Journal of Soils and Sediments

, Volume 14, Issue 3, pp 483–494 | Cite as

Interactive effects of biochar and the earthworm Pontoscolex corethrurus on plant productivity and soil enzyme activities

  • Jorge Paz-Ferreiro
  • Shenglei Fu
  • Ana Méndez
  • Gabriel Gascó



There is a growing interest in the use of soil enzymes as early indicators of soil quality change under contrasting agricultural management practices. In recent years, there has been increasing interest in the use of biochar to improve soil properties and thus soil quality. In addition, earthworms can also be used to ameliorate soil properties. However, there is no literature available on how biochar and earthworms interact and affect soil enzymes.

The general objective of the present study was to test the suitability of adding biochar and earthworms in two tropical soils with low fertility status in order to improve their characteristics and productivity.

Materials and methods

Biochars were prepared from four different materials [sewage sludge (B1), deinking sewage sludge (B2), Miscanthus (B3) and pine wood (B4)] on two tropical soils (an Acrisol and a Ferralsol) planted with proso millet (Panicum milliaceum L.). In addition, in order to investigate the interaction between earthworms and biochar, earthworm Pontoscolex corethrurus was added to half of the mesocosms, while excluded in the remaining half. The activities of invertase, β-glucosidase, β-glucosaminidase, urease, phosphomonoesterase and arylsulphatase were determined. The geometric mean of the assayed enzymes (GMea) was used as an integrative soil quality index.

Results and discussion

Overall, earthworms and especially biochar had a positive effect on soil quality. GMea showed B1, B2 and B3 performing better than B4; however, results were soil specific. Plant productivity increased under both biochar and earthworm addition. Fruit productivity and plant growth was enhanced by B1 and B2 but not by B3 or B4.


Enhancements of productivity and soil enzymatic activities are possible in the presence of earthworms and the combination of the practices earthworm and biochar addition can be suggested in low fertility tropical soils. However, scientists should proceed carefully in the selection of biochars as the results of this study show a high specificity in the biochar–soil interaction.


Biochar Pontoscolex corethrurus Soil enzymes Soil quality Tropical soils 


  1. Acosta-Martínez V, Tabatabai MA (2000) Enzyme activities in a limed agricultural soil. Biol Fertil Soils 31:85–91Google Scholar
  2. Aira M, Monroy F, Domínguez J (2003) Effects of two species of earthworms (Allolobophora spp.) on soil systems: a microfaunal and biochemical analysis. Pedobiologia 47:877–881Google Scholar
  3. Augustenborg CA, Hepp S, Kammann C, Hagan D, Schmidt O, Müller C (2012) Biochar and earthworm effects on soil nitrous oxide and carbon dioxide emissions. J Environ Qual 41:1203–1209CrossRefGoogle Scholar
  4. Bailey VL, Fansler SJ, Smith JL, Bolton H (2011) Reconciling apparent variability in effects of biochar amendment on soil enzyme activities by assay optimization. Soil Biol Biochem 43:296–301Google Scholar
  5. Bandick AB, Dick RP (1999) Field management effects on soil enzyme activities. Soil Biol Bioche 31:1471–1479Google Scholar
  6. Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–45CrossRefGoogle Scholar
  7. Brown G, Pashanasi B, Villenave C, Patron JC, Senapati BK, Giri S, Barois I, Lavelle P, Blanchart E, Blakemore RJ, Spain BJ (1999) Effects of earthworms on plant production in the tropics. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical agroecosystems. CABI, Wallingford, pp 87–147Google Scholar
  8. Curry JP, Schmidt O (2007) The feeding ecology of earthworms—a review. Pedobiologia 50:463–477CrossRefGoogle Scholar
  9. Day PR (1965) Particle fractionation and particle-size analysis. In: Black CA, Evans DD, White JL, Ensminger LE, Clark FE (eds) Methods of soil analysis, part 1, physical and mineralogical properties. Including statistics of measurement and sampling. ASASSSA, Madison, pp 545–567Google Scholar
  10. Doube BM, Brown GG (1998) Life in a complex community: functional interactions between earthworms, organic matter, microorganisms, and plant growth. In: Edwards CA (ed) Earthworm ecology. St. Lucie Press, Boca Raton, pp 179–211Google Scholar
  11. Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606CrossRefGoogle Scholar
  12. Ekenler M, Tabatabai MA (2003) Tillage and residue management effects on β-glucosaminidase activity in soils. Soil Biol Biochem 35:871–874CrossRefGoogle Scholar
  13. FAO (2006) World reference base for soils resources. World Soil No. 103. Rome, ItalyGoogle Scholar
  14. García-Ruiz R, Ochoa V, Hinojosa MB, Carreira JA (2008) Suitability of enzyme activities for the monitoring of soil quality improvement in organic agricultural systems. Soil Biol Biochem 40:2137–2145CrossRefGoogle Scholar
  15. Gascó G, Paz-Ferreiro J, Méndez A (2012) Thermal analysis of soil amended with sewage sludge and biochar from sewage sludge pyrolysis. J Therm Anal Calorim 108:769–775CrossRefGoogle Scholar
  16. Glaser B, Lehmann J, Zech W (2002) Ameliorating physical and chemical properties of highly weathered soils in the tropics with charcoal—a review. Biol Fertil Soils 35:219–230CrossRefGoogle Scholar
  17. Jeffery S, Verheijen FGA, van der Velde M, Bastos AC (2011) A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis. Agr Ecosyst Environ 144:175–187CrossRefGoogle Scholar
  18. Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72CrossRefGoogle Scholar
  19. Lammirato C, Miltner A, Kaestner M (2011) Effects of wood char and activated carbon on the hydrolysis of cellobiose by β-glucosidase from Aspergillus niger. Soil Biol Biochem 43:1936–1942Google Scholar
  20. Lavelle P, Spain AV (2001) Soil ecology. Kluwer Academic, Dordrecht, 654 ppCrossRefGoogle Scholar
  21. Lavelle P, Barois I, Cruz I, Fragoso C, Hernandez A, Pineda A, Rangel P (1987) Adaptive strategies of Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta), a peregrine geophagous earthworm of the humid tropics. Biol Fertil Soils 5:188–194CrossRefGoogle Scholar
  22. Li H, Xiang D, Wang C, Li X, Lou Y (2012) Effects of epigeic earthworm (Eisenia fetida) and arbuscular mycorrhizal fungus (Glomus intraradices) on enzyme activities of a sterilized soil–sand mixture and nutrient uptake by maize. Biol Fertil Soils 48:879–887CrossRefGoogle Scholar
  23. Li JY, Liu ZD, Zhao AZ, Xu RK (2013) Microbial and enzymatic properties in response to amelioration of an acidic Ultisol by industrial and agricultural by-products. J Soils Sediments. doi:10.1007/s11368-013-0666-6 Google Scholar
  24. Liu X, Zhang A, Ji C, Joseph S, Bian R, Li L, Pan G, Paz-Ferreiro J (2013) Biochar's effect on crop productivity and the dependence on experimental conditions—a meta-analysis of literature data. Plant Soil. doi:10.1007/s11104-013-1806-x Google Scholar
  25. Medina-Roldán E, Paz-Ferreiro J, Bardgett RD (2012) Grazing exclusion affects soil and plant communities, but has no impact on soil carbon storage in an upland grassland. Agr Ecosyst Environ 149:118–123CrossRefGoogle Scholar
  26. Mijangos I, Albizu I, Epelde L, Amezaga I, Mendarte S, Garbisu C (2010) Effects of liming on soil properties and plant performance of temperate mountainous grasslands. J Environ Manag 91:2066–2074Google Scholar
  27. Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soils. In: Burns RG, Dick RP (eds) Enzymes in the Environment: Activity, Ecology and Applications. Marcel Dekker Inc, Nueva York, pp 1–34Google Scholar
  28. Noguera D, Rondón M, Laossi KR, Hoyos V, Lavelle P, de Carvalho MHC, Barot S (2010) Contrasted effect of biochar and earthworms on rice growth and resource allocation in different soils. Soil Biol Biochem 42:1017–1027CrossRefGoogle Scholar
  29. Noguera D, Barot S, Laossi KR, Cardoso J, Lavelle P, Cruz de Carvalho MH (2012) Biochar but not earthworms enhances rice growth through increased protein turnover. Soil Biol Biochem 52:13–20CrossRefGoogle Scholar
  30. Parham JA, Deng SP (2000) Detection, quantification and characterization of β-glucosaminidase activity in soil. Soil Biol Biochem 32:1183–1190CrossRefGoogle Scholar
  31. Paz-Ferreiro J, Trasar-Cepeda C, Leirós MC, Seoane S, Gil-Sotres F (2007) Biochemical properties of acid soils under native grassland in a temperate humid zone. N Z J Agr Res 50:537–548CrossRefGoogle Scholar
  32. Paz-Ferreiro J, Trasar-Cepeda C, Leirós MC, Seoane S, Gil-Sotres F (2009) Biochemical properties in managed grassland soils in a temperate humid zone: modifications of soil quality as a consequence of intensive grassland use. Biol Fertil Soils 45:711–722CrossRefGoogle Scholar
  33. Paz-Ferreiro J, Trasar-Cepeda C, Leirós MC, Seoane S, Gil-Sotres F (2010) Effect of management and climate on biochemical properties of grassland soils from Galicia (NW Spain). Eur J Soil Biol 46:136–143Google Scholar
  34. Paz-Ferreiro J, Trasar-Cepeda C, Leirós MdC, Seoane S, Gil-Sotres F (2011) Intraannual variation in biochemical properties and the biochemical equilibrium of different grassland soils under contrasting management and climate. Biol Fertil Soils 47:633–645Google Scholar
  35. Paz-Ferreiro J, Gascó G, Gutiérrez B, Méndez A (2012) Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil. Biol Fertil Soils 48:511–517CrossRefGoogle Scholar
  36. Pietikäinen J, Kiikkilä O, Fritze H (2000) Charcoal as a habitat for microbes and its effects on the microbial community of the underlying humus. Oikos 89:231–242CrossRefGoogle Scholar
  37. Ponge JF, Ballof S, Rossi JP, Lavelle P, Betsch JM, Gaucher P (2006) Ingestion of charcoal by the Amazonian earthworm Pontoscolux corethrurus: a potential for tropical soil fertility. Soil Biol Biochem 38:2008–2009CrossRefGoogle Scholar
  38. Puglisi E, Del Re AAM, Rao MA, Gianfreda L (2006) Development and validation of numerical indexes integrating enzyme activities of soils. Soil Biol Biochem 38:1673–1681CrossRefGoogle Scholar
  39. Ross DJ (1976) Invertase and amylase activities in ryegrass and white clover plants and their relationships with activities in soils under pasture. Soil Biol Biochem 8:351–356CrossRefGoogle Scholar
  40. Saá A, Trasar-Cepeda MC, Gil-Sotres F, Carballas T (1993) Changes in soil phosphorus and acid phosphatase activity immediately following forest fires. Soil Biol Biochem 25:1223–1230CrossRefGoogle Scholar
  41. Schinner F, von Mersi W (1990) Xylanase-, CM-cellulase and invertase activity in soil: an improved method. Soil Biol Biochem 22:511–515CrossRefGoogle Scholar
  42. Tabatabai MA, Bremner JM (1970) Arylsulfatase activity of soils. Soil Sci Soc Am Proc 34:225–229CrossRefGoogle Scholar
  43. Tao J, Griffiths B, Zhang S, Chen X, Liu M, Hu F, Li H (2009) Effects of earthworms on soil enzyme activity in an organic residue amended rice–wheat rotation agro-ecosystem. Appl Soil Ecol 42:221–226CrossRefGoogle Scholar
  44. Thies JE, Rillig M (2009) Characteristics of biochar: biological properties. In: Lehmann J, Joseph S (eds) Biochar for environmental management: science and technology. Earthscan, London, pp 85–105Google Scholar
  45. 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
  46. Topoliantz S, Ponge JF (2005) Charcoal consumption and casting activity by Pontoscolex corethrurus (Glossoscolecidae). Appl Soil Ecol 28:217–224CrossRefGoogle Scholar
  47. USEPA (1997) Method 3051a: microwave assisted acid dissolution of sediments, sludges, soils, and oils, 2nd edn. U.S. Gov. Print. Office, WashingtonGoogle Scholar
  48. van Zwieten L, Kimber S, Morris S, Chan KY, Downie A, Rust J, Joseph S, Cowie A (2010) Effects of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant Soil 327:235–246Google Scholar
  49. Wu F, Jia Z, Wang S, Chang SX, Startsev A (2013) Contrasting effects of wheat straw and its biochar on greenhouse gas emissions and enzyme activities in a Chernozemic soil. Biol Fertil Soils 49:555–565CrossRefGoogle Scholar
  50. Zhang B, Li G, Shen T, Wang T, 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

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Jorge Paz-Ferreiro
    • 1
    • 2
  • Shenglei Fu
    • 2
  • Ana Méndez
    • 3
  • Gabriel Gascó
    • 1
  1. 1.Departamento de Edafologia, ETSI AgrónomosUniversidad Politécnica de MadridMadridSpain
  2. 2.Institute of Ecology, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  3. 3.Departamento de Ingeniería de Materiales, ETSI MinasUniversidad Politécnica de MadridMadridSpain

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