Skip to main content
Log in

Soil nutrients and microbial biomass in three contrasting Mediterranean forests

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

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.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bohlen PJ, Groffman PM, Driscoll CT, Fahey TJ, Siccama TG (2001) Plant-soil-microbial interactions in a northern hardwood forest. Ecology 82:965–978

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial phosphorus in soil. Soil Biol Biochem 14:319–329

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Systems:1695

    Google Scholar 

  • Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183. doi:10.1016/S0169-5347(02)02496-5

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gallardo A, Rodríguez-Saucedo JJ, Covelo F, Fernández-Alés R (2000) Soil nitrogen heterogeneity in a Dehesa ecosystem. Plant Soil 222:71–82

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 51:33–69

    Article  Google Scholar 

  • Gil Torres J, Rodero Pérez I, Odierna C (2003) Inventario de los suelos de la provincia de Cordoba. Diputacion de Cordoba, Spain

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lambers H, Chapin F III, Pons T (1998) Plant physiological ecology. Springer, New York

    Book  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) In: USDA (ed) Estimation of available phosphorous in soils by extraction with sodium bicarbonate. USDA, Washington

    Google Scholar 

  • 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, Seville

    Google Scholar 

  • 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 

  • Quilchano C, Marañón T (2002) Dehydrogenase activity in Mediterranean forest soils. Biol Fertil Soils 35:102. doi:10.1007/s00374-002-0446-8

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sparks DL (1996) Methods of soil analysis. Part 3. Chemical Methods Soil Science Society of America and American Society of Agronomy, Madison

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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, Rome

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cristina Aponte.

Additional information

Responsible Editor: Zucong Cai.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 44 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aponte, C., Matías, L., González-Rodríguez, V. et al. Soil nutrients and microbial biomass in three contrasting Mediterranean forests. Plant Soil 380, 57–72 (2014). https://doi.org/10.1007/s11104-014-2061-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-014-2061-5

Keywords

Navigation