Environmental Science and Pollution Research

, Volume 25, Issue 36, pp 35811–35820 | Cite as

Recycling of wastes from fish beneficiation by composting: chemical characteristics of the compost and efficiency of their humic acids in stimulating the growth of lettuce

  • Jader Galba BusatoEmail author
  • Caroline Moreira de Carvalho
  • Daniel Basilio Zandonadi
  • Fernando Fabriz Sodré
  • Alan Ribeiro Mol
  • Aline Lima de Oliveira
  • Rodrigo Diana Navarro
Sustainable Waste Management


Waste from the beneficiation of fish was composted with crushed grass aiming to characterize their chemical composition and investigate the possibility of the use of the final compost as source of humic acids (HA) able to stimulate the growth of lettuce. Compost presented pH value, C/N ratio, and electrical conductivity that allow its use as an organic fertilizer. The element content was present in the following order of abundance in the compost: P > Ca > N > Mg > K > Fe > Zn > Mn > Mo > Cu, and the humus composition was similar to that observed in others kind of organic residues composted. The high content of oxygen pointed out a high level of oxidation of HA, in line with the predominance of phenolic acidity in the functional groups. The 13C-NMR spectra showed marked resonances due to the presence of lipids and other materials resistant to degradation as methoxy substituent and N-alkyl groups. A concentration of 20 mg L−1 HA increased significantly both dry and wet root matter in lettuce but the CO2 assimilation, stomatal conductance, and number of lateral roots of the plants were not affected. However, increases of 64% in the water-use efficiency was observed due to the HA addition, probably related to the root morphology alteration which resulted in 1.6-fold increase of lateral root average length and due to the higher H+ extrusion activity. Reuse of residues from the fish beneficiation activity by composting may represent a safe tool to increase the value of recycled organic residues and generate HA with potential use as plant growth stimulants.


Organic residue Plant growth Root development Photosynthetic rate Water-use efficiency 


Funding information

This research was supported by the Ministry of Science and Technology of Brazil (CNPq 475152/2012-3).


  1. Aguiar NO, Olivares FL, Novotny EH, Dobbss LB, Martinez-Balmori D, Santos-Júnior LG, Chagas JG, Façanha AR, Canellas LP (2013) Bioactivity of humic acids isolated from vermicomposts at different maturation stages. Plant Soil 362:161–174CrossRefGoogle Scholar
  2. Alenazi M, Wahb-Allah MA, Abdel-Razzak HS, Ibrahim AA, Alsadon A (2016) Water regimes and humic acid application influences potato growth, yield, tuber quality and water use efficiency. Am J Potato Res 93:463–473CrossRefGoogle Scholar
  3. Arslan EI, Ünlü A, Topal M (2011) Determination of the effect of aeration rate on composting of vegetable–fruit wastes. Clean–Soil Air Water 39:1014–1021CrossRefGoogle Scholar
  4. Baldock JA, Oades JM, Waters AG, Peng X, Vassalo AM, Wilson MA (1992) Aspects of the chemical structure of soil organic materials as revealed by solid-state 13C NMR spectroscopy. Biogeochemistry 16:1–42CrossRefGoogle Scholar
  5. Brock TD, Madigan MT, Martinko JM, Parker J (1994) Biology of microorganism. Prentice-Hall, Englewood CliffsGoogle Scholar
  6. Busato JG, Zandonadi DB, Dobbss LB, Façanha AR, Canellas LP (2010) Humic substances isolated from residues of sugar cane industry as root growth promoter. Sci Agric 67:206–212CrossRefGoogle Scholar
  7. Busato JG, Papa G, Canellas LP, Adani F, Oliveira AL, Leão TP (2016) Phosphatase activities and its relationship with physical and chemical parameters during vermicomposting of filter cake and cattle manure. J Sci Food Agric 96:1223–1230CrossRefGoogle Scholar
  8. Canellas LP, Okorokova-Façanha A, Olivares FL, Façanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957CrossRefGoogle Scholar
  9. Certini G, Vestgarden LS, Forte C, Strand LT (2014) Litter decomposition rate and soil organic matter quality in a patchwork heathland of Southern Norway. Soil Discuss 1:267–294CrossRefGoogle Scholar
  10. Fan H, Wang X, Suna X, Lia Y, Sun X, Zheng C (2014) Effects of humic acid derived from sediments on growth, photosynthesis and chloroplast ultrastructure in chrysanthemum. Sci Hortic 177:118–123CrossRefGoogle Scholar
  11. Feleafel MN, Mirdad ZM (2014) Ameliorating tomato productivity and water-use efficiency under water salinity. J Anim Plant Sci 24:302–309Google Scholar
  12. Fourti O, Jedidi N, Hassen A (2010) Humic substances change during the co-composting process of municipal solid wastes and sewage sludge. World J Microbiol Biotechnol 26:2117–2122CrossRefGoogle Scholar
  13. García AC, Tavares OCH, Balmori DM, Almeida VS, Canellas LP, García-Mina JM, Berbara RLL (2016) Structure-function relationship of vermicompost humic fractions for use in agriculture. J Soils Sediments 1:1–11Google Scholar
  14. Hayes MHB (2006) Solvent systems for the isolation of organic components from soil. Soil Sci Soc Am J 70:986–994CrossRefGoogle Scholar
  15. Hernandez OL, Garcia AC, Huelva R, Martínez-Balmori D, Guridi F, Aguiar NO, Olivares FL, Canellas LP (2015) Humic substances from vermicompost enhance urban lettuce production. Agron Sustain Dev 35:225–232CrossRefGoogle Scholar
  16. Heslin A (2015) Sustainable agriculture. Inter Encycl Soc B Sci 23:807–811Google Scholar
  17. Iglesias Jiménez E, Perez Garcia V (1989) Evaluation of city refuse compost maturity: a review. Biol Wastes 27:115–142CrossRefGoogle Scholar
  18. Illera-Vives M, Labandeira SS, López-Mosquera ME (2013) Production of compost from marine waste: evaluation of the product for use in ecological agriculture. Phycologia 25:1395–1403Google Scholar
  19. Illera-Vives M, Seoane LS, Brito LM, López-Fabal A, López-Mosquera ME (2015) Evaluation of compost from seaweed and fish waste as a fertilizer for horticultural use. Sci Hortic 186:101–107CrossRefGoogle Scholar
  20. du Jardin P (2012) The science of plant biostimulants—a bibliographic analysis. Contract 30-CE0455515/00-96, ad hoc study on bio-stimulants products.
  21. du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic 196:3–14CrossRefGoogle Scholar
  22. Lang T, Barling D (2012) Food security and food sustainability: reformulating the debate. Geogr J 178:313–326CrossRefGoogle Scholar
  23. Lazcano C, Gómez-Brandón M, Domínguez J (2008) Comparison of the effectiveness of composting and vermicomposting for the biological stabilization of cattle manure. Chemosphere 72:1013–1019CrossRefGoogle Scholar
  24. Lim SL, Wu TY, Lim PN, Shak KPY (2015) The use of vermicompost in organic farming: overview, effects on soil and economics. J Sci Food Agric 95:11143–11156CrossRefGoogle Scholar
  25. Maji D, Misra P, Singh S, Kalra A (2017) Humic acid rich vermicompost promotes plant growth by improving microbial community structure of soil as well as root nodulation and mycorrhizal colonization in the roots of Pisum sativum. Appl Soil Ecol 110:97–108CrossRefGoogle Scholar
  26. Martinez DE, Luquez VM, Bartoli CG, Guiamét JJ (2003) Persistence of photosynthetic components and photochemical efficiency in ears of water-stressed wheat (Triticum aestivum). Physiol Plant 119:519–525CrossRefGoogle Scholar
  27. Martinez-Balmori D, Spaccini R, Aguiar NO, Novotny EH, Olivares FL, Canellas LP (2014) Molecular characteristics of humic acids isolated from vermicomposts and their relationship to bioactivity. J Agric Food Chem 62:11412–11419CrossRefGoogle Scholar
  28. Mitchell A (1997) Production of Eisenia fetida and vermicompost from feed-lot cattle manure. Soil Biol Biochem 29:763–766Google Scholar
  29. Olaetxea M, Mora V, Bacaicoa E, Garnica M, Fuentes M, Casanova E, Gonzalo R (2015) Abscisic acid regulation of root hydraulic conductivity and aquaporin gene expression is crucial to the plant shoot growth enhancement caused by rhizosphere humic acids. Plant Physiol 169:2587–2596Google Scholar
  30. Olivares FL, Aguiar NO, Rosa RCC, Canellas LP (2015) Substrate biofortification in combination with foliar sprays of plant growth promoting bacteria and humic substances boosts production of organic tomatoes. Sci Hortic 183:100–108CrossRefGoogle Scholar
  31. Ottinger M, Clauss K, Kuenzer C (2016) Aquaculture: relevance, distribution, impacts and spatial assessments—a review. Ocean Coast Manag 119:244–266CrossRefGoogle Scholar
  32. Rayle DL, Cleland RE (1992) The acid growth theory of auxin induced cell elongation is alive and well. Plant Physiol 99:1271–1274CrossRefGoogle Scholar
  33. Reijnders L (2014) Phosphorus resources, their depletion and conservation, a review. Resour Conserv Recycl 93:32–49CrossRefGoogle Scholar
  34. Rice JA, MacCarthy P (1991) Statistical evaluation of the elemental composition of humic substances. Org Geochem 17:635–648CrossRefGoogle Scholar
  35. Rodda MRC, Canellas LP, Façanha AR, Zandonadi DB, Guerra JGM, Almeida DL, Santos GA (2006) Improving lettuce seedling root growth and ATP hidrolysis with humates from vermicompost. I. Effect of vermicompost concentration. Rev Bras Cienc Solo 30:649–656CrossRefGoogle Scholar
  36. Sadeghi-Shoae M, Paknejad F, Darvishi HH, Mozafari H, Moharramzadeh M, Tookalloo MR (2013) Effect of intermittent furrow irrigation, humic acid and deficit irrigation on water use efficiency of sugar beet. Ann Biol Res 4:187–193Google Scholar
  37. Sanes FSM, Strassburger AS, Araújo FB, Medeiros CAB (2015) Compostagem e fermentação de resíduos de pescado para produção de fertilizantes orgânicos. Semina 36:1241–1252Google Scholar
  38. Saranya R, Prasanna R, Jayapriya J, Aravindhan R, Tamil Selvi A (2016) Value addition of fish waste in the leather industry for dehairing. J Clean Prod 118:179–186CrossRefGoogle Scholar
  39. SAS, SAS/STAT (1999) User’s guide,version 8. SAS Institute, CaryGoogle Scholar
  40. Schnitzer M, Gupta UC (1965) Determination of acidity in soil organic matter. Soil Sci Am Soc Proc 29:274–277CrossRefGoogle Scholar
  41. Tahiri A, Delporte F, Muhovski Y, Ongena M, Thonart P, Druart P (2016) Change in ATP-binding cassette B1/19, glutamine synthetase and alcohol dehydrogenase gene expression during root elongation in Betula pendula Roth and Alnus glutinosa L. Gaertn in response to leachate and leonardite humic substances. Plant Physiol Biochem 98:25–38CrossRefGoogle Scholar
  42. Vaccaro S, Muscolo A, Pizzeghello D, Spaccini R, Piccolo A, Nardi S (2009) Effect of a compost and its water-soluble fractions on key enzymes of nitrogen metabolism in maize seedlings. J Agric Food Chem 57:11267–11276CrossRefGoogle Scholar
  43. Yeomans JC, Bremner JA (1988) A rapid and precise method for routine determination of organic carbon in soil. Commun Soil Sci Plant Anal 19:1467–1476CrossRefGoogle Scholar
  44. Zandonadi DB, Santos MP, Dobbss LB, Olivares FL, Canellas LP, Binzel ML, Okorokova-Façanha AL, Façanha AR (2010) Nitric oxide mediates humic acids-induced root development and plasma membrane H+-ATPase activation. Planta 231:1025–1036CrossRefGoogle Scholar
  45. Zandonadi DB, Santos MP, Caixeta LS, Marinho EB, Peres LEP, Façanha AR (2016) Plant proton pumps as markers of biostimulant action. Sci Agric 73:24–28CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Jader Galba Busato
    • 1
    Email author
  • Caroline Moreira de Carvalho
    • 1
  • Daniel Basilio Zandonadi
    • 2
  • Fernando Fabriz Sodré
    • 3
  • Alan Ribeiro Mol
    • 3
  • Aline Lima de Oliveira
    • 3
  • Rodrigo Diana Navarro
    • 1
  1. 1.Faculdade de Agronomia e Medicina Veterinária, Campus Universitário Darcy RibeiroUniversidade de BrasíliaBrasíliaBrazil
  2. 2.Laboratório de Biotecnologia Vegetal, Núcleo de Pesquisas em Ecologia e Desenvolvimento Sócio-ambientalUniversidade Federal do Rio de JaneiroMacaéBrazil
  3. 3.Instituto de QuímicaCampus Universitário Darcy Ribeiro, Universidade de BrasíliaBrasíliaBrazil

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