Advertisement

Plant and Soil

, Volume 380, Issue 1–2, pp 57–72 | Cite as

Soil nutrients and microbial biomass in three contrasting Mediterranean forests

  • Cristina AponteEmail author
  • Luis Matías
  • Victoria González-Rodríguez
  • Jorge Castro
  • Luis V. García
  • Rafael Villar
  • Teodoro Marañón
Regular Article

Abstract

Aims

The extent to which the spatial and temporal patterns of soil microbial and available nutrient pools hold across different Mediterranean forest types is unclear impeding the generalization needed to consolidate our understanding on Mediterranean ecosystems functioning.

Methods

We explored the response of soil microbial, total, organic and inorganic extractable nutrient pools (C, N and P) to common sources of variability, namely habitat (tree cover), soil depth and season (summer drought), in three contrasting Mediterranean forest types: a Quercus ilex open woodland, a mixed Q. suber and Q. canariensis woodland and a Pinus sylvestris forest.

Results

Soil microbial and available nutrient pools were larger beneath tree cover than in open areas in both oak woodlands whereas the opposite trend was found in the pine forest. The greatest differences in soil properties between habitat types were found in the open woodland. Season (drought effect) was the main driver of variability in the pine forest and was related to a loss of microbial nutrients (up to 75 % loss of Nmic and Pmic) and an increase in microbial ratios (Cmic/Nmic, Cmic/Pmic) from Spring to Summer in all sites. Nutrient pools consistently decreased with soil depth, with microbial C, N and P in the top soil being up to 208 %, 215 % and 274 % larger than in the deeper soil respectively.

Conclusions

Similar patterns of variation emerged in relation to season and soil depth across the three forest types whereas the direction and magnitude of the habitat (tree cover) effect was site-dependent, possibly related to the differences in tree species composition and forest structure, and thus in the quality and distribution of the litter input.

Keywords

Soil fertility Plant-soil interactions Soil carbon Nitrogen Phosphorus 

Notes

Acknowledgments

We thank the Consejería de Medio Ambiente (Andalusian Government) and the Direction of the Los Alcornocales Natural Park, Sierra de Cardeña and Montoro Natural Park and Sierra Nevada National Park for the facilities and support to carry out our field work. We are grateful to Susana Hitos, Eduardo Gutiérrez, Carlos Ros, Raquel Casado, Nacho Villegas, Ramón Ruiz and Eulogio Corral for field and lab assistance. This study was supported by the coordinated Spanish MEC Projects DINAMED (CGL2005-05830-C03), INTERBOS (CGL2008- 4503-C03-01), and DIVERBOS (CGL2011-30285-C02), the Andalusian Projects GESBOME (P06-RNM-1890) and ANASINQUE (PE2010-RNM5782), the Life + Biodehesa project (11/BIO/ES/000726), three FPI-MEC predoctoral fellowships to CA, LM and VGR, the Subprograma de Técnicos de Apoyo MICINN (PTA2009-1782-I), a MECD postdoctoral grant E-28-2012-0934030 to CA and a EU Marie Curie fellowship (FP7-2011-IEF-300825) to LM.

Supplementary material

11104_2014_2061_MOESM1_ESM.docx (44 kb)
ESM 1 (DOCX 44 kb)

References

  1. Alameda D, Villar R, Iriondo JM (2012) Spatial pattern of soil compaction: trees’ footprint on soil physical properties. For Ecol Manag 283:128–137. doi: 10.1016/j.foreco.2012.07.018 CrossRefGoogle Scholar
  2. Aponte C, García LV, Marañón T, Gardes M (2010a) Indirect host effect on ectomycorrhizal fungi: leaf fall and litter quality explain changes in fungal communities on the roots of co-occurring Mediterranean oaks. Soil Biol Biochem 42:788–796. doi: 10.1016/j.soilbio.2010.01.014 CrossRefGoogle Scholar
  3. Aponte C, Marañón T, García LV (2010b) Microbial C, N and P in soils of Mediterranean oak forests: influence of season, canopy cover and soil depth. Biogeochemistry 101:77–92. doi: 10.1007/s10533-010-9418-5 CrossRefGoogle Scholar
  4. Aponte C, García LV, Pérez-Ramos IM, Gutiérrez E, Marañón T (2011) Oak trees and soil interactions in Mediterranean forests: a positive feedback model. J Veg Sci 22:856–867. doi: 10.1111/j.1654-1103.2011.01298.x CrossRefGoogle Scholar
  5. Aponte C, García L, Marañón T (2013) Tree species effects on nutrient cycling and soil biota: a feedback mechanism favouring species coexistence. For Ecol Manag 309:36–46. doi: 10.1016/j.foreco.2013.05.035 CrossRefGoogle Scholar
  6. Augusto L, Ranger J, Binkley D, Rothe A (2002) Impact of several common tree species of European temperate forests on soil fertility. Ann For Sci 59:233–253. doi: 10.1051/forest:2002020 CrossRefGoogle Scholar
  7. Barcenas-Moreno G, Garcia-Orenes F, Mataix-Solera J, Mataix-Beneyto J, Baath E (2011) Soil microbial recolonisation after a fire in a Mediterranean forest. Biol Fertil Soils 47:261–272. doi: 10.1007/s00374-010-0532-2 CrossRefGoogle Scholar
  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300Google Scholar
  9. Bennett LT, Kasel S, Tibbits J (2009) Woodland trees modulate soil resources and conserve fungal diversity in fragmented landscapes. Soil Biol Biochem 41:2162–2169. doi: 10.1016/j.soilbio.2009.07.030 CrossRefGoogle Scholar
  10. Bohlen PJ, Groffman PM, Driscoll CT, Fahey TJ, Siccama TG (2001) Plant-soil-microbial interactions in a northern hardwood forest. Ecology 82:965–978Google Scholar
  11. Bray RH, Kurtz LT (1945) Determination of total, organic and available forms of phosphorous in soils. Soil Sci 59:39–45. doi: 10.1097/00010694-194501000-00006 CrossRefGoogle Scholar
  12. Bremner J, Keeney D (1965) Steam distillation methods for determination of ammonium nitrate and nitrate. Anal Chim Acta 32:485–495. doi: 10.1016/S0003-2670(00)88973-4 CrossRefGoogle Scholar
  13. Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial phosphorus in soil. Soil Biol Biochem 14:319–329CrossRefGoogle Scholar
  14. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. doi: 10.1016/0038-0717(85)90144-0 CrossRefGoogle Scholar
  15. Carreira JA, Niell FX, Lajtha K (1994) Soil nitrogen availability and nitrification in Mediterranean shrublands of varying fire history and successional stage. Biogeochemistry 26:189–209. doi: 10.1007/bf00002906 CrossRefGoogle Scholar
  16. Chen CR, Xu ZH, Blumfield TJ, Hughes JM (2003) Soil microbial biomass during the early establishment of hoop pine plantation: seasonal variation and impacts of site preparation. For Ecol Manag 186:213–225. doi: 10.1016/S0378-1127(03)00275-5 CrossRefGoogle Scholar
  17. Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252. doi: 10.1007/s10533-007-9132-0 CrossRefGoogle Scholar
  18. Corre MD, Schnabel RR, Stout WL (2002) Spatial and seasonal variation of gross nitrogen transformations and microbial biomass in a Northeastern US grassland. Soil Biol Biochem 34:445–457. doi: 10.1016/S0038-0717(01)00198-5 CrossRefGoogle Scholar
  19. Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Systems:1695Google Scholar
  20. Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183. doi: 10.1016/S0169-5347(02)02496-5 CrossRefGoogle Scholar
  21. Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176. doi: 10.1016/S0038-0717(02)00251-1 CrossRefGoogle Scholar
  22. Gallardo A (2003) Effect of tree canopy on the spatial distribution of soil nutrients in a Mediterranean Dehesa. Pedobiologia 47:117–125. doi: 10.1078/0031-4056-00175 CrossRefGoogle Scholar
  23. Gallardo A, Schlesinger WH (1994) Factors limiting microbial biomass in the mineral soil and forest floor of a warm-temperate forest. Soil Biol Biochem 26:1409–1415. doi: 10.1016/0038-0717(94)90225-9 CrossRefGoogle Scholar
  24. Gallardo A, Rodríguez-Saucedo JJ, Covelo F, Fernández-Alés R (2000) Soil nitrogen heterogeneity in a Dehesa ecosystem. Plant Soil 222:71–82CrossRefGoogle Scholar
  25. García LV (2003) Controlling the false discovery rate in ecological research. Trends Ecol Evol 18:553–554. doi: 10.1016/j.tree.2003.08.011 CrossRefGoogle Scholar
  26. García C, Hernandez T, Roldan A, Martin A (2002) Effect of plant cover decline on chemical and microbiological parameters under Mediterranean climate. Soil Biol Biochem 34:635–642. doi: 10.1016/S0038-0717(01)00225-5 CrossRefGoogle Scholar
  27. García LV, Maltez-Mouro S, Pérez-Ramos IM, Freitas H, Marañón T (2006) Counteracting gradients of light and soil nutrients in the understorey of Mediterranean oak forest. Web Ecol 6:67–74. doi: 10.5194/we-6-67-2006 CrossRefGoogle Scholar
  28. Gaudinski JB, Trumbore SE, Davidson EA, Zheng S (2000) Soil carbon cycling in a temperate forest: radiocarbon-based estimates of residence times, sequestration rates and partitioning of fluxes. Biogeochemistry 51:33–69CrossRefGoogle Scholar
  29. Gil Torres J, Rodero Pérez I, Odierna C (2003) Inventario de los suelos de la provincia de Cordoba. Diputacion de Cordoba, SpainGoogle Scholar
  30. Goberna M, Sánchez J, Pascual JA, García C (2006) Surface and subsurface organic carbon, microbial biomass and activity in a forest soil sequence. Soil Biol Biochem 38:2233–2243. doi: 10.1016/j.soilbio.2006.02.003 CrossRefGoogle Scholar
  31. Goberna M, Pascual JA, García C, Sánchez J (2007) Do plant clumps constitute microbial hotspots in semiarid Mediterranean patchy landscapes? Soil Biol Biochem 39:1047–1054. doi: 10.1016/j.soilbio.2006.11.015 CrossRefGoogle Scholar
  32. Hackl E, Pfeffer M, Donat C, Bachmann G, Zechmeister-Boltenstern S (2005) Composition of the microbial communities in the mineral soil under different types of natural forest. Soil Biol Biochem 37:661–671. doi: 10.1016/j.soilbio.2004.08.023 CrossRefGoogle Scholar
  33. Hassink J (1994) Effect of soil texture on the size of the microbial biomass and on the amount of c and n mineralized per unit of microbial biomass in dutch grassland soils. Soil Biol Biochem 26:1573–1581. doi: 10.1016/0038-0717(94)90100-7 CrossRefGoogle Scholar
  34. Huang Z, Wan X, He Z, Yu Z, Wang M, Hu Z, Yang Y (2013) Soil microbial biomass, community composition and soil nitrogen cycling in relation to tree species in subtropical China. Soil Biol Biochem 62:68–75. doi: 10.1016/j.soilbio.2013.03.008 CrossRefGoogle Scholar
  35. Insam H, Parkinson D, Domsch KH (1989) Influence of macroclimate on soil microbial biomass. Soil Biol Biochem 21:211–221. doi: 10.1016/0038-0717(89)90097-7 CrossRefGoogle Scholar
  36. Jensen KD, Beier C, Michelsen A, Emmett BA (2003) Effects of experimental drought on microbial processes in two temperate heathlands at contrasting water conditions. Appl Soil Ecol 24:165–176. doi: 10.1016/S0929-1393(03)00091-X CrossRefGoogle Scholar
  37. King JR, Jackson DA (1999) Variable selection in large environmental data sets using principal components analysis. Environmetrics 10:67–77. doi: 10.1002/(SICI)1099-095X(199901/02)10:1%3C67::AID-ENV336%3E3.0.CO;2-0 CrossRefGoogle Scholar
  38. Kozlowski TT, Pallardi SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334. doi: 10.1663/0006-8101(2002)068%5B0270:AAAROW%5D2.0.CO;2 CrossRefGoogle Scholar
  39. Lambers H, Chapin F III, Pons T (1998) Plant physiological ecology. Springer, New YorkCrossRefGoogle Scholar
  40. Lindo Z, Visser S (2003) Microbial biomass, nitrogen and phosphorus mineralization, and mesofauna in boreal conifer and deciduous forest floors following partial and clear-cut harvesting. Can J For Res 33:1610–1620. doi: 10.1139/x03-080 CrossRefGoogle Scholar
  41. Liu L, Gundersen P, Zhang T, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38. doi: 10.1016/j.soilbio.2011.08.017 CrossRefGoogle Scholar
  42. Lucas-Borja ME, Candel D, Jindo K, Moreno JL, Andrés M, Bastida F (2012) Soil microbial community structure and activity in monospecific and mixed forest stands, under Mediterranean humid conditions. Plant Soil 354:359–370. doi: 10.1007/s11104-011-1072-8 CrossRefGoogle Scholar
  43. Malchair S, Carnol M (2009) Microbial biomass and C and N transformations in forest floors under European beech, sessile oak, Norway spruce and Douglas-fir at four temperate forest sites. Soil Biol Biochem 41:831–839. doi: 10.1016/j.soilbio.2009.02.004 CrossRefGoogle Scholar
  44. Maltez-Mouro S, García L, Marañón T, Freitas H (2005) The combined role of topography and overstorey tree composition in promoting edaphic and floristic variation in a Mediterranean forest. Ecol Res 20:668–677. doi: 10.1007/s11284-005-0081-6 CrossRefGoogle Scholar
  45. Marañón-Jiménez S, Castro J, Kowalski AS, Serrano-Ortiz P, Reverter BR, Sánchez-Cañete EP, Zamora R (2011) Post-fire soil respiration in relation to burnt wood management in a Mediterranean mountain ecosystem. For Ecol Manag 261:1436–1447. doi: 10.1016/j.foreco.2011.01.030 CrossRefGoogle Scholar
  46. Matías L, Castro J, Zamora R (2011) Soil-nutrient availability under a global-change scenario in a Mediterranean mountain ecosystem. Glob Chang Biol 17:1646–1657. doi: 10.1111/j.1365-2486.2010.02338.x CrossRefGoogle Scholar
  47. Monokrousos N, Papatheodorou EM, Diamantopoulos JD, Stamou GP (2004) Temporal and spatial variability of soil chemical and biological variables in a Mediterranean shrubland. For Ecol Manag 202:83–91. doi: 10.1016/j.foreco.2004.07.039 CrossRefGoogle Scholar
  48. Nadelhoffer KJ, Giblin AE, Shaver GR, Laundre JA (1991) Effects of temperature and substrate quality on element mineralization in six arctic soils. Ecology 72:242–253. doi: 10.2307/1938918 CrossRefGoogle Scholar
  49. Nielsen PL, Andresen LC, Michelsen A, Schmidt IK, Kongstad J (2009) Seasonal variations and effects of nutrient applications on N and P and microbial biomass under two temperate heathland plants. Appl Soil Ecol 42:279–287. doi: 10.1016/j.apsoil.2009.05.006 CrossRefGoogle Scholar
  50. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) In: USDA (ed) Estimation of available phosphorous in soils by extraction with sodium bicarbonate. USDA, WashingtonGoogle Scholar
  51. Polo A (2006) Heterogeneidad edáfica en una parcela experimental de bosque mixto de Quercus suber y Quercus canariensis del Parque Natural de los Alcornocales (La Panera). Escuela Universitaria Ingenieros Técnicos Agrícolas. Universidad de Sevilla, SevilleGoogle Scholar
  52. Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. For Ecol Manag. doi: 10.1016/j.foreco.2013.02.034 Google Scholar
  53. Quilchano C, Marañón T (2002) Dehydrogenase activity in Mediterranean forest soils. Biol Fertil Soils 35:102. doi: 10.1007/s00374-002-0446-8 CrossRefGoogle Scholar
  54. Raubuch M, Joergensen RG (2002) C and net N mineralisation in a coniferous forest soil: the contribution of the temporal variability of microbial biomass C and N. Soil Biol Biochem 34:841–849. doi: 10.1016/S0038-0717(02)00016-0 CrossRefGoogle Scholar
  55. Rey A, Pegoraro E, Tedeschi V, De Parri I, Jarvis PG, Valentini R (2002) Annual variation in soil respiration and its components in a coppice oak forest in Central Italy. Glob Chang Biol 8:851–866. doi: 10.1046/j.1365-2486.2002.00521.x CrossRefGoogle Scholar
  56. Ross DJ, Tate KR, Feltham CW (1996) Microbial biomass, and C and N mineralization, in litter and mineral soil of adjacent montane ecosystems in a southern beech (Nothofagus) forest and a tussock grassland. Soil Biol Biochem 28:1613–1620. doi: 10.1016/S0038-0717(96)00255-6 CrossRefGoogle Scholar
  57. Rutigliano FA, D’Ascoli R, Virzo De Santo A (2004) Soil microbial metabolism and nutrient status in a Mediterranean area as affected by plant cover. Soil Biol Biochem 36:1719–1729. doi: 10.1016/j.soilbio.2004.04.029 CrossRefGoogle Scholar
  58. Sagova-Mareckova M, Omelka M, Cermak L, Kamenik Z, Olsovska J, Hackl E, Kopecky J, Hadacek F (2011) Microbial communities show parallels at sites with distinct litter and soil characteristics. Appl Environ Microbiol 77:7560–7567. doi: 10.1128/AEM.00527-11 PubMedCentralPubMedCrossRefGoogle Scholar
  59. Sardans J, Peñuelas J, Rodà F (2005) Changes in nutrient status, retranslocation and use efficiency in young post-fire regeneration Pinus halepensis in response to sudden N and P input, irrigation and removal of competing vegetation. Trees 19(19):233–250. doi: 10.1007/s00468-004-0374-3 CrossRefGoogle Scholar
  60. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. doi: 10.1890/06-0219 PubMedCrossRefGoogle Scholar
  61. Schmidt IK, Jonasson S, Michelsen A (1999) Mineralization and microbial immobilization of N and P in arctic soils in relation to season, temperature and nutrient amendment. Appl Soil Ecol 11:147–160. doi: 10.1016/S0929-1393(98)00147-4 CrossRefGoogle Scholar
  62. Singh JS, Raghubanshi AS, Singh RS, Srivastava SC (1989) Microbial biomass acts as a source of plant nutrients in dry tropical forest and savanna. Nature 338:499–500. doi: 10.1038/338499a0 CrossRefGoogle Scholar
  63. Smolander A, Kitunen V (2002) Soil microbial activities and characteristics of dissolved organic C and N in relation to tree species. Soil Biol Biochem 34:651–660. doi: 10.1016/S0038-0717(01)00227-9 CrossRefGoogle Scholar
  64. Sparks DL (1996) Methods of soil analysis. Part 3. Chemical Methods Soil Science Society of America and American Society of Agronomy, MadisonGoogle Scholar
  65. Sparling GP (1992) Ratio of microbial biomass carbon to soil organic carbon as a sensitive indicator of changes in soil organic matter. Soil Res 30:195–207. doi: 10.1071/SR9920195 CrossRefGoogle Scholar
  66. Ste-Marie C, Pare D, Gagnon D (2007) The contrasting effects of aspen and jack pine on soil nutritional properties depend on parent material. Ecosystems 10:1299–1310. doi: 10.1007/s10021-007-9098-8 CrossRefGoogle Scholar
  67. Thoms C, Gattinger A, Jacob M, Thomas FM, Gleixner G (2010) Direct and indirect effects of tree diversity drive soil microbial diversity in temperate deciduous forest. Soil Biol Biochem 42:1558–1565. doi: 10.1016/j.soilbio.2010.05.030 CrossRefGoogle Scholar
  68. Ushio M, Kitayama K, Balser TC (2010) Tree species-mediated spatial patchiness of the composition of microbial community and physicochemical properties in the topsoils of a tropical montane forest. Soil Biol Biochem 42:1588–1595. doi: 10.1016/j.soilbio.2010.05.035 CrossRefGoogle Scholar
  69. van der Putten W, Bardgett R, de Ruiter P, Hol W, Meyer K, Bezemer T, Bradford M, Christensen S, Eppinga M, Fukami T, Hemerik L, Molofsky J, Schädler M, Scherber C, Strauss S, Vos M, Wardle D (2009) Empirical and theoretical challenges in aboveground–belowground ecology. Oecologia 161:1–14. doi: 10.1007/s00442-009-1351-8 PubMedCentralPubMedCrossRefGoogle Scholar
  70. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. doi: 10.1016/0038-0717(87)90052-6 CrossRefGoogle Scholar
  71. Wang FE, Chen YX, Tian GM, Kumar S, He YF, Fu QL, Lin Q (2004) Microbial biomass carbon, nitrogen and phosphorus in the soil profiles of different vegetation covers established for soil rehabilitation in a red soil region of southeastern China. Nutr Cycl Agroecosyst 68:181–189. doi: 10.1023/B:FRES.0000017470.14789.2a CrossRefGoogle Scholar
  72. Wilkinson SC, Anderson JM, Scardelis SP, Tisiafouli M, Taylor A, Wolters V (2002) PLFA profiles of microbial communities in decomposing conifer litters subject to moisture stress. Soil Biol Biochem 34:189–200. doi: 10.1016/S0038-0717(01)00168-7 CrossRefGoogle Scholar
  73. WRB IWG (2006) In: FAO (ed) World reference base for soil resources 2006: a framework for international classification, correlation and communication. World Soil Resources Reports No 103, RomeGoogle Scholar
  74. Xiang SR, Doyle A, Holden PA, Schimel JP (2008) Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils. Soil Biol Biochem 40:2281–2289. doi: 10.1016/j.soilbio.2008.05.004 CrossRefGoogle Scholar
  75. Zhong Z, Makeschin F (2006) Differences of soil microbial biomass and nitrogen transformation under two forest types in Central Germany. Plant Soil 283:287–297. doi: 10.1007/s11104-006-0018-z CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Cristina Aponte
    • 1
    • 2
    Email author
  • Luis Matías
    • 3
    • 4
  • Victoria González-Rodríguez
    • 5
  • Jorge Castro
    • 3
  • Luis V. García
    • 1
  • Rafael Villar
    • 5
  • Teodoro Marañón
    • 1
  1. 1.Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSICSevillaSpain
  2. 2.Department of Forest and Ecosystem ScienceThe University of MelbourneRichmondAustralia
  3. 3.Grupo de Ecología Terrestre, Dpto. de Ecología, Facultad de CienciasUniversidad de GranadaGranadaSpain
  4. 4.Biological and Environmental Sciences, School of Natural SciencesUniversity of StirlingStirlingUK
  5. 5.Área de Ecología, Campus de RabanalesUniversidad de CórdobaCórdobaSpain

Personalised recommendations