, Volume 101, Issue 1–3, pp 77–92 | Cite as

Microbial C, N and P in soils of Mediterranean oak forests: influence of season, canopy cover and soil depth

  • Cristina AponteEmail author
  • Teodoro Marañón
  • Luis V. García


In Mediterranean ecosystems the effect of aboveground and belowground environmental factors on soil microbial biomass and nutrient immobilization-release cycles may be conditioned by the distinctive seasonal pattern of the Mediterranean-type climates. We studied the effects of season, canopy cover and soil depth on microbial C, N and P in soils of two Mediterranean forests using the fumigation-extraction procedure. Average microbial values recorded were 820 μg C g−1, 115 μg N g−1 and 19 μg P g−1, which accounted for 2.7, 4.7 and 8.8% of the total pools in the surface soil, respectively. Microbial N and P pools were about 10 times higher than the inorganic N and P fractions available for plants. Microbial C values differed between forest sites but in each site they were similar across seasons. Both microbial and inorganic N and P showed maximum values in spring and minimum values in summer, which were positively correlated with soil moisture. Significant differences in soil microbial properties among canopy cover types were observed in the surface soil but only under favourable environmental conditions (spring) and not during summer. Soil depth affected microbial contents which decreased twofold from surface to subsurface soil. Microbial nutrient ratios (C/N, C/P and N/P) varied with seasons and soil depth. Soil moisture regime, which was intimately related to seasonality, emerged as a potential key factor for microbial biomass growth in the studied forests. Our research shows that under a Mediterranean-type climate the interaction among season, vegetation type and structure and soil properties affect microbial nutrient immobilization and thus could influence the biogeochemical cycles of C, N and P in Mediterranean forest ecosystems.


Microbial biomass Nitrogen Nutrient immobilization Phosphorus Plant–soil interactions Seasonal dynamics Vegetation cover 



We thank the Consejería de Medio Ambiente (Andalusian Government) and Marco Antonio Tena, then Director of Los Alcornocales Natural Park, for the facilities and support to carry out our field work. We are grateful to Eduardo Gutiérrez, Carlos Ros and Susana Hito for field and lab assistance and to Jorge Castro for introducing us to soil microbial ecology. This study was supported by a FPI-MEC grant to CA, by the Spanish MEC projects Dinamed (CGL2005-5830-C03-01), and Interbos (CGL2008-4503-C03-01), the Andalusian GESBOME Project (RNM 1890), and the European FEDER funds. This research is part of the Globimed ( network in forest ecology.


  1. Anderson JPE, Domsch KH (1980) Quantities of plant nutrients in the microbial biomass of selected soils. Soil Sci 130:211–216CrossRefGoogle Scholar
  2. 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 59:233–253CrossRefGoogle Scholar
  3. Balser TC, Firestone MK (2005) Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry 73:395–415CrossRefGoogle Scholar
  4. Bates BC, Kundzewicz ZW, Wu S, Palutikof JP (eds) (2008) Climate change and water, technical paper of the intergovernmental panel on climate change. IPCC Secretariat, GenevaGoogle Scholar
  5. Billore SK, Ohsawa M, Numata M, Okano S (1995) Microbial biomass nitrogen pool in soils from a warm temperate grassland, and from deciduous and evergreen forests in Chiba, central Japan. Biol Fertil Soils 19:124–128CrossRefGoogle Scholar
  6. 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
  7. Bray RH, Kurtz LT (1945) Determination of total, organic and available forms of phosphorous in soils. Soil Sci 59:39–45CrossRefGoogle Scholar
  8. Brookes PC, Powlson DS, Jenkinson DS (1982) Measurment of microbial phosphorus in soil. Soil Biol Biochem 14:319–329CrossRefGoogle Scholar
  9. 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 17:837–842CrossRefGoogle Scholar
  10. Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  11. Crenshaw CL, Lauber C, Sinsabaugh RL, Stavely LK (2008) Fungal control of nitrous oxide production in semiarid grassland. Biogeochemistry 87:17–27CrossRefGoogle Scholar
  12. Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53:121–147Google Scholar
  13. Díaz-Raviña M, Acea MJ, Carballas T (1993) Seasonal fluctuations in microbial populations and available nutrients in forest soils. Biol Fertil Soils 16:205–210CrossRefGoogle Scholar
  14. Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176CrossRefGoogle Scholar
  15. Fisk MC, Fahey TJ (2001) Microbial biomass and nitrogen cycling responses to fertilization and litter removal in young northern hardwood forests. Biogeochemistry 53:201–223CrossRefGoogle Scholar
  16. Fontaine S, Barot S, Barre P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280CrossRefGoogle Scholar
  17. Gallardo A, Merino J (1992) Nitrogen immobilization in leaf litter at two Mediterranean ecosystems of SW Spain. Biogeochemistry 15:213–228CrossRefGoogle Scholar
  18. Gallardo A, Merino J (1993) Leaf decomposition in two Mediterranean ecosystems of southwest Spain: influence of substrate quality. Ecology 74:152–161CrossRefGoogle Scholar
  19. Gallardo A, Rodríguez-Saucedo JJ, Covelo F, Fernández-Alés R (2000) Soil nitrogen heterogeneity in a Dehesa ecosystem. Plant Soil 222:71–82CrossRefGoogle Scholar
  20. Gallardo A, Covelo F, Morillas L, Delgado M (2009) Ciclos de nutrientes y procesos edáficos en los ecosistemas terrestres: especificidades del caso mediterráneo y sus implicaciones para las relaciones suelo-planta. Ecosistemas 18:4–19Google Scholar
  21. García LV (2003) Controlling the false discovery rate in ecological research. Trends Ecol Evol 18:553–554CrossRefGoogle Scholar
  22. 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 34:635–642CrossRefGoogle Scholar
  23. 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
  24. Goberna M, Pascual JA, García C, Sánchez J (2007) Do plant clumps constitute microbial hotspots in semiarid Mediterranean patchy landscapes? Soil Biol Biochem 39:1047–1054CrossRefGoogle Scholar
  25. 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 26:1573–1581CrossRefGoogle Scholar
  26. Hernández T, García C, Reinhardt I (1997) Short-term effect of wildfire on the chemical, biochemical and microbiological properties of Mediterranean pine forest soils. Biol Fertil Soils 25:109–116CrossRefGoogle Scholar
  27. Jenkinson D, Ladd J (1981) Microbial biomass in soil: measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry. Marcel Dekker Inc, New York, pp 415–471Google Scholar
  28. Joergensen RG, Meyer B, Mueller T (1994) Time-course of the soil microbial biomass under wheat–a one-year field-study. Soil Biol Biochem 26:987–994CrossRefGoogle Scholar
  29. Joergensen RG, Kübler H, Meyer B, Wolters V (1995) Microbial biomass phosphorus in soils of beech (Fagus sylvatica L.) forests. Biol Fertil Soils 19:215–219CrossRefGoogle Scholar
  30. Joffre R, Rambal S, Romane F (1996) Local variations of ecosystem functions in Mediterranean evergreen oak woodland. Ann For Sci 53:561–570CrossRefGoogle Scholar
  31. Jonasson S, Michelsen A, Schmidt IK, Nielsen EV, Callaghan TV (1996) Microbial biomass C, N and P in two arctic soils and responses to addition of NPK fertilizer and sugar: implications for plant nutrient uptake. Oecologia 106:507–515CrossRefGoogle Scholar
  32. Jonasson S, Michelsen A, Schmidt IK (1999) Coupling of nutrient cycling and carbon dynamics in the Arctic, integration of soil microbial and plant processes. Appl Soil Ecol 11:135–146CrossRefGoogle Scholar
  33. Kara Ö, Bolat I, Çakiroğlu K, Öztürk M (2008) Plant canopy effects on litter accumulation and soil microbial biomass in two temperate forests. Biol Fertil Soils 45:193–198CrossRefGoogle Scholar
  34. Killham K, Amato M, Ladd JN (1993) Effect of substrate location in soil and soil pore-water regime on carbon turnover. Soil Biol Biochem 25:57–62CrossRefGoogle Scholar
  35. Kuikman PJ, Van Vuure MMI, Van Veen JA (1989) Effect of soil moisture regime on predation by protozoa of bacterial biomass and the release of bacterial nitrogen. Agric Ecosyst Environ 27:271–279CrossRefGoogle Scholar
  36. Ley RE, Williams MW, Schmidt SK (2004) Microbial population dynamics in an extreme environment: controlling factors in talus soils at 3750 m in the Colorado Rocky Mountains. Biogeochemistry 68:313–335CrossRefGoogle Scholar
  37. Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80:1623–1631CrossRefGoogle Scholar
  38. 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 41:831–839CrossRefGoogle Scholar
  39. Miller AE, Schimel JP, Sickman JO, Skeen K, Meixner T, Melack JM (2009) Seasonal variation in nitrogen uptake and turnover in two high-elevation soils: mineralization responses are site-dependent. Biogeochemistry 93:253–270CrossRefGoogle Scholar
  40. Mlambo D, Mwenje E, Nyathi P (2007) Effects of tree cover and season on soil nitrogen dynamics and microbial biomass in an African savanna woodland dominated by Colophospermum mopane. J Trop Ecol 23:437–448CrossRefGoogle Scholar
  41. Myers RT, Zak DR, White DC, Peacock A (2001) Landscape-level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65:359–367CrossRefGoogle Scholar
  42. 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 42:279–287CrossRefGoogle Scholar
  43. Oades J (1988) The retention of organic matter in soils. Biogeochemistry 5:35–70CrossRefGoogle Scholar
  44. Ojeda F, Marañón T, Arroyo J (2000) Plant diversity patterns in the Aljibe Mountains (S. Spain): a comprehensive account. Biodivers Conserv 9:1323–1343CrossRefGoogle Scholar
  45. Pérez-Ramos IM, Zavala MA, Marañón T, Díaz-Villa MD, Valladares F (2008) Dynamics of understorey herbaceous plant diversity following shrub clearing of cork oak forests: a five-year study. For Ecol Manage 255:3242–3253CrossRefGoogle Scholar
  46. Quilchano C, Marañón T (2002) Dehydrogenase activity in Mediterranean forest soils. Biol Fertil Soils 35:102CrossRefGoogle Scholar
  47. Quilchano C, Marañón T, Pérez-Ramos I, Noejovich L, Valladares F, Zavala M (2008) Patterns and ecological consequences of abiotic heterogeneity in managed cork oak forests of Southern Spain. Ecol Res 23:127–139CrossRefGoogle Scholar
  48. 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 34:841–849CrossRefGoogle Scholar
  49. Rinnan R, Michelsen A, Jonasson S (2008) Effects of litter addition and warming on soil carbon, nutrient pools and microbial communities in a subarctic heath ecosystem. Appl Soil Ecol 39:271–281CrossRefGoogle Scholar
  50. 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 28:1613–1620CrossRefGoogle Scholar
  51. 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 36:1719–1729CrossRefGoogle Scholar
  52. Schade JD, Hobbie SE (2005) Spatial and temporal variation in islands of fertility in the Sonoran Desert. Biogeochemistry 73:541–553CrossRefGoogle Scholar
  53. Schimel JP, Scott WJ, Killham K (1989) Changes in cytoplasmic carbon and nitrogen pools in a soil bacterium and a fungus in response to salt stress. Appl Environ Microbiol 55:1635–1637Google Scholar
  54. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394CrossRefGoogle Scholar
  55. 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 11:147–160CrossRefGoogle Scholar
  56. Schmidt SK, Costello EK, Nemergut DR, Cleveland CC, Reed SC, Weintraub MN, Meyer AF, Martin AM (2007) Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 88:1379–1385CrossRefGoogle Scholar
  57. 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 338:499–500CrossRefGoogle Scholar
  58. Smolander A, Kitunen V (2002) Soil microbial activities and characteristics of dissolved organic C and N in relation to tree species. Soil Biol Biochem 34:651–660CrossRefGoogle Scholar
  59. Soil Survey Staff (2006) Keys to soil taxonomy, 10th edn. USDA-Natural Resources Conservation Service, Washington, DCGoogle Scholar
  60. Sparks DL (1996) Methods of soil analysis. Part 3. Chemical methods soil science society of America and American society of agronomy. Madison, WisconsinGoogle Scholar
  61. Urbieta I, Zavala M, Marañón T (2008) Human and non-human determinants of forest composition in southern Spain: evidence of shifts toward cork oak dominance due to management over the past century. J Biogeogr 35:1688–1700CrossRefGoogle Scholar
  62. Van Veen J, Kuikman P (1990) Soil structural aspects of decomposition of organic matter by micro-organisms. Biogeochemistry 11:213–233CrossRefGoogle Scholar
  63. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  64. Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol Rev 67:321–358CrossRefGoogle Scholar
  65. Witteveen CFB, Visser J (1995) Polyol pools in Aspergillus niger. FEMS Microbiol Lett 134:57–62CrossRefGoogle Scholar
  66. 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 40:2281–2289CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Cristina Aponte
    • 1
    Email author
  • Teodoro Marañón
    • 1
  • Luis V. García
    • 1
  1. 1.Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSICSevillaSpain

Personalised recommendations