Advertisement

Rapid effects of windfall on soil microbial activity and substrate utilization patterns in the forest belt in the Tatra Mountains

  • Katarzyna WasakEmail author
  • Beata Klimek
  • Marek Drewnik
Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
  • 51 Downloads

Abstract

Purpose

The aim of the study was to compare the activity, functional diversity, and community-level physiological profiles of soil microorganisms in light of soil physical and chemical properties in areas where a forest was damaged by hurricane-force winds and in untouched spruce forests of the lower montane belt of the Tatra Mountains (the Carpathians).

Materials and methods

Foehn winds caused a huge windfall in December 2013. The studied valley was strongly affected by windthrow, but in some places, patches of mature forest did survive. In the studied windthrow area, the first stage of secondary succession can now be observed. Sampling sites were selected in places where the soil was not mechanically disturbed. Soil samples were taken from the organic O and humus A soil horizons and basic soil properties were measured, as were the microbial parameters. Overall microbial activity was determined via the soil respiration rate (R), whereas the microbial biomass was determined via the substrate-induced respiration rate (SIR). Bacterial and fungal catabolic activity, functional diversity (H′), and community-level physiological profiles (CLPP) were determined using Biolog® ECO and FF plates, respectively.

Results and discussion

Research has shown that 21 months following the studied windthrow, in Hypereutric Skeletic Cambisols developed on calcareous parent material, changes have occurred in some soil properties: soil field moisture in O and A horizons has increased, DOC concentration in O horizons has decreased, and the C/N ratio in A horizons has decreased. The effect of the windthrow episode on overall biological activity was observed in soil A horizons, where overall microbial respiration and SIR biomass decreased. In both O and A horizons, the ratio of bacterial and fungal functional activity (AUCbact/fungi) increased as a result of a fungal AUC decrease. Significant differences in substrate utilization by bacteria occurred between forest-covered soils and windthrow soils in O horizons, where the share of polymer-utilized bacteria activity increased.

Conclusions

Rapid effects of windfall on soil microbial parameters expressed mostly in decrease overall microbial activity caused by breakdown in fungal activity. However, those differences are more pronounced in A than in O horizons. In spite of changes in those differences, windthrow did not produce a significant effect on the functional diversity index of microorganisms found in the studied soils.

Keywords

Calcareous soils Carpathians Microbial activity Microbial diversity Windthrow 

Notes

Acknowledgments

The authors wish to thank the authorities of Tatra National Park for permission to survey the study area and for their overall support. The research was partly funded by Project No. UJ/IGiGP/K/ZDS/007288 and DS/MND/WBiNoZ/IGiGP/42/2014. Language editing was done by Greg Zebik.

Funding information

The research was partly funded by Project No. UJ/IGiGP/K/ZDS/007288 and DS/MND/WBiNoZ/IGiGP/42/2014 by Jagiellonian University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11368_2019_2439_MOESM1_ESM.docx (23 kb)
ESM 1 (DOCX 22 kb)

References

  1. Adamczyk B, Adamczyk S, Kukkola M, Tamminen P, Smolander A (2015) Logging residue harvest may decrease enzymatic activity of boreal forest soils. Soil Biol Biochem 82:74–80CrossRefGoogle Scholar
  2. Ahmed YAR, Pichler V, Homolák M (2012) High organic carbon stock in a karstic soil of the Middle-European Forest Province persists after centuries-long agroforestry management. Eur J For Res 131:1669–1680CrossRefGoogle Scholar
  3. Alexander M (1977) Introduction to soil microbiology. John Wiley & Sons, New YorkGoogle Scholar
  4. Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:15–22Google Scholar
  5. Anderson T-H, Domsch KH (1986) Carbon assimilation and microbial activity in soil. Zeitschrift für Pflanzenernährung und Bodenkunde (now: Journal of Plant Nutrition and Soil Science) 149:457–468CrossRefGoogle Scholar
  6. Anderson T-H, Domsh KH (1993) The metabolic quotient for CO2 (qCO2) as a specific parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem 25:393–395CrossRefGoogle Scholar
  7. Bailey VL, Smith JL, Bolton H Jr (2002) Fungal-to-bacterial ratios in soil investigated for enhanced C sequestration. Soil Biol Biochem 34:997–1007Google Scholar
  8. Bertin C, Yan X, Weston L (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83CrossRefGoogle Scholar
  9. Blagodatskaya EV, Anderson T-H (1998) Interactive effects of pH and substrate quality on the fungal-to-bacterial ratio and qCO2 of microbial communities in forest soils. Soil Biol Biochem 30:1269–1274CrossRefGoogle Scholar
  10. Bouget C, Duelli P (2004) The effects of windthrow on forest insect communities: a literature review. Biol Conserv 118:281–299CrossRefGoogle Scholar
  11. Buckley DH, Schmidt TM (2001) The structure of microbial communities in soil and the lasting impact of cultivation. Microb Ecol 42:11–21Google Scholar
  12. Cambi M, Paffetti D, Vettori C, Picchio R, Venanzi R, Marchi E (2017) Assessment of the impact of forest harvesting operations on the physical parameters and microbiological components on a Mediterranean sandy soil in an Italian stone pine stand. Eur J Forest Res 136:205–215CrossRefGoogle Scholar
  13. Canarche A, Vintila I, Munteanu I (eds) (2006) Elsevier’s dictionary of soil science. ElsevierGoogle Scholar
  14. Castaño C, Alday JG, Lindahl BD, de Aragón JM, de Migual S, Colinas C, Parladé J, Pera J, Bonet JA (2018) Lack of thinning effects over inter-annual changes in soil fungal community and diversity in a Mediterranean pine forest. For Ecol Manag 424:420–427CrossRefGoogle Scholar
  15. Chodak M, Niklińska M, Śliwińska E (2011) Chemical and microbial properties of sandy mine soils afforested with Scots pine and silver birch. Polish J Env Studies 20:285–291Google Scholar
  16. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  17. Clinton B, Baker C (2000) Catastrophic windthrow in the southern Appalachians: characteristics of pits and mounds and initial vegetation responses. For Ecol Manag 126:51–60CrossRefGoogle Scholar
  18. De Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microb Rev 29:795–811CrossRefGoogle Scholar
  19. Dobranic JK, Zak JC (1999) A microtiter plate procedure for evaluating fungal functional diversity. Mycologia 91:756–765CrossRefGoogle Scholar
  20. Don A, Bärwolff M, Kalbitz K, Andruschkewitsch R, Jungkunst HF, Schulze E-D (2012) No rapid soil carbon loss after a windthrow event in the High Tatra. For Ecol Manag 276:239–246CrossRefGoogle Scholar
  21. Drewnik M (2006) The effect of environmental conditions on the decomposition rate of cellulose in mountain soils. Geoderma 132:116–130CrossRefGoogle Scholar
  22. Durall DM, Gamiet S, Simard SW, Kudrna L, Sakakibara SM (2006) Effects of clearcut logging and tree species composition on the diversity and community composition of epigeous fruit bodies formed by ectomycorrhizal fungi. Can J Bot 84:966–980CrossRefGoogle Scholar
  23. Fierer N, McCain CM, Meir P, Zimmermann M, Rapp JM, Silman MR, Knight R (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92:797–804CrossRefGoogle Scholar
  24. Frąc M, Hannula SE, Bełka M, Jędryczka M (2018) Fungal biodiversity and their role in soil health. Front Microbiol 9:707.  https://doi.org/10.3389/fmicb.2018.00707 CrossRefGoogle Scholar
  25. Garland JL (1997) Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol Ecol 24:289–300CrossRefGoogle Scholar
  26. Geng Y, Dighton J, Gray D (2012) The effects of thinning and soil disturbance on enzyme activities under pitch pine soil in New Jersey Pinelands. Appl Soil Ecol 62:1–7Google Scholar
  27. Gömöryová E, Hrivnák R, Jonašová M, Ujházy K, Gömöry D (2009) Changes of the functional diversity of soil microbial community during the colonization of abandoned grassland by a forest. Appl Soil Ecol 43:191–199CrossRefGoogle Scholar
  28. Gömöryová E, Strelcová K, Fleischer P, Gömöry D (2011) Soil microbial characteristics at the monitoring plots on windthrow areas of the Tatra National Park (Slovakia): their assessment as environmental indicators. Environ Monit Assess 174:1–45CrossRefGoogle Scholar
  29. Gömöryová E, Fleischer P, Gömöry D (2014) Soil microbial community responses to windthrow disturbance in Tatra National Park (Slovakia) during the period 2006–2013. Lesnicky časopis – Forestry J 60:137–142Google Scholar
  30. Gömöryová E, Fleischer P, Pichler V, Homolák GR, Gömöry D (2017) Soil microorganisms at the windthrow plots: the effect of postdisturbance management and the time since disturbance. IForest 10:515–521CrossRefGoogle Scholar
  31. Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56CrossRefGoogle Scholar
  32. Griffiths BS, Bonkowski M, Roy J, Ritz K (2001) Functional stability, substrate utilisation and biological indicators of soils following environmental impacts. Appl Soil Ecol 16:49–61CrossRefGoogle Scholar
  33. Guidelines for Soil Description (2006) Food and Agriculture Organization of the United Nations, Rome.Google Scholar
  34. Hackett CA, Griffiths BS (1997) Statistical analysis of the time-course of Biolog substrate utilization. J Microbiol Methods 30:63–69CrossRefGoogle Scholar
  35. Haichar FZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80CrossRefGoogle Scholar
  36. Homolová Z, Soltés R, Kyselová Z, Skolek J (2011) Initial successional stages with different type of management in the Tatra National Park. In: Fleischer P, Homolova Z (eds) Studies of the Tatra National Park. TANAP, Tatranska LomnicaGoogle Scholar
  37. Huber C, Baumgarten M, Göttlein A, Rotter V (2004) Beetle attack in mountainous spruce stands of the Bavarian Forest National Park. Water Air Soil Pollut 4:391–414CrossRefGoogle Scholar
  38. Huggard DJ, Vyse A (2002) Comparing clearcutting and alternatives in a high-elevation forest: early results from Sicamous Creek. British Columbia Ministry of Forests Extension Note 63. Victoria, Canada: British Columbia Ministry of Forests.Google Scholar
  39. Ishizuka S, Tsuruta H, Murdiyarso D (2002) An intensive field study on CO2, CH4, and N2O emissions from soils at four land-use types in Sumatra, Indonesia. Glob Biogeochem Cycles 16:1049CrossRefGoogle Scholar
  40. Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–2991CrossRefGoogle Scholar
  41. Jones MD, Durall DM, Cairney JWG (2003) Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol 157:399–422CrossRefGoogle Scholar
  42. Jordan D, Ponder F, Hubbard V (2003) Effects of soil compaction, forest leaf litter and nitrogen fertilizer on two oak species and microbial activity. Appl Soil Ecol 23:33–41CrossRefGoogle Scholar
  43. Kalbitz K, Solinger S, Park J-H, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci 165:277–304CrossRefGoogle Scholar
  44. Klimek B, Niklińska M, Jaźwa M, Tarasek A, Tekielak I, Musielok Ł (2015) Covariation of soil bacteria functional diversity and vegetation diversity along an altitudinal climatic gradient in the Western Carpathians. Pedobiologia 58:105–112CrossRefGoogle Scholar
  45. Klimek B, Chodak M, Jaźwa M, Solak A, Tarasek A, Niklińska M (2016) The relationship between soil bacteria substrate utilisation patterns and the vegetation structure in temperate forests. Europ J For Res 135:179–189CrossRefGoogle Scholar
  46. Köster K, Püttsepp Ü, Pumpanen J (2011) Comparison of soil CO2 flux between uncleared and cleared windthrow areas in Estonia and Latvia. For Ecol Manage 262:65–70Google Scholar
  47. Kreutzweiser DP, Hazlett PW, Gunn JM (2008) Logging impacts on the biogeochemistry of boreal forest soils and nutrient export to aquatic systems: a review. Environ Rev 16:157–179CrossRefGoogle Scholar
  48. Kruskal JB (1964) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27CrossRefGoogle Scholar
  49. Kulmala L, Aaltonen H, Berninger F, Kieloaho AJ, Levula J, Bäck J, Hari P, Kolari P, Korhonen FJ, Kulmala M, Nikinmaa E, Pihlatie M, Vesala T, Pumpanen J (2014) Changes in biogeochemistry and carbon fluxes in a boreal forest after the clear-cutting and partial burning of slash. Agricultural For Meteo 188:33–44CrossRefGoogle Scholar
  50. Kuo S (1996) Phosphorus. In: Methods of soil analysis. Part 3. Chemical methods. Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (eds.) SSSA-ASA, Madison, Wisconsin.Google Scholar
  51. Laskowski R, Niklińska M, Nycz-Wasilec P, Wójtowicz M, Weiner J (2003) Variance components of the respiration rate and chemical characteristics of soil organic layers in Niepołomice Forest, Poland. Biogeochem 64:149–163CrossRefGoogle Scholar
  52. Legout A, Nys C, Picard J-F, Turpault M-P, Dambrine E (2009) Effects of storm Lothar (1999) on the chemical composition of soil solutions and on herbaceous cover, humus and soils (Fougéres, France). For Ecol Manag 257:800–811CrossRefGoogle Scholar
  53. León-Sánchez L, Nicolás E, Goberna M, Prieto, I, Maestre FT, Querejeta JI (2017) Poor plant performance under simulated climate change is linked to mycorrhizal responses in a semi-arid shrubland. J Ecol 1–17Google Scholar
  54. Likens GE (2013) Biogeochemistry of a forested ecosystem. Springer Science & Business, New YorkCrossRefGoogle Scholar
  55. Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi—potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–1447CrossRefGoogle Scholar
  56. Liu CP, Sheu BH (2003) Dissolved organic carbon in precipitation, throughfall, stemflow, soil solution and stream water at the Guandaushi subtropical forest in Taiwan. For Ecol Manag 172:315–325CrossRefGoogle Scholar
  57. Lu N, Chen S, Wilske B, Sun G, Chen J (2011) Evapotranspiration and soil water relationships in a range of disturbed and undisturbed ecosystems in the semi-arid Inner Mongolia, China. J Plant Ecol 4:49–60CrossRefGoogle Scholar
  58. Myczkowski S, Jagiełło Z, Larendowicz Z, Skawiński P (1985) Mapa drzewostanów 1:50000. In: Atlas of the Tatra NP. Trafas K (eds.) TPN-PTPNoZ, Kraków.Google Scholar
  59. Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships. Eur J Soil Sci 62:105–116CrossRefGoogle Scholar
  60. Norton JM, Firestone MK (1991) Metabolic status of bacteria and fungi in the rhizosphere of Ponderosa pine seedlings. Appl Environ Microbiol 57:1161–1167Google Scholar
  61. Nüsslein K, Tiedje JM (1999) Soil bacterial community shift correlated with change from forest to pasture vegetation in a tropical soil. Appl Environ Microbiol 65:3622–3626Google Scholar
  62. Pennock DJ (2004) Designing field studies in soil science. Can J Soil Sci 84:1–10CrossRefGoogle Scholar
  63. Peterken GF (1996) Natural woodland, ecology and conservation in northern temperate regions. Cambridge University Press, CambridgeGoogle Scholar
  64. Phillips LA, Ward V, Jones MD (2014) Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests. ISME J 8:699–713CrossRefGoogle Scholar
  65. Phoenix GK, Leake JR, Read DJ, Grime JP, Lee JA (2004) Accumulation of pollutant nitrogen in calcareous and acidic grasslands: evidence from N flux and 15N tracer studies. Water Air Soil Poll Focus 4:159–167CrossRefGoogle Scholar
  66. Piotrowska K, Danel W, Iwanow A, Gaździcka E, Rączkowski W, Bezák V, Maglay J, Polák M, Kohút M, Gross P (2015) Geology. In: Dabrowska K, Guzik M (eds) Atlas of the Tatra Mts. TPN, ZakopaneGoogle Scholar
  67. Ponge JF, Jabiol B, Gégout JC (2011) Geology and climate conditions affect more humus forms than forest canopies at large scale in temperate forests. Geoderma 162:187–195CrossRefGoogle Scholar
  68. Preston-Mafham J, Boddy L, Randerson PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles—a critique. FEMS Microbiol Ecol 42:1–14Google Scholar
  69. Rusch S, Hagedorn F, Zimmermann S, Luscher P (2009) Bodenkohlenstoffnach Windwurf – eine CO2-Quelle? Swiss Federal Institute for Forest Snow and Landscape Research (WSL)/Swiss Federal Office for the Environment.Google Scholar
  70. Schaetzl RJ, Johnson DL, Burns SF, Small TW (1989) Tree uprooting: review of terminology, process, and environmental implications. Can J For Res 19:1–11CrossRefGoogle Scholar
  71. Schlichting E, Blume HP (1966) Bodenkundliches Praktikum. Parey P, HamburgGoogle Scholar
  72. Setälä H, McLean MA (2004) Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi. Oecologia 139:98–107CrossRefGoogle Scholar
  73. Settineri G, Mallamaci C, Mitrović M, Sidari M, Muscolo A (2018) Effects of different thinning intensities on soil carbon storage in Pinus laricio forest of Apennine South Italy. Eur J For Res 137:131–141CrossRefGoogle Scholar
  74. Smykla J, Drewnik M, Szarek-Gwiazda E, Hii YS, Knap W, Emslie SD (2015) Variation in the characteristics and development of soils at Edmonson Point due to abiotic and biotic factors, northern Victoria Land, Antarctica. Catena 132:56–67CrossRefGoogle Scholar
  75. Steenwerth KL, Jackson LE, Calderón FJ, Stromberg MR, Scow KM, Caldero FJ (2002) Soil microbial community composition and land use history in cultivated and grassland ecosystems of coastal California. Soil Biol Biochem 34:1599–1611CrossRefGoogle Scholar
  76. Taylor DL, Sinsabaugh RL (2015) The soil fungi: occurrence, phylogeny and ecology. In: Paul EA (ed) Soil microbiology, ecology and biochemistry, 4th edn. ElsevierGoogle Scholar
  77. Thomas GW (1996) Soil pH and soil acidity. In: Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour P, Tabatabai MA, Johnston CT, Sumner ME (eds) Methods of soil analysis, part 3, chemical methods. SSSA-ASA, Madison, WisconsinGoogle Scholar
  78. Ulanova NG (2000) The effects of windthrow on forests at different spatial scales: a review. For Ecol Manag 135:155–167CrossRefGoogle Scholar
  79. Usbeck T, Wohlgemuth T, Dobbertin M, Pfister C, Burgi A, Robertez M (2010) Increasing storm damage to forests in Switzerland from 1858 to 2007. Agric For Meteorol 150:47–55CrossRefGoogle Scholar
  80. Ustrnul Z, Walawender E, Czekierda D, Štástný P, Lapin M, Mikulová K (2015) Precipitation and snow cover. In: Dabrowska K, Guzik M (eds) Atlas of the Tatra Mts. TPN, ZakopaneGoogle Scholar
  81. Van Miegroet H, Olsson M (2011) Ecosystem disturbance and soil organic carbon—a review. Soil Carbon in Sensitive European Ecosystems. John Wiley & Sons, Ltd.Google Scholar
  82. Vargas R, Hasselquist N, Allen EB, Allen MF (2010) Effects of hurricane disturbance on aboveground forest structure, arbuscular mycorrhizae and belowground carbon in restored tropical forest. Ecosystems 13:118–128CrossRefGoogle Scholar
  83. Wasak K, Drewnik M (2012) Properties of humus horizons of soils developed in the lower montane belt in the Tatra Mountains. Pol J Soil Sci 45:57–68Google Scholar
  84. Wasak K, Drewnik M (2015) Land use effects on soil organic carbon sequestration in calcareous Leptosols in former pastureland—a case study from the Tatra Mountains (Poland). Solid Earth 6:1103–1115CrossRefGoogle Scholar
  85. Wilczynski CJ, Pickett STA (1993) Fine root biomass within experimental canopy gaps: evidence for a below-ground gap. J Veg Sci 4:571–574CrossRefGoogle Scholar
  86. Withlington CL, Stanford RL Jr (2007) Decomposition rate of buried substrate increase with altitude in the forest-alpine tundra ecotone. Soil Biol Biochem 39:68–75CrossRefGoogle Scholar
  87. Wolińska A, Frąc M, Oszust K, Szafranek-Nakonieczna A, Zielenkiewicz U, Stępniewska Z (2017) Microbial biodiversity of meadows under different modes of land use: catabolic and genetic fingerprinting. World J Microbiol Biotechnol 33(8):154.  https://doi.org/10.1007/s11274-017-2318-2 CrossRefGoogle Scholar
  88. Yao W, Bowman D, Shi W (2006) Soil microbial community structure and diversity in a turfgrass chronosequence: land-use change versus turfgrass management. Appl Soil Ecol 34:209–218CrossRefGoogle Scholar
  89. Yeakley JA, Coleman DC, Haines BL, Kloeppel BD, Meyer JL, Swank WT, Argo BW, Deal JM, Taylor SF (2003) Hillslope nutrient dynamics following upland riparian vegetation disturbance. Ecosystems 6:154–167CrossRefGoogle Scholar
  90. Zak JC, Willig MR, Moorhead DL, Wildmand HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26:1101–1108CrossRefGoogle Scholar
  91. Zech W, Guggenberger G, Haumaier L, Pöhhacker R, Schäfer D, Amelung W, Miltner A, Kaiser K, Ziegler F (1996) Organic matter dynamics in forest soils of temperate and tropical ecosystems. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, AmsterdamGoogle Scholar
  92. Żmudzka E, Nejedlík P, Mikulová K (2015) Temperature, thermal indices. In: Guzik M (ed) Dąbrowska K. Atlas of the Tatra Mts. TPN, ZakopaneGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Geography and Spatial OrganizationPolish Academy of ScienceKrakówPoland
  2. 2.Institute of Environmental Sciences, Faculty of Biology and Earth SciencesJagiellonian UniversityKrakówPoland
  3. 3.Institute of Geography and Spatial Management, Faculty of Geography and GeologyJagiellonian UniversityKrakówPoland

Personalised recommendations