Environmental Science and Pollution Research

, Volume 25, Issue 31, pp 30998–31006 | Cite as

Influence of earthworms on the nitrogen transfer of sewage sludge in the vermifilter process

  • Jian Yang
  • Wanyin Di
  • Jing Liu
  • Meiyan XingEmail author
Research Article


A 6-year laboratory study was conducted to explore the performance of the vermifilter (VF) on reducing sewage sludge. Sewage sludge was found to be reduced significantly in the VF and exhibited a better performance of sludge reduction as compared with the conventional biofilter (BF), which could be traced through the nitrogen-rich organic matter. The nitrogen stable isotope technology was applied to study the matter flow of sewage sludge in the VF process and the influence of earthworms Eisenia fetida on sewage sludge reduction. Results showed that (1) the protein material could be consumed more than the polysaccharide and lipid materials, respectively, in the VF; (2) the presence of earthworms could enhance the consumption capacity of the VF on the protein-rich material of the sewage sludge; (3) earthworms played a leading role on the nitrogen lifting of the sewage sludge, leading to the performance difference of the effluent sludge or biofilm sludge between the VF and BF; (4) in the VF, nitrogen-isotope accumulation in either biofilms or earthworms happened more significantly in the lower layer than in the upper one, while nitrogen transfer of sewage sludge happened more significantly in the upper layer than in the lower one; (5) earthworms improved the feeding environment of organisms (microorganisms in biofilms, moth fly larvae, Limacidaes, and Lymnaeidaes); (6) biofilms, Limacidaes, and moth fly larvae performed better than leeches, Lymnaeidaes, and moth fly adults at nitrogen transfer of sewage sludge.


Vermifilter Sewage sludge Biopolymeric carbon Stable isotope Nitrogen transfer Earthworm 





conventional biofilter without earthworms


the biopolymeric carbon


the lipid part of BPC


the protein part of BPC


the carbohydrate part of BPC


the influent sewage sludge


the effluent sludge of the BF


the effluent sludge of the VF


the biofilm sludge of the BF


the biofilm sludge of the VF


the casts of earthworms in the VF



This study was funded by National Key R&D Program of China (2016YFC0400805) and the National Natural Science Foundation of China (51679168).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Braun A, Auerswald K, Vikari A, Schnyder H (2013) Dietary protein content affects isotopic carbon and nitrogen turnover. Rapid Commun Mass Spectrom 27:2676–2684. CrossRefGoogle Scholar
  2. Briones MJI, Bol R, Sleep D, Allen D, Sampedro L (2001) Spatio-temporal variation of stable isotope ratios in earthworms under grassland and maize cropping systems. Soil Biol Biochem 33:1673–1682. CrossRefGoogle Scholar
  3. Cividanes S, Incera M, López J (2002) Temporal variability in the biochemical composition of sedimentary organic matter in an intertidal flat of the Galician coast (NW Spain). Oceanol Acta 25:1–12. CrossRefGoogle Scholar
  4. Curry JP, Schmidt O (2007) The feeding ecology of earthworms – a review. Pedobiologia 50:463–477. CrossRefGoogle Scholar
  5. Deniro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  6. Di W, Xing M (2018) Study on the biomass and size spectra of bio-particles in vermifilter biofilms. Sci Total Environ 636:891–900. CrossRefGoogle Scholar
  7. Di W, Xing M, Yang J (2016) Investigation on the difference between biofilm morphologies of the vermifilter and conventional biofilter with the flow cytometer. Bioresour Technol 216:308–316. CrossRefGoogle Scholar
  8. Driscoll ZG, Bootsma HA, Christiansen E (2015) Zooplankton trophic structure in Lake Michigan as revealed by stable carbon and nitrogen isotopes. J Great Lakes Res 41(Supplement 3):104–114. CrossRefGoogle Scholar
  9. Edwards CA (2004) Earthworm ecology. CRC Press, AmericanCrossRefGoogle Scholar
  10. Fabiano M, Danovaro R (1994) Composition of organic matter in sediments facing a river estuary (Tyrrhenian Sea): relationships with bacteria and microphytobenthic biomass. Hydrobiologia 277:71–84. CrossRefGoogle Scholar
  11. Fabiano M, Danovaro R, Fraschetti S (1995) A three-year time series of elemental and biochemical composition of organic matter in subtidal sandy sediments of the Ligurian Sea (northwestern Mediterranean). Cont Shelf Res 15:1453–1469. CrossRefGoogle Scholar
  12. Fry B (2007) Stable isotope ecology. Springer, New YorkGoogle Scholar
  13. Haines EB, Montague CL (1979) Food sources of estuarine invertebrates analyzed using 13C/12C ratios. Ecology 60:48–56. CrossRefGoogle Scholar
  14. Hanson RS, Phillips JA (1981) Manual of methods for general bacteriology. American Society for Microbiology, Washington D.C.Google Scholar
  15. Li XW, Xing MY, YANG J, Dai XH (2014) Earthworm eco-physiological characteristics and quantification of earthworm feeding in vermifiltration system for sewage sludge stabilization using stable isotopic natural abundance. J Hazard Mater 276:353–361. CrossRefGoogle Scholar
  16. Luque De Castro MD, Priego-Capote F (2010) Soxhlet extraction: past and present panacea. J Chromatogr 1217:2383–2389. CrossRefGoogle Scholar
  17. Ma X, Xing M, Wang Y, Xu Z, Yang J (2016) Microbial enzyme and biomass responses: deciphering the effects of earthworms and seasonal variation on treating sewage sludge. J Environ Manag 170:207–214. CrossRefGoogle Scholar
  18. MacNeil MA, Drouillard KG, Fisk AT (2006) Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Can J Fish Aquat Sci 63:345–353. CrossRefGoogle Scholar
  19. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ 15N and animal age. Geochim Cosmochim Acta 48:1135–1140. CrossRefGoogle Scholar
  20. Mirto S, Gristina M, Sinopoli M, Maricchiolo G, Genovese L, Vizzini S, Mazzola A (2012) Meiofauna as an indicator for assessing the impact of fish farming at an exposed marine site. Ecol Indic 18:468–476. CrossRefGoogle Scholar
  21. Nathanael CO, Donna LP (2001) Stable isotope composition of walleye: 15N accumulation with age and area-specific differences in δ13C. Can J Fish Aquat Sci 58(6):1253–1260. CrossRefGoogle Scholar
  22. Nifong JC, Layman CA, Silliman BR (2015) Size, sex and individual-level behaviour drive intrapopulation variation in cross-ecosystem foraging of a top-predator. J Anim Ecol 84:35–48. CrossRefGoogle Scholar
  23. Persic A, Roche H, Ramade F (2004) Stable carbon and nitrogen isotope quantitative structural assessment of dominant species from the Vaccarès Lagoon trophic web (Camargue Biosphere Reserve, France). Estuar Coast Shelf Sci 60:261–272. CrossRefGoogle Scholar
  24. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718. CrossRefGoogle Scholar
  25. Pusceddu A, Bianchelli S, Canals M, Sanchez-Vidal A, De Madron XD, Heussner S, Lykousis V, de Stigter H, Trincardi F, Danovaro R (2010) Organic matter in sediments of canyons and open slopes of the Portuguese, Catalan, Southern Adriatic and Cretan Sea margins. Deep-Sea Res I Oceanogr Res Pap 57:441–457. CrossRefGoogle Scholar
  26. Pusceddu A, Della PL, Beliaeff B (2011) Trophic status of earthen ponds used for semi-intensive shrimp (Litopenaeus stylirostris, Stimpson, 1874) farming in New Caledonia (Pacific Ocean). Mar Environ Res 72:160–171. CrossRefGoogle Scholar
  27. Sabbatini A, Bonatto S, Bianchelli S, Pusceddu A, Danovaro R, Negri A (2012) Foraminiferal assemblages and trophic state in coastal sediments of the Adriatic Sea. Mar Syst 105-108:163–174. CrossRefGoogle Scholar
  28. Schmidt O (1999) Intrapopulation variation in carbon and nitrogen stable isotope ratios in the earthworm Aporrectodea longa. Ecol Res 14:317–328. CrossRefGoogle Scholar
  29. Schmidt O, Curry JP, Dyckmans J, Rota E, Scrimgeour CM (2004) Dual stable isotope analysis (δ 13C and δ 15N) of soil invertebrates and their food sources. Pedobiologia 48:171–180. CrossRefGoogle Scholar
  30. Schmidt O, Ostle NJ (1999) Tracing nitrogen derived from slurry in earthworms using 15N/14N stable isotope ratios at natural abundances. Appl Soil Ecol 12:7–13. CrossRefGoogle Scholar
  31. Schmidt O, Scrimgeour CM, Handley LL (1997) Natural abundance of 15N and 13C in earthworms from a wheat and a wheat-clover field. Soil Biol Biochem 29:1301–1308. CrossRefGoogle Scholar
  32. Singh AP (2010) Medicinal leech therapy (Hirudotherapy): a brief overview. Complement Ther Clin 16:213–215. CrossRefGoogle Scholar
  33. Tabatabai MA (1994) Soil enzymes. In: Methods of soil analysis. Soil Science Society of America, Madison, pp 775–833Google Scholar
  34. Van den Akker B, Beard H, Kaeding U, Giglio S, Short MD (2010) Exploring the relationship between viscous bulking and ammonia-oxidiser abundance in activated sludge: A comparison of conventional and IFAS systems. Water Res 44: 2919-2929. CrossRefGoogle Scholar
  35. Van der Zanden MJ, Cabana G, Rasmussen JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ 15N) and literature dietary data. Can J Fish Aquat Sci 54:1142–1158. CrossRefGoogle Scholar
  36. Xing MY, Li XW, Yang J, Lv BY, Lu YS (2012) Performance and mechanism of vermifiltration system for liquid-state sewage sludge treatment using molecular and stable isotopic techniques. Chem Eng 197:143–150. CrossRefGoogle Scholar
  37. Xing MY, Zhao CH, Yang J, Lv BY (2014) Feeding behavior and trophic relationship of earthworms and other predators in vermifiltration system for liquid-state sludge stabilization using fatty acid profiles. Bioresour Technol 169:149–154. CrossRefGoogle Scholar
  38. Xu T, Xing MY, YANG J, Lv BY, Duan T, Nie J (2014) Tracking the composition and dominant components of the microbial community via polymerase chain reaction-denaturing gradient gel electrophoresis and fluorescence in situ hybridization during vermiconversion for liquid-state excess sludge stabilization. Bioresour. Technol. 167: 100-107. CrossRefGoogle Scholar
  39. Zhao L, Wang Y, Yang J, Xing M, Li X, Yi D, Deng D (2010) Earthworm-microorganism interactions: a strategy to stabilize domestic wastewater sludge. Water Res 44: 2572-2582. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Yangtze River Water Environment, Ministry of Education, State Key Laboratory of Pollution Control and Resources Reuse, College of Environmental Science and EngineeringTongji UniversityShanghaiChina
  2. 2.School of Chemical and Environmental EngineeringShanghai Institute of TechnologyShanghaiChina

Personalised recommendations