi and characterized their polyphenol oxidase activities. The relative abundance of ligninocellulolytic fungi was higher in leaf litter mixtures from the native forest. The abundance of cellulolytic fungi was negatively related with soil pH while the abundance of ligninolytic fungi was positively related with soil humidity. We identified fifteen genera of ligninolytic fungi; four strains were isolated from both forest types, six strains only from the invaded forest and five strains were isolated only from the native forest. The results found in this study suggest that L. Lucidum invasion could alter the abundance and composition of fungal decomposers. Long-term studies that include an analysis of the nutritional quality of litter are needed, for a more complete overview of the influence of L. Lucidum invasion on fungal decomposers and on leaf litter decomposition.


Exotic plants Fungal decomposers Leaf litter Lignocellulolytic activities Ligustrum lucidum Subtropical forest 



This work was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET-PIP 0372) and Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT-PICT 0480). We thank Fernandez MJ for field assistance, Nanni S for the help with the English version of this manuscript and associate editor and two anonymous reviewers for comments that improved the manuscript. Finally we acknowledge the authorities of Parque Sierra de San Javier for the permissions to conduct this study.

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study


  1. Alexopoulos CJ, Mims CW, Blackwell M (1996) Introductory mycology, 4th edn. Wiley, New York, USAGoogle Scholar
  2. Aragón R, Groom M (2003) Invasion by Ligustrum lucidum (Oleaceae) in NW Argentina: early stage characteristics in different habitat types. Rev Biol Trop 51:59–70PubMedGoogle Scholar
  3. Aragón R, Morales JM (2003) Species composition and invasion in NW Argentinian secondary forests: effects of land use history, environment and landscape. J Veg Sci 14:195–204CrossRefGoogle Scholar
  4. Aragón R, Montti L, Ayup MM, Fernández R (2014a) Exotic species as modifiers of ecosystem processes: Litter decomposition in native and invaded secondary forests of NW Argentina. Acta Oecol 54:21–28CrossRefGoogle Scholar
  5. Aragón R, Sardans J, Peñuelas J (2014b) Soil enzymes associated with carbon and nitrogen cycling in invaded and native secondary forests of northwestern Argentina. Plant Soil 384:169–183CrossRefGoogle Scholar
  6. Araujo Costa L, Pascholati Gusmão LF (2015) Characterization saprobic fungi on leaf litter of two species of trees in the Atlantic Forest, Brazil. Braz J Microbiol 46:1027–1035CrossRefGoogle Scholar
  7. Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Lerdau MT (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272CrossRefGoogle Scholar
  8. 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 54:72–81CrossRefGoogle Scholar
  9. Bachelot B, Uriarte M, Zimmerman JK, Thompson J, Leff JW, Asiaii A, Koshner J, McGuire K (2016) Long-lasting effects of land use history on soil fungal communities in second-growth tropical rain forests. Ecol Appl 26:1881–1895CrossRefPubMedGoogle Scholar
  10. Berg B (2000) Litter decomposition and organic matter turnover in northern forest soils. Forest Ecol Manag 133:13–22CrossRefGoogle Scholar
  11. Berg B, McClaugherty CA (2008) Plant litter: decomposition, humus formation, carbon sequestration, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  12. Bianchi AR (1981) Las precipitaciones en el Noroeste argentino. INTA, SaltaGoogle Scholar
  13. Bills GF, Polishook JD (1994) Abundance and diversity of microfungi in leaf litter of a lowland rain forest in Costa Rica. Mycologia 86:187–198CrossRefGoogle Scholar
  14. Broz AK, Manter DK, Vivanco JM (2007) Soil fungal abundance an-d diversity: another victim of the invasive plant Centaurea maculosa. The ISME J 1:763–765CrossRefPubMedGoogle Scholar
  15. Cabrera A (1976) Regiones fitogeográficas de Argentina. In: Kugler WF (ed) Enciclopedia Argentina de Agricultura y Jardinería II, 2nd edn. Acme, Buenos Aires, pp 1–85Google Scholar
  16. Cabuk A, Unal AT, Kolankaya N (2006) Biodegradation of cyanide by a white rot fungus, Trametes versicolor. Biotechnol Lett 28:1313–1317CrossRefPubMedGoogle Scholar
  17. Ceballos SJ, Malizia A, Chacoff NP (2015) Influencia de la invasión de Ligustrum lucidum (Oleaceae) sobre la comunidad de lianas en la sierra de San Javier (Tucumán-Argentina). Ecol Aust 25:65–74Google Scholar
  18. Colpaert JV, Van Laere A (1996) A comparison of the extracellular enzyme activities of two ectomycorrhizal and a leaf-saprotrophic basidiomycete colonizing beech leaf litter. New Phytol 133:133–141CrossRefGoogle Scholar
  19. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  20. de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811CrossRefPubMedGoogle Scholar
  21. DeAngelis KM, Chivian D, Fortney JL, Arkin AP, Simmons B, Hazen TC, Silver WL (2013) Changes in microbial dynamics during long-term decomposition in tropical forests. Soil Biol Biochem 66:60–68CrossRefGoogle Scholar
  22. 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 95:1234–1239CrossRefGoogle Scholar
  23. Ehrenfeld J, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300CrossRefGoogle Scholar
  24. Estación Experimental Agroindustrial Obispo Colombres (2015) Accessed 10 Nov 2016
  25. Fang G, Hammar S, Grumet R (1992) A quick and inexpensive method for removing polysaccharides from plant genomic DNA. Biotechniques 13:52–55PubMedGoogle Scholar
  26. Geml J, Pastor N, Fernandez L, Pacheco S, Semenova TA, Becerra AG, Wicaksono CY, Nouhra ER (2014) Large-scale fungal diversity assessment in the Andean Yungas forests reveals strong community turnover among forest types along an altitudinal gradient. Mol Ecol 23:2452–2472CrossRefPubMedGoogle Scholar
  27. Grau HR, Aragón R (2000) Árboles invasores de la Sierra de San Javier. In: Grau HR, Aragón R (eds) Árboles exóticos de las Yungas Argentinas. LIEY- UNT, Tucumán, pp 5–20Google Scholar
  28. Grau HR, Arturi MF, Brown AD, Aceñolaza PG (1997) Floristic and structural patterns along a chronosequence of secondary forest succession in Argentinean subtropical montane forest. For Ecol Manag 95:161–171CrossRefGoogle Scholar
  29. Grau HR, Hernández ME, Gutierrez J, Gasparri NI, Casavecchia MC, Flores E, Paolini L (2008) A peri-urban neotropical forest transition and its consequences for environmental services. Ecol Soc 13:35CrossRefGoogle Scholar
  30. Hammel KE (1997) Fungal degradation of lignin. In: Cadisch G, Giller KE (eds) Plant litter quality and decomposition. CAB-International, Wallingford, pp 33–46Google Scholar
  31. Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218CrossRefGoogle Scholar
  32. Kerekes J, Kaspari M, Stevenson B, Nilsson RH, Hartmann M, Amend A, Bruns TD (2013) Nutrient enrichment increased species richness of leaf litter fungal assemblages in a tropical forest. Mol Ecol 22:2827–2838CrossRefPubMedGoogle Scholar
  33. Korniłłowicz-Kowalska T, Iglik H, Wojdyło B (2003) Correlation between the abundance of cellulolitic fungi and selected soil properties. Acta Micol 38:161–172CrossRefGoogle Scholar
  34. Kourtev PS, Ehrenfeld JG, 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 Bioch 35:895–905CrossRefGoogle Scholar
  35. Kurtzman CP, Fell JW, Boekhout T, Robert V (eds) (2011) Methods for isolation, phenotypic characterization and maintenance of yeasts. In: The yeasts, a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 87–110CrossRefGoogle Scholar
  36. Kwiatkowski NP, Babiker WM, Merz WG, Carroll KC, Zhang SX (2012) Evaluation of nucleic acid sequencing of the D1/D2 region of the large subunit of the 28S rDNA and the internal transcribed spacer region using SmartGene IDNS Software for identification of filamentous fungi in a clinical laboratory. J Mol Diagn 14(4):393–401CrossRefPubMedGoogle Scholar
  37. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Bioch 40:2407–2415CrossRefGoogle Scholar
  38. Lichstein JW, Grau HR, Aragón R (2004) Recruitment limitation in secondary forests dominated by an exotic tree. J Veg Sci 15:721–728CrossRefGoogle Scholar
  39. Lomascolo A, Uzan-Boukhris E, Herpoel-Gimbert I, Sigoillot JC, Lesage-Meessen L (2011) Peculiarities of Pycnoporus species for applications in biotechnology. Appl Microbiol Biotechnol 92:1129–1149CrossRefPubMedGoogle Scholar
  40. Malherbe S, Cloete TE (2002) Lignocellulose biodegradation: fundamentals and applications. Rev Environ Sci Bio/Technol 1:105–114CrossRefGoogle Scholar
  41. Malizia A, Grau HR, Lichstein JW (2010) Soil phosphorus and disturbance influence liana communities in a subtropical montane forest. J Veg Sci 21:551–560CrossRefGoogle Scholar
  42. Márquez ATA, Mendoza MGD, González MSS (2007) Actividad fibrolitica de enzimas producidas por Trametes sp. EUM1, Pleurotus ostreatus IE8 y Aspergillus niger AD96.4 en fermentación sólida. Interciencia 32:780–785Google Scholar
  43. McGuire KL, Bent E, Borneman J, Majumder A, Allison SD, Treseder KK (2010) Functional diversity in resource use by fungi. Ecology 91(8):2324–2332CrossRefPubMedGoogle Scholar
  44. McGuire KL, Fierer N, Bateman C, Treseder KK, Turne BL (2012) Fungal community composition in neotropical rain forests: the influence of tree diversity and precipitation. Microb Ecol 63:804–812CrossRefPubMedGoogle Scholar
  45. Moredo N, Lorenzo M, Domínguez A, Moldes D, Cameselle C, Sanroman A (2003) Enhanced ligninolytic enzyme production and degrading capability of Phanerochaete chrysosporium and Trametes versicolor. World J Microb Biotechnol 19:665–669CrossRefGoogle Scholar
  46. Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974CrossRefGoogle Scholar
  47. Osono T, Hirose D, Fujimaki R (2006) Fungal colonization as affected by litter depth and decomposition stage of needle litter. Soil Biol Bioch 38:2743–2752CrossRefGoogle Scholar
  48. Osono T, Ishii Y, Takeda H, Seramethakun T, Khamyong S, To-Anun C, Hirose D, Tokumasu S, Kakishima M (2009) Fungal succession and lignin decomposition on Shorea obtusa leaves in a tropical seasonal forest in northern Thailand. Fungal divers 36:101–119Google Scholar
  49. Paulus BC, Kanowski J, Gadek PA, Hyde KD (2006) Diversity and distribution of saprobic microfungi in leaf litter of an Australian tropical rainforest. Mycol Res 110:1441–1454CrossRefPubMedGoogle Scholar
  50. Pérez J, Muñoz-Dorado J, De-la-Rubia T, Martínez J (2002) Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int Microbiol 5:53–63CrossRefPubMedGoogle Scholar
  51. Pietikäinen J, Pettersson M, Bååth E (2004) Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol 52:49–58CrossRefPubMedGoogle Scholar
  52. Pointing SB (1999) Qualitative methods for the determination of lignocellulolytic enzyme production by tropical fungi. Fungal Divers 2:17–33Google Scholar
  53. Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. Forest Ecol Manag 309:19–27CrossRefGoogle Scholar
  54. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  55. Reiss R, Ihssen J, Richter M, Eichhorn E, Schilling B, Thöny-Meyer L (2013) Laccase versus laccase-like multi-copper oxidase: a comparative study of similar enzymes with diverse substrate spectra. PLoS ONE 8:e65633CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351CrossRefPubMedGoogle Scholar
  57. Sánchez C (2009) Lignocellulosic residues: Biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194CrossRefPubMedGoogle Scholar
  58. Saparrat MCN, Hammer E (2006) Decolorization of synthetic dyes by the deuteromycete Pestalotiopsis guepinii CLPS no. 786 strain. J Basic Microbiol 46:28–33CrossRefPubMedGoogle Scholar
  59. Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–1762CrossRefPubMedPubMedCentralGoogle Scholar
  60. Schoch CL, Seifert KA, Huhndorf A et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. PNAS 109:6241–6246CrossRefPubMedPubMedCentralGoogle Scholar
  61. Slesak RA, Harrington TB, D’Amato AW (2016) Invasive scotch broom alters soil chemical properties in Douglas-fir forests of the Pacific Northwest, USA. Plant Soil 398:281–289CrossRefGoogle Scholar
  62. Stefanowicz AM, Stanek M, Nobis M, Zubek S (2016) Species-specific effects of plant invasions on activity, biomass, and composition of soil microbial communities. Biol Fertil Soils 52:841–852CrossRefGoogle Scholar
  63. Strauss MLA, Jolly NP, Lambrechts MG, Van Rensburg P (2001) Screening for the production of extracellular hydrolytic enzymes by non- Sacchraromyces wine yeasts. J Appl Microbiol 91:182–190CrossRefPubMedGoogle Scholar
  64. Tateno R, Tokuchi N, Yamanaka N, Du S, Otsuki K, Shimamura T, Xue Z, Wang S, Hou Q (2007) Comparison of litterfall production and leaf litter decomposition between an exotic black locust plantation and an indigenous oak forest near Yan’an on the Loess Plateau, China. For Ecol Manag 241:84–90CrossRefGoogle Scholar
  65. Tong P, Hong Y, Xiao Y, Zhang M, Tu X, Cui T (2007) High production of laccase by a new basidiomycete, Trametes sp. Biotechnol Lett 29:295–301CrossRefPubMedGoogle Scholar
  66. Voříšková J, Baldrian P (2013) Fungal community on decomposing leaf litter undergoes rapid successional changes. ISME J 7:477–486CrossRefPubMedGoogle Scholar
  67. Wardle DA, Yeates GW, Barker GM, Bonner KI (2006) The influence of plant litter diversity on decomposer abundance and diversity. Soil Biol Biochem 38:1052–1062CrossRefGoogle Scholar
  68. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  69. Zamora Nasca LB, Montti L, Grau HR, Paolini L (2014) Efectos de la invasión del ligustro, Ligustrum lucidum, en la dinámica hídrica de las Yungas del noroeste Argentino. Bosque 35:195–205CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Romina Daiana Fernandez
    • 1
    Email author
  • Natalia Bulacio
    • 2
  • Analía Álvarez
    • 2
    • 3
  • Hipólito Pajot
    • 2
  • Roxana Aragón
    • 1
    • 3
  1. 1.Instituto de Ecología Regional (IER, UNT- CONICET)Yerba BuenaArgentina
  2. 2.Planta Piloto de Procesos Industriales Microbiológicos (PROIMI, CONICET)San Miguel De TucumánArgentina
  3. 3.Facultad de Ciencias Naturales e IML (UNT)San Miguel De TucumánArgentina

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