Environmental Science and Pollution Research

, Volume 25, Issue 31, pp 31062–31070 | Cite as

Earthworms as plug flow reactors: a first-order kinetic study on the gut of the vermicomposting earthworm Eudrilus eugeniae

  • Katheem KiyasudeenEmail author
  • Mahamad Hakimi Ibrahim
  • Syahidah Akmal Muhammad
  • Sultan Ahmed Ismail
  • Fadzil Noor Gonawan
  • Mark Harris Zuknik
Research Article


Earthworms are commonly referred as environmental engineers and their guts are often compared with chemical reactors. However, modeling experiments to substantiate it are lacking. The aim of this study was to use established reactor models, particularly PFR, on the gut of the vermicomposting earthworm Eudrilus eugeniae to understand more on its digestion. To achieve the objective, a mathematical model based on first-order kinetics was framed and used to determine the pattern of digestion rates of nutrient indicators, namely total carbon (%), total nitrogen (%), C/N ratio, 13C (‰), and 15N (‰) at five intersections (pre-intestine, foregut, midgut A, midgut B, and hindgut) along the gut of E. eugeniae. The experimental results revealed that the concentrations of TC, TN, 13C, and 15N decreased during gut transit, whereas C/N ratio increased. The first-order model demonstrated that all the nutrients exhibit a linear pattern of digestion during gut transit, which supports the PFR model. On this basis, the present study concludes that the gut of E. eugeniae functions as PFR.


Plug flow Modeling Digestion kinetics First-order Earthworm Gut 



We acknowledge Analytical Biochemistry Research Center (ABrC) at USM for providing stable isotope analysis. The first author, Katheem Kiyasudeen acknowledges USM fellowship (2015-2018) for the academic support.


This research work was supported by Universiti Sains Malaysia (USM) via RUI grant (Grant Number: 1001/PTEKIND/811254).


  1. Alexander RM (1991) Optimization of gut structure and diet for higher vertebrate herbivores. Phil Trans R Soc Lond B 333(1267):249–255CrossRefGoogle Scholar
  2. Benner R, Pakulski JD, McCarthy M, Hedges JI, Hatcher PG (1992) Bulk chemical characteristics of dissolved organic matter in the ocean. Science 255:1561–1564CrossRefGoogle Scholar
  3. Boutton TW, Arshad MA, Tieszen LL (1983) Stable isotope analysis of termite food habits in east African grasslands. Oecologia 59(1):1–6CrossRefGoogle Scholar
  4. 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(3):177–198CrossRefGoogle Scholar
  5. Curry JP, Schmidt O (2007) The feeding ecology of earthworms–a review. Pedobiologia 50(6):463–477CrossRefGoogle Scholar
  6. Dähnke K, Thamdrup B (2013) Nitrogen isotope dynamics and fractionation during sedimentary denitrification in Boknis Eck, Baltic Sea. Biogeosciences 710(5):3079–3088CrossRefGoogle Scholar
  7. Edwards CA (ed) (2004) Earthworm ecology. CRC press, Boca RatonGoogle Scholar
  8. Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms, 3rd edn. Chapman & Hall, LondonGoogle Scholar
  9. Edwards CA, Lofty JR (1972) Biology of earthworms. Report of Rothamsted Experimental Station, LondonCrossRefGoogle Scholar
  10. Fonseca MRJ (2012) An engineering understanding of the small intestine. Doctoral dissertation, University of BirminghamGoogle Scholar
  11. Frund HC, Butt K, Capowiez Y et al (2010) Using earthworms as model organisms in the laboratory: recommendations for experimental implementations. Pedobiologia 53(2):119–125CrossRefGoogle Scholar
  12. German DP (2009) Do herbivorous minnows have “plug-flow reactor” guts? Evidence from digestive enzyme activities, gastrointestinal fermentation, and luminal nutrient concentrations. J Comp Physiol B 179(6):759–771CrossRefGoogle Scholar
  13. Goswami B, Kalita MC (2000) Efficiency of some indigenous earthworms species of Assam and its characterization through vermitechnology. Indian J Environ Ecoplan 3:351–354Google Scholar
  14. Gunadi B, Blount C, Edwards CA (2002) The growth and fecundity of Eisenia fetida (Savigny) in cattle solids pre-composted for different periods. Pedobiologia 46(1):15–23CrossRefGoogle Scholar
  15. Gunya B, Masika PJ, Hugo A, Muchenje V (2016) Nutrient composition and fatty acid profiles of oven-dried and freeze-dried earthworm Eisenia foetida. J Food Nutr Res 4(6):343–348Google Scholar
  16. Hendriksen NB (1991) Gut load and food-retention time in the earthworms Lumbricus festivus and L. castaneus: a field study. Biol Fertil Soils 11(3):170–173CrossRefGoogle Scholar
  17. Hickman CP (2005) Integrated principles of zoology, 13th edn. Mcgraw-Hill, TexasGoogle Scholar
  18. Horn MH, Messer KS (1992) Fish guts as chemical reactors: a model of the alimentary canals of marine herbivorous fishes. Mar Biol 113(4):527–535CrossRefGoogle Scholar
  19. Horn MA, Schramm A, Drake HL (2003) The earthworm gut: an ideal habitat for ingested N2O-producing microorganisms. Appl Environ Microbiol 69(3):1662–1669CrossRefGoogle Scholar
  20. Hume (2002) Digestive strategies of mammals. Acta Zool Sin 48(1):1–19Google Scholar
  21. Jager T, Fleuren RH, Roelofs W, de Groot AC (2003) Feeding activity of the earthworm Eisenia andrei in artificial soil. Soil Biol Biochem 35(2):313–322CrossRefGoogle Scholar
  22. Jayakumar M, Karthikeyan V, Karmegam N (2009) Comparative studies on physico-chemical, microbiological and enzymatic activities of vermicasts of the earthworms, Eudrilus eugeniae, Lampito mauritii and Perionyx ceylanensis cultured in press mud. Int J Appl Agric Res 4(1):75–85Google Scholar
  23. Jumars PA (2000) Animal guts as nonideal chemical reactors: partial mixing and axial variation in absorption kinetics. Am Nat 155(4):544–555CrossRefGoogle Scholar
  24. Karasov HW, Douglas AE (2013) Comparative digestive physiology. Compr Physiol 3(2):741–783Google Scholar
  25. Kiyasudeen KS, Jessy RS, Ibrahim MH (2014) Earthworm’s gut as reactor in vermicomposting process: a mini review. Int J Sci Res Publ 4(7):1–6Google Scholar
  26. Kiyasudeen KS, Ibrahim MH, Ismail SA (2015) Characterization of fresh cattle wastes using proximate, microbial and spectroscopic principles. Am-Euras J Agric. Environ Sci 15(8):1700–1709Google Scholar
  27. Kiyasudeen KS, Ibrahim MH, Quaik S, Ismail SA (2016) Prospects of organic waste management and the significance of earthworms. Springer International Publishing, RotterdamGoogle Scholar
  28. Krishnamoorthy U, Sniffen CJ, Stern MD, Van Soest PJ (1983) Evaluation of a mathematical model of rumen digestion and an in vitro simulation of rumen proteolysis to estimate the rumen-undegraded nitrogen content of feedstuffs. Br J Nutr 50(3):555–568CrossRefGoogle Scholar
  29. Lazcano C, Gómez-Brandón M, Domínguez J (2008) Comparison of the effectiveness of composting and vermicomposting for the biological stabilization of cattle manure. Chemosphere 72(7):1013–1019CrossRefGoogle Scholar
  30. Levenspiel O (1972) Chemical reaction engineering, 2nd edn. Wiley, New YorkGoogle Scholar
  31. Levenspiel O (1999) Chemical reaction engineering. Ind Eng Chem Res 38(11):4140–4143CrossRefGoogle Scholar
  32. Majeed A, Hwang HG, Connolly SJ, Eikelboom JW, Ezekowitz MD, Wallentin L, Brueckmann M, Fraessdorf M, Yusuf S, Schulman S (2013) Management and outcomes of major bleeding during treatment with dabigatran or warfarin. Circulation 128(21):2325–2332CrossRefGoogle Scholar
  33. Mba CC (1989) Biomass and vermicompost production by the earthworm Eudrilus eugeniae (Kinberg). Rev Biol Trop 37(1):11–13Google Scholar
  34. Ndegwa PM, Thompson SA, Das KC (2000) Effects of stocking density and feeding rate on vermicomposting of biosolids. Bioresour Technol 71(1):5–12CrossRefGoogle Scholar
  35. Penry DL, Jumars PA (1986) Chemical reactor analysis and optimal digestion. Bioscience 36(5):310–315CrossRefGoogle Scholar
  36. Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129(1):69–96CrossRefGoogle Scholar
  37. Peter SDJ, Siu MT, Marcus AH, Harold LD (2013) Emission of nitrous oxide and dinitrogen by diverse earthworm families from Brazil and resolution of associated denitrifying and nitrate-dissimilating taxa. FEMS Microbiol Ecol 83(2):375–391CrossRefGoogle Scholar
  38. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18(1):293–320CrossRefGoogle Scholar
  39. Rupani PF, Embrandiri A, Ibrahim MH, Shahadat M, Hansen SB, Ismail SA, Ab. Kadir MO (2017) Recycling of palm oil industrial wastes using vermicomposting technology: its kinetics study and environmental application. Environ Sci Pollut Res 24(14):12982–12990CrossRefGoogle Scholar
  40. Sampedro L, Whalen JK (2007) Changes in the fatty acid profiles through the digestive tract of the earthworm Lumbricus terrestris L. Appl Soil Ecol 35(1):226–236CrossRefGoogle Scholar
  41. 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(1):7–13CrossRefGoogle Scholar
  42. 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 29:1301–1308CrossRefGoogle Scholar
  43. Schnell S, Mendoza C (2000) Enzyme kinetics of multiple alternative substrates. J Math Chem 27(1–2):155–170CrossRefGoogle Scholar
  44. Schönholzer 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(3):235–248CrossRefGoogle Scholar
  45. Schulz K, Hunger S, Brown GG, Tsai SM, Cerri CC, Conrad R, Drake HL (2015) Methanogenic food web in the gut contents of methaneemitting earthworm Eudrilus eugeniae from Brazil. ISME J 9(8):1778–1792CrossRefGoogle Scholar
  46. Srividhya J, Schnell S (2006) Why substrate depletion has apparent first-order kinetics in enzymatic digestion. Comput Biol Chem 30(3):209–214CrossRefGoogle Scholar
  47. Sruthy PB, Anjana JC, Rathinamala J, Jayashree S (2013) Screening of earthworm (Eudrilus eugeniae) gut as a transient microbial habitat. Advances in Zoology and Botany 1(3):53–56Google Scholar
  48. Taylor GB (1917) Experiments on determination of cow manure in milk; moisture content and solubility of cow Manure1. J Dairy Sci 1(4):303–312CrossRefGoogle Scholar
  49. Tillinghast EK, MacDonnell PC (1973) The distribution of ammonia-generating enzymes along the intestine of the earthworm, Lumbricus terrestris L. J Exp Zool A Ecol Genet Physiol 185(2):153–158Google Scholar
  50. Van Bentum R, Nelson MI (2011) Modelling the passage of food through an animal stomach: a chemical reactor engineering approach. Chem Eng J 166(1):315–323CrossRefGoogle Scholar
  51. Van Gansen P, Brien P (1962) Structures et fonctions du tube digestif du lombric Eisenia foetida Savigny. J Microsc, p 120Google Scholar
  52. Vivas A, Moreno B, Garcia-Rodriguez S, Benitez E (2009) Assessing the impact of composting and vermicomposting on bacterial community size and structure, and microbial functional diversity of an olive-mill waste. Bioresour Technol 100(3):1319–1326CrossRefGoogle Scholar
  53. Whalen JK, Paustian KH, Parmelee RW (1999) Simulation of growth and flux of carbon and nitrogen through earthworms. Pedobiologia 43(6):537–546Google Scholar
  54. Wolesensky W, Joern A, Logan JD (2005) A model of digestion modulation in grasshoppers. Ecol Model 188(2):358–373CrossRefGoogle Scholar
  55. Woods HA, Kingsolver JG (1999) Feeding rate and the structure of protein digestion and absorption in lepidopteran midguts. Arch Insect Biochem Physiol 42(1):74–87CrossRefGoogle Scholar
  56. Zhang BG, Rouland C, Lattaud C, Lavelle P (1993) Activity and origin of digestive enzymes in gut of the tropical earthworm Pontoscolex corethrurus. Eur J Soil Biol 29(1):7–11Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.School of Industrial Technology, Environmental Technology DivisionUniversity Sains MalaysiaPenangMalaysia
  2. 2.Analytical Biochemistry Research Centre (ABrC)Universiti Sains MalaysiaPenangMalaysia
  3. 3.Ecoscience Research FoundationChennaiIndia
  4. 4.School of Chemical Engineering, Engineering CampusUniversiti Sains MalaysiaPenangMalaysia

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