Earthworm Interactions with Soil Enzymes

  • Ridvan KizilkayaEmail author
  • Ayten Karaca
  • Oguz Can Turgay
  • Sema Camci Cetin
Part of the Soil Biology book series (SOILBIOL, volume 24)


As one of the dominant members of soil fauna, earthworms fulfill significant tasks in the soil ecosystem by participating in the physico-chemical processes of the soil, such as organic matter cycles, nutrient transformations, and modifications in soil structure. These processes are also directed by the activities and amounts of the enzymes produced by soil microorganisms that inhabit a wide range of soil environments including intestine systems, excretions, casts, and burrow linings of the earthworms. Therefore, microbial activity and the enzymes produced are considered to be closely related with earthworm life in soil. The purpose of this chapter is to describe the interactions between soil enzymes and earthworms at different levels in soil.


Microbial Biomass Sewage Sludge Soil Enzyme Soil Enzyme Activity Earthworm Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aina PO (1984) Contribution of earthworms to porosity and water infiltration in a tropical soil under forest and long-term cultivation. Pedobiologia 26:131–136Google Scholar
  2. Araujo Y, Lopez-Hernandez D (1999) Earthworm populations in a savannaagro forestry system of Venezuelan Amazonia. Biol Fertil Soils 29:413–418CrossRefGoogle Scholar
  3. Askin T, Kizilkaya R (2006) Assessing spatial variability of soil enzyme activities in pasture topsoils using geostatistics. Eur J Soil Biol 42:230–237CrossRefGoogle Scholar
  4. Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Pollut 47:335–379CrossRefGoogle Scholar
  5. Banerjee MR, Burton DL, Depoe S (1997) Impact of sewage sludge application on soil biological characteristics. Agr Ecosyst Environ 66:241–249CrossRefGoogle Scholar
  6. Bauer C, Römbke J (1997) Factors influencing the toxicity of two pesticides on three lumbricid species in laboratory tests. Soil Biol Biochem 29:705–708CrossRefGoogle Scholar
  7. Beiderbeck VO, Campbell CA, Smith AE (1987) Effect of long term 2,4-D field application on soil biochemical processes. J Environ Qual 16:257–262CrossRefGoogle Scholar
  8. Benitez E, Nogales R, Elvira C, Masciandaro G, Ceccanti B (1999) Enzyme activities as indicators of the stabilization of sewage sludges composting with Eisenia foetida. Bioresour Technol 6:297–303CrossRefGoogle Scholar
  9. Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36:177–198CrossRefGoogle Scholar
  10. Burns RG (1978) Enzyme activity in soil: some theoretical and practical considerations. In: Burns RG (ed) Soil enzymes. Academic, New York, pp 295–340Google Scholar
  11. Butler JHA, Ladd JN (1969) The effect of methylation of humic acids and their influence on proteolytic enzyme activity. Aust J Soil Res 7:263–268CrossRefGoogle Scholar
  12. Cashel M, Freese E (1964) Excretion of alkaline phosphatase by Bacillus subtilis. Biochem Biophys Res Commun 16:541–544PubMedCrossRefGoogle Scholar
  13. Ceccanti B, Nannipieri P, Cervelli S, Sequi P (1978) Fractionation of humus–urease complexes. Soil Biol Biochem 10:39–45CrossRefGoogle Scholar
  14. Chan KY (2001) An overview of some tillage impacts on earthworm population abundance and diversity – implications for functioning in soils. Soil Till Res 57:179–191CrossRefGoogle Scholar
  15. Chan KY, Heenan DP (1995) Occurrence of enchytraeid worms and some properties of their casts in an Australian soil under cropping. Aust J Soil Res 33:651–657CrossRefGoogle Scholar
  16. Conrad JP (1940) The nature of the catalyst causing the hydrolysis of urea in soils. Soil Sci 54:367–380Google Scholar
  17. Crawford DL, Lynch JM, Whipps JM, Ousley MA (1993) Isolation and characterization of actinomycete antagonists of a fungal root pathogen. Appl Environ Microbiol 59:3899–3905PubMedGoogle Scholar
  18. Daniel O, Anderson JM (1992) Microbial biomass and activity in contrasting soil materials after passage through the gut of the earthworm Lumbricus rubellus Hoffmeister. Soil Biol Biochem 24:465–470CrossRefGoogle Scholar
  19. Decaens T, Rangel AF, Asakawa N, Thomas RJ (1999) Carbon and nitrogen dynamics in ageing earthworm casts in grasslands of the eastern plains of Colombia. Biol Fertil Soils 30:20–28CrossRefGoogle Scholar
  20. Dengiz O, Kizilkaya R, Gol C, Hepsen S (2007) Effects of different topographic positions on soil properties and soil enzymes activities. Asian J Chem 19:2295–2306Google Scholar
  21. Doelman P, Haanstra L (1979) Effect of lead on soil respiration and dehydrogenase activity. Soil Biol Biochem 11:475–479CrossRefGoogle Scholar
  22. Doube BM, Schmidt O, Killham K, Correll R (1997) Influence of mineral soil on the palatability of organic matter for lumbricid earthworms: a simple food preference study. Soil Biol Biochem 29:569–575CrossRefGoogle Scholar
  23. Edwards CA (1984) Changes in agricultural practice and their impact upon soil organisms. In: Jenkins D (ed) Proceedings of Symposium No. 13, The impact of agriculture on wildlife, agriculture and the environment, UK pp 46–65Google Scholar
  24. Edwards CA (1998) Earthworm ecology. St. Lucie, Boca Raton, pp 327–354Google Scholar
  25. Edwards CA, Bohlen PJ (1996) Earthworm ecology and biology. Chapman & Hall, London, pp 196–212Google Scholar
  26. Edwards CA, Lofty JR (1982a) The effect of direct drilling and minimal cultivation on earthworm populations. J Appl Ecol 19:723–724CrossRefGoogle Scholar
  27. Edwards CA, Lofty JR (1982b) Nitrogenous fertilizers and earthworm populations in agricultural soils. Soil Biol Biochem 14:515–521CrossRefGoogle Scholar
  28. Edwards CA, Thompson AR (1973) Pesticides and the soil fauna. Residue Rev 45:1–79PubMedGoogle Scholar
  29. Ekberli İ, Kizilkaya R (2005) Microbial biomass carbon and basal soil respiration in soil affected by addition of different organic wastes and earthworm L. terrestris. Second Congress of Azerbaijan soil science society on soil resources their using and protection, 10–14 November 2005, Baku, AzerbaijanGoogle Scholar
  30. Ekberli İ, Kizilkaya R (2006) Catalase enzyme and its kinetic parameters in earthworm L. terrestris casts and surrounding soil. Asian J Chem 18:2321–2328Google Scholar
  31. Ekberli İ, Kizilkaya R, Kars N (2006) Urease enzyme and its kinetic and thermodynamic parameters in clay loam soil. Asian J Chem 18:3097–3105Google Scholar
  32. Estermann EF, McLaren AD (1961) Contribution of rhizoplane organisms to the total capacity of plants to utilize organic nutrients. Plant Soil 15:243–260CrossRefGoogle Scholar
  33. Flieβbach A, Martens R, Reber HH (1994) Soil microbial biomass and microbial activity in soil treated with heavy metal contaminated sewage sludge. Soil Biol Biochem 26:1201–1205CrossRefGoogle Scholar
  34. Frankenberger WT Jr, Tabatabai MA (1982) Amidase and urease activities in plants. Plant Soil 64:153–166CrossRefGoogle Scholar
  35. Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414CrossRefGoogle Scholar
  36. Goyal S, Dhull SK, Kapoor KK (2005) Chemical and biological changes during composting of different organic wastes and assessment of compost maturity. Bioresour Technol 96:1584–1591PubMedCrossRefGoogle Scholar
  37. Guild WJMcL (1948) Studies on the relationship between earthworms and soil fertility III. The effect of soil type on the structure of earthworm populations. Ann Appl Biol 35:181–192CrossRefGoogle Scholar
  38. Haanstra L, Doelman P (1991) An ecological dose–response model approach to short and long-term effects of heavy metals on arylsulphatase activity in soil. Biol Fertil Soils 11:18–23CrossRefGoogle Scholar
  39. Haimi J, Huhta V, Boucelham M (1992) Growth increase of birch seedlings under the influence of earthworms – a laboratory study. Soil Biol Biochem 24:1525–1528CrossRefGoogle Scholar
  40. Heimbach F (1992) Correlation between data from laboratory and field tests for investigating the toxicity of pesticides to earthworms. Soil Biol Biochem 24:1749–1753CrossRefGoogle Scholar
  41. Heimbach F (1997) Field tests on the side effects of pesticides on earthworms: influence of plot size and cultivation practices. Soil Biol Biochem 29:671–676CrossRefGoogle Scholar
  42. Hubbard VC, Jordan D, Stecker JA (1999) Earthworm response to rotation and tillage in a Missouri claypan soil. Biol Fertil Soils 29:343–347CrossRefGoogle Scholar
  43. Jin K, Sleutel S, Buchan D, Neve SD, Cai DX, Gabriels D, Jin JY (2009) Changes of soil enzyme activities under different tillage practices in the Chinese Loess Plateau. Soil Till Res 104:115–120CrossRefGoogle Scholar
  44. Johnson-Maynard JL, Umiker KJ, Guy SO (2007) Earthworm dynamics and soil physical properties in the first three years of no-till management. Soil Till Res 94:338–345CrossRefGoogle Scholar
  45. Jordan D, JrF P, Hubbard VC (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
  46. Joschko M, Diestel H, Larink O (1989) Assessment of earthworm burrowing efficiency in compacted soil with a combination of morphological and soil physical measurements. Biol Fertil Soils 8:191–196CrossRefGoogle Scholar
  47. Kandeler E, Palli S, Stemmer M, Gerzabek MH (1999) Tillage changes microbial biomass and enzyme activities in particle-size fractions of a Haplic Chernozem. Soil Biol Biochem 31:1253–1264CrossRefGoogle Scholar
  48. Karaca A, Haktanir K, Kizilkaya R (2000) The effect of lead and cadmium compounds on soil catalase enzyme activity. Proceedings of International symposium on desertification (ISD), 416–421, 13–17 June, 2000, Konya, TurkeyGoogle Scholar
  49. Karaca A, Naseby D, Lynch J (2002) Effect of cadmium-contamination with sewage sludge and phosphate fertilizer amendments on soil enzyme activities, microbial structure and available cadmium. Biol Fertil Soil 35:435–440CrossRefGoogle Scholar
  50. Karaca A, Turgay C, Tamer N (2006) Effects of a humic deposit (Gyttja) on soil chemical and microbiological properties and heavy metal availability. Biol Fertil Soil 42:585–592CrossRefGoogle Scholar
  51. Karaca A, Kizilkaya R, Turgay OC, Cetin SC (2010a) Effects of earthworms on the availability and removal of heavy metals in soils. In: Sherameti I, Varma A (eds) Soil heavy metals, soil biology series, vol 19. Springer, Berlin, pp 369–388CrossRefGoogle Scholar
  52. Karaca A, Cetin SC, Turgay OC, Kizilkaya R (2010b) Effects of heavy metals on soil enzyme activities. In: Sherameti I, Varma A (eds) Soil heavy metals, soil biology, vol 19. Springer, Berlin, pp 237–262CrossRefGoogle Scholar
  53. Keogh RG, Christensen MJ (1976) Influence of passage through Lumbricus rubellus Hoffmeister earthworms on viability of Pithomyces chartarum (Berk. and Curt.) M.B. Ellis spores. NZ J Agric Res 19:255–256Google Scholar
  54. Khalaf El-Duweini A, Ghabbour SI (1965) Population density and biomass of earthworms in different types of Egyptian soils. J Appl Ecol 2:271–287CrossRefGoogle Scholar
  55. Killham K (1994) Soil ecology. Cambridge University Press, Cambridge, pp 141–150Google Scholar
  56. Kizilkaya R (2004) Cu and Zn accumulation in earthworm Lumbricus terrestris L. in sewage sludge amended soil and fractions of Cu and Zn in casts and surrounding soil. Ecol Eng 22:141–151CrossRefGoogle Scholar
  57. Kizilkaya R (2005) The role of different organic wastes on zinc bioaccumulation by earthworm Lumbricus terrestris L. (Oligochaeta) in successive Zn added soil. Ecol Eng 25:322–331CrossRefGoogle Scholar
  58. Kizilkaya R (2008) Dehydrogenase activity in Lumbricus terrestris casts and surrounding soil affected by addition of different organic wastes and Zn. Bioresour Technol 99:946–953PubMedCrossRefGoogle Scholar
  59. Kizilkaya R, Askin T (2002) Influence of cadmium fractions on microbiological properties in Bafra plain soils. Arch Agron Soil Sci 48:263–272CrossRefGoogle Scholar
  60. Kizilkaya R, Bayrakli B (2005) Effects of N-enriched sewage sludge on soil enzyme activities. Appl Soil Ecol 30:192–202CrossRefGoogle Scholar
  61. Kizilkaya R, Ekberli İ (2008) Determination of the effects of hazelnut husk and tea waste treatments on urease enzyme activity and its kinetics in soil. Turk J Agric For 32:299–310Google Scholar
  62. Kizilkaya R, Hepsen S (2004) Effect of biosolid amendment on enzyme activities in earthworm (Lumbricus terrestris) casts. J Plant Nutr Soil Sci 167:202–208CrossRefGoogle Scholar
  63. Kizilkaya R, Hepsen S (2007) Microbiological properties in earthworm Lumbricus terrestris L. cast and surrounding soil amended with various organic wastes. Commun Soil Sci Plant Anal 38:2861–2876CrossRefGoogle Scholar
  64. Kizilkaya R, Askin T, Bayrakli B, Saglam M (2004) Microbiological characteristics of soils contaminated with heavy metals. Eur J Soil Biol 40:95–102CrossRefGoogle Scholar
  65. Kizilkaya R, Bayrakli F, Surucu A (2007a) Relationships between phosphatase activity and phosphorus fractions in agricultural soils. Int J Soil Sci 2:107–118CrossRefGoogle Scholar
  66. Kizilkaya R, Ekberli I, Kars N (2007b) Urease activity and its kinetics in soil treated with tobacco waste and wheat straw. Ankara Univ J Agric Sci 13:186–194Google Scholar
  67. Kizilkaya R, Hepsen S, Akca İ, Bayrakli B, Askin T, Turkmen C (2009) Determination of total and mobile Pb fractions during vermicomposting in sewage sludge. International Symposium on Environment. 20-23 May 2009. Kyrgyzstan – Turkey Manas Unıversity, Faculty of Engineering, Bishkek, Kyrgyz RebublicGoogle Scholar
  68. Kladivko EJ, Mackay AD, Bradford JM (1986) Earthworms as a factor in the reduction of soil crusting. Soil Sci Soc Am J 50:191–196CrossRefGoogle Scholar
  69. Knight BP, McGrath MJ, Doran JW, Cline RG, Harris RF, Schuman GE (1997) Biomass carbon measurements and substrate utilization patterns of microbial populations from soils amended with cadmium, copper, or zinc. Appl Environ Microb 63:39–43Google Scholar
  70. Kooistra MJ (1991) A micromorphological approach to the interactions between soil structure and soil biota. Agric Ecosyst Environ 34:315–328CrossRefGoogle Scholar
  71. Ladd JN, Butler JAH (1975) Humus–enzyme systems and synthetic, organic polymer–enzyme analogs. Soil Biol Biochem 4:143–194Google Scholar
  72. Lavelle P, Spain AV (2001) Soil ecology. Chapman & Hall, LondonGoogle Scholar
  73. Le Bayon RC, Binet F (2006) Earthworms change the distribution and availability of phosphorous in organic substrates. Soil Biol Biochem 38:235–246Google Scholar
  74. Leroy BLM, Van den Bossche A, Neve SD, Reheul D, Moens M (2007) The quality of exogenous organic matter: short-term influence on earthworm abundance. Eur J Soil Biol 43:S196–S200CrossRefGoogle Scholar
  75. Leroy BLM, Schmidt O, Van den Bossche A, Reheul D, Moens M (2008) Earthworm population dynamics as influenced by the quality of exogenous organic matter. Pedobiologia 52:139–150CrossRefGoogle Scholar
  76. Lui SX, Xiong DZ, Wu DB (1991) Studies on the effect of earthworms on the fertility of red-arid soil. Advances in management and conservation of soil fauna, Proceedings of the 10th International Soil Zoology Colloquium, held at Bangalore, India, August 7–13Google Scholar
  77. Marininssen JCY, Hillenaar SI (1997) Earthworm-induced distribution of organic matter in macro-aggregates from differently managed arable fields. Soil Biol Biochem 29:391–395CrossRefGoogle Scholar
  78. Mawdsley JL, Burns RG (1994) Inoculation of plants with Flavobacterium P25 results in altered rhizosphere enzyme activities. Soil Biol Biochem 26:871–882CrossRefGoogle Scholar
  79. McLaren AD (1975) Soil as a system of humus and clay immobilized enzymes. Chem Screpta 8:97–99Google Scholar
  80. Mijangos I, Pérez R, Albizu I, Garbisu C (2006) Effects of fertilization and tillage on soil biological parameters. Enzyme Microl Technol 40:100–106CrossRefGoogle Scholar
  81. Morgan MH (1988) The role of microorganisms in the nutrition of Eisenia foetida. In: Edwards CA, Neuhauser EF (eds) Earthworms in waste and environmental management. SPB Academic Publishing, The Hague, pp 71–82Google Scholar
  82. Mulongoy K, Bedoret A (1989) Properties of worm casts and surface soils under various plant covers in the humid tropics. Soil Biol Biochem 21:197–203CrossRefGoogle Scholar
  83. Naseby DC, Lynch JM (2002) Enzymes and microorganisms in the rhizosphere. In: Burns RG, Dick RP (eds) Enzymes in the environment, activity, ecology and environment. Marcel Dekker Inc, New York, pp 109–125Google Scholar
  84. Niemi RM, Heiskanen I, Ahtiainen JH, Rahkonen A, Mäntykoski K, Welling L, Laitinen P, Ruuttunen P (2009) Microbial toxicity and impacts on soil enzyme activities of pesticides used in potato cultivation. Appl Soil Ecol 41:293–304CrossRefGoogle Scholar
  85. Nishimura S, Nomura M (1959) Ribonuclease of Bacillus subtilis. J Biochem 46:161–167Google Scholar
  86. Nordström S, Rundgren S (1974) Environmental factors and lumbricid associations in southern Sweden. Pedobiologia 14:1–27Google Scholar
  87. Parkin TB, Berry EC (1994) Nitrogen transformations associated with earthworm casts. Soil Biol Biochem 26:1233–1238CrossRefGoogle Scholar
  88. Pashanasi B, Lavelle P, Alegre J, Charpentier F (1996) Effect of the endogeic earthworm, Pontoscolex corethrurus on soil chemical characteristics and plant growth in a low-input tropical agroecosystem. Soil Biol Biochem 28:801–808CrossRefGoogle Scholar
  89. Reddell P, Spain AV (1991a) Earthworms as vectors of viable propagules of mycorrhizal fungi. Soil Biol Biochem 23:767–774CrossRefGoogle Scholar
  90. Reddell P, Spain AV (1991b) Transmission of infective Frankia (Actinomycetales) propagules in casts of the endogeic earthworm Pontoscolex corethrurus (Oligochaeta: Glossoscolecidae). Soil Biol Biochem 23:775–778CrossRefGoogle Scholar
  91. Ros M, Pascual JA, Garcia C, Hernandez MT, Insam H (2006) Hydrolase activities, microbial biomass and bacterial community in a soil after long-term amendment with different composts. Soil Biol Biochem 38:3443–3452CrossRefGoogle Scholar
  92. Rossi JP, Lavelle P, Albrecht A (1997) Relationships between spatial pattern of the endogeic earthworm Polypheretima elongata and soil heterogeneity. Soil Biol Biochem 29:485–488CrossRefGoogle Scholar
  93. Ruz-Jerez BE, Ball PR, Tillman RW (1992) Laboratory assessment of nutrient release from a pasture soil receiving grass or clover residues, in the presence or absence of Lumbricus rubellus or Eisenia foetida. Soil Biol Biochem 24:1529–1534CrossRefGoogle Scholar
  94. Sastre I, Vicente MA, Lobo MC (1996) Influence of the application of sewage sludges on soil microbial activity. Bioresource Technol 57:19–23CrossRefGoogle Scholar
  95. Satchell JE (1967) Lumbricidae. In: Burges A, Raw F (eds) Soil biology. Academic, London, pp 259–322Google Scholar
  96. Satchell JE, Martin K (1984) Phosphatase activity in earthworm faeces. Soil Biol Biochem 16:191–194CrossRefGoogle Scholar
  97. Scheu S (1987) Microbial activity and nutrient dynamics in earthworm casts (Lumbricidae). Biol Fertil Soils 3:230–234Google Scholar
  98. Scheu S (1991) Mucus excretion and carbon turnover of endogeic earthworms. Biol Fertil Soils 12:217–220CrossRefGoogle Scholar
  99. Scheu S, Parkinson D (1994) Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soil from cool temperate forests on the Canadian Rocky Mountains-laboratory studies. Appl Soil Ecol 1:113–125CrossRefGoogle Scholar
  100. Schmidt O, Doube BM, Ryder MH, Killham K (1997) Population dynamics of Pseudomonas corrugata 2140R lux8 in earthworm food and in earthworm casts. Soil Biol Biochem 29:523–528CrossRefGoogle Scholar
  101. Schmidt O, Scrimgeour CM, Curry JP (1999) Carbon and nitrogen stable isotope ratios in body tissue and mucus of feeding and fasting earthworms (Lumbricus festivus). Oecologia 118:9–15PubMedCrossRefGoogle Scholar
  102. Schonholzer F, Hahn D, Zeyer J (1999) Origins and fate of fungi and bacteria in the gut of Lumbricus terrestris L. studied by image analysis. FEMS Microbiol Ecol 28:235–248Google Scholar
  103. Sharpley AN, Syers JK (1976) Potential role of earthworm casts for the phosphorus enrichment of run-off waters. Soil Biol Biochem 8:341–346CrossRefGoogle Scholar
  104. Shaw C, Pawluk S (1986) Faecal microbiology of Octolasion tyrtaeum, Aporrectodea turgida and Lumbricus terrestris and its relation to the carbon budgets of three artificial soils. Pedobiologia 29:377–389Google Scholar
  105. Simonart P, Batistic L, Mayaudon J (1967) Isolation of protein from humic acid extracted from soil. Plant Soil 27:153–161CrossRefGoogle Scholar
  106. Springett JA (1983) Effect of five species of earthworm on some soil properties. J Appl Ecol 20:865–887CrossRefGoogle Scholar
  107. Stamatiadis S, Nerantzis ET, Giannakopoulou E, Maniatis LM (1994) The nutritive value of two species of microorganisms to the earthworm Eisenia fetida. Eur J Soil Biol 30:177–185Google Scholar
  108. Striganova BR, Marfenina OE, Ponomarenko VA (1989) Some aspects of the effect of earthworms on soil fungi. Biol Bull Acad Sci USSR 15:460–463Google Scholar
  109. Sylvestre GS, Fournier JC (1979) Effects of pesticides on the soil microflora. Adv Agron 31:63–72.Google Scholar
  110. Tabatabai MA, Dick WA (2002) Enzymes in soil: research and developments in measuring activities. In: Burns GR, Dick RP (eds) Enzymes in the environment, activity, ecology and environment. Marcel Dekker Inc, New York, pp 567–598Google Scholar
  111. Tam NFY, Wong YS (1990) Respiration studies on the decomposition of organic waste-amended colliery spoil. Agr Ecosyst Environ 32:25–38CrossRefGoogle Scholar
  112. Tarrant KA, Field SA, Langton SD, Hart ADM (1997) Effects on earthworm populations of reducing pesticide use in arable crop rotations. Soil Biol Biochem 29:657–661CrossRefGoogle Scholar
  113. Tiunov AV, Scheu S (1999) Microbial respiration, biomass, biovolume and nutrient status in burrow walls of Lumbricus terrestris L. (Lumbricidae). Soil Biol Biochem 31:2039–2048CrossRefGoogle Scholar
  114. Tiwari SC, Tiwari BK, Mishra RR (1989) Microbial populations, enzyme activities and nitrogen–phosphorus–potassium enrichment in earthworm casts and in the surrounding soil of a pineapple plantation. Biol Fertil Soils 8:178–182CrossRefGoogle Scholar
  115. Tomlin AD, McCabe D, Protz R (1992) Species composition and seasonal variation of earthworms and their effect on soil properties in southern Ontario, Canada. Soil Biol Biochem 24:1451–1457CrossRefGoogle Scholar
  116. Turgay OC, Erdogan EE, Karaca A (2010) Effect of humic deposit (leonardite) on degradation of semi-volatile and heavy hydrocarbons and soil quality in crude-oil-contaminated soil. Environ Monit Assess. doi: 10.1007/s10661-009-1213-1 PubMedGoogle Scholar
  117. Weetall HH (1975) Immobilized enzymes and their application in the food and beverage industry. Process Biochem 10:3–24Google Scholar
  118. Weimberg R, Orton WL (1963) Repressible acid phosphomonoesterase and constitutive pyrophosphatase of Saccharomyces mellis. J Bacteriol 86:805–813PubMedGoogle Scholar
  119. Weimberg R, Orton WL (1964) Evidence for an exocellular site for the acid phosphatase of Saccharomyces mellis. J Bacteriol 88:1743–1754PubMedGoogle Scholar
  120. Wolter C, Scheu S (1999) Changes in bacterial numbers and hyphal lengths during the gut passage through Lumbricus terrestris (Lumbricidae, Oligochaeta). Pedobiologia 43:891–900Google Scholar
  121. Yakupoglu T, Hepsen S, Ozdemir N, Kizilkaya R (2007) The effects of various organic wastes applied into eroded soil on dehydrogenase enzyme activity. II. International Conference on Environmental, Industrial and Applied Microbiology (BioMicroWorld 2007), 28 November–1 December, Seville, SpainGoogle Scholar
  122. Zhang BG, Li GT, Shen TS, Wang JK, Sun Z (2000) Changes in microbial biomass C, N, and P and enzyme activities in soil incubated with the earthworms Metaphire guillelmi or Eisenia fetida. Soil Biol Biochem 32:2055–2062CrossRefGoogle Scholar

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© Springer Berlin Heidelberg 2011

Authors and Affiliations

  • Ridvan Kizilkaya
    • 1
    Email author
  • Ayten Karaca
    • 2
  • Oguz Can Turgay
    • 2
  • Sema Camci Cetin
    • 3
  1. 1.Department of Soil Science, Faculty of AgricultureOndokuz Mayis UniversitySamsunTurkey
  2. 2.Faculty of Agriculture, Department of Soil ScienceAnkara UniversityAnkaraTurkey
  3. 3.Department of Soil Science and Ecology, Faculty of ForestryCankiri Karatekin UniversityCankiriTurkey

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