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Resistance of black soldier fly (Diptera: Stratiomyidae) larvae to combined heavy metals and potential application in municipal sewage sludge treatment

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Abstract

Treating municipal sewage sludge (MSS) sustainably and economically in China remains a challenge because of risks associated with the heavy metals it contains. In this study, black solider fly larvae (BSFL) were used for MSS treatment. The resistance of larvae to combined heavy metals and their potential use in conversion of MSS were investigated. The results indicated that seven MSS samples contained large amounts of heavy metals, with the lead and nickel contents of several samples exceeding Chinese national discharge standards. BSFL were highly tolerant to an artificial diet spiked with combined heavy metals. Principal component analysis revealed that high concentrations of lead, nickel, boron, and mercury potentially interfered with larval weight gain, while zinc, copper, chromium, cadmium, and mercury slightly reduced larval survival. The addition of chicken manure and wheat bran as co-substrates improved the conversion process, which was influenced by the nature and amount of added co-substrate and especially the quantity of nitrogen added. With the amended substrate, the BSFL accumulated heavy metals into their bodies but not into extracted larval oil. The heavy metal content of the treatment residue was lower than that considered safe for organic-inorganic compound fertilizers standards in China and the harvested larvae could be used as a source of oil for industrial application.

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References

  • Ajeej A, Thanikal JV, Narayanan CM, Senthil Kumar R (2015) An overview of bio augmentation of methane by anaerobic co-digestion of municipal sludge along with microalgae and waste paper. Renew Sust Energ Rev 50:270–276

    Article  CAS  Google Scholar 

  • Borowska J, Sulima B, Nilińska M, Pyza E (2004) Heavy metal accumulation and its effects on development, survival and immuno-competent cells of the housefly Musca domestica from closed laboratory populations as model organism. Fresenius Environ Bull 13:1402–1409

    CAS  Google Scholar 

  • Budych-Gorzna M, Smoczynski M, Oleskowicz-Popiel P (2016) Enhancement of biogas production at the municipal wastewater treatment plant by co-digestion with poultry industry waste. Appl Energ 161:387–394

    Article  CAS  Google Scholar 

  • Chen M, Li X-m, Yang Q, Zeng G-m, Zhang Y, Liao D-x, Liu J-j, Hu J-m, Guo L (2008) Total concentrations and speciation of heavy metals in municipal sludge from Changsha, Zhuzhou and Xiangtan in middle-south region of China. J Hazard Mater 160:324–329

    Article  CAS  Google Scholar 

  • Čičková H, Newton GL, Lacy RC, Kozánek M (2015) The use of fly larvae for organic waste treatment. Waste Manag 35:68–80

    Article  Google Scholar 

  • Dede G, Ozdemir S (2016) Effects of elemental sulphur on heavy metal uptake by plants growing on municipal sewage sludge. J Environ Manag 166:103–108

    Article  CAS  Google Scholar 

  • Diener S, Zurbrügg C, Tocknera K (2009) Conversion of organic material by black soldier fly larvae—establishing optimal feeding rates. Waste Manag Res 27:603–610

    Article  CAS  Google Scholar 

  • Diener S, Studt Solano NM, Roa Gutiérrez F, Zurbrügg C, Tockner K (2011) Biological treatment of municipal organic waste using black soldier fly larvae. Waste Biomass Valori 2:357–363

    Article  CAS  Google Scholar 

  • Diener S, Zurbrügg C, Tockner K (2015) Bioaccumulation of heavy metals in the black soldier fly, Hermetia illucens and effects on its life cycle. J Insects Food Feed 1:261–270

    Article  Google Scholar 

  • Dzulkurnain Z, Hassan MA, Zakaria MR, Wahab PEM, Hasan MY, Shirai Y (2017) Co-composting of municipal sewage sludge and landscaping waste: a pilot scale study. Waste Biomass Valori 8:695–705

    Article  CAS  Google Scholar 

  • Gao M, Liang F, Yu A, Li B, Yang L (2009) Evaluation of stability and maturity during forced-aeration composting of chicken manure and sawdust at different C/N ratios. Chemosphere 78:614–619

    Article  Google Scholar 

  • Hsu L-C, Huang C-Y, Chuang Y-H, Chen H-W, Chan Y-T, Teah HY, Chen T-Y, Chang C-F, Liu Y-T, Tzou Y-M (2016) Accumulation of heavy metals and trace elements in fluvial sediments received effluents from traditional and semiconductor industries. Sci Rep-UK 6:34250

    Article  CAS  Google Scholar 

  • Hung CV, Cam BD, Mai PTN, Dzung BQ (2015) Heavy metals and polycyclic aromatic hydrocarbons in municipal sewage sludge from a river in highly urbanized metropolitan area in Hanoi, Vietnam: levels, accumulation pattern and assessment of land application. Environ Geochem Health 37:133–146

    Article  CAS  Google Scholar 

  • Lalander C, Diener S, Magri ME, Zurbrügg C, Lindström A, Vinnerås B (2013) Faecal sludge management with the larvae of the black soldier fly (Hermetia illucens)—from a hygiene aspect. Sci Total Environ 458–460:312–318

    Article  Google Scholar 

  • Lalander CH, Fidjeland J, Diener S, Eriksson S, Vinnerås B (2014) High waste-to-biomass conversion and efficient salmonella spp. reduction using black soldier fly for waste recycling. Agron Sustain Dev 35:261–271

    Article  Google Scholar 

  • Li Q, Zheng L, Qiu N, Cai H, Tomberlin JK, Yu Z (2011) Bioconversion of dairy manure by black soldier fly (Diptera: Stratiomyidae) for biodiesel and sugar production. Waste Manag 31:1316–1320

    Article  CAS  Google Scholar 

  • Li W, Li Q, Zheng L, Wang Y, Zhang J, Yu Z, Zhang Y (2015) Potential biodiesel and biogas production from corncob by anaerobic fermentation and black soldier fly. Bioresour Technol 194:276–282

    Article  CAS  Google Scholar 

  • Liu J, Chen J, Huang L (2015) Heavy metal removal from MSS fly ash by thermal and chlorination treatments. Sci Rep-UK 5:17270

    Article  CAS  Google Scholar 

  • Milinovic J, Vidal M, Lacorte S, Rigol A (2014) Leaching of heavy metals and alkylphenolic compounds from fresh and dried sewage sludge. Environ Sci Pollut R 21:2009–2017

    Article  CAS  Google Scholar 

  • Nakamura S, Ichiki TR, Shimoda M, Morioka S (2016) Small-scale rearing of the black soldier fly, Hermetia illucens (Diptera: Stratiomyidae), in the laboratory: low-cost and year-round rearing. Appl Entomol Zool 51:161–166

    Article  Google Scholar 

  • Ogunwande GA, Osunade JA, Adekalu KO, Ogunjimi LA (2008) Nitrogen loss in chicken litter compost as affected by carbon to nitrogen ratio and turning frequency. Bioresour Technol 99:7495–7503

    Article  CAS  Google Scholar 

  • Parra Paz AS, Carrejo NS, Gómez Rodríguez CH (2015) Effects of larval density and feeding rates on the bioconversion of vegetable waste using black soldier fly larvae Hermetia illucens (L.), (Diptera: Stratiomyidae). Waste Biomass Valori 6:1059–1065

    Article  Google Scholar 

  • Peng C, Cai Y, Wang T, Xiao R, Chen W (2016) Regional probabilistic risk assessment of heavy metals in different environmental media and land uses: an urbanization-affected drinking water supply area. Sci Rep-UK 6:37084

    Article  CAS  Google Scholar 

  • Popa R, Green TR (2012) Using black soldier fly larvae for processing organic leachates. J Econ Entomol 105:374–378

    Article  Google Scholar 

  • Ščančar J, Milačič R, Stražar M, Burica O (2000) Total metal concentrations and partitioning of Cd, Cr, Cu, Fe, Ni and Zn in sewage sludge. Sci Total Environ 250:9–19

    Article  Google Scholar 

  • Shamuyarira KK, Gumbo JR (2014) Assessment of heavy metals in municipal sewage sludge: a case study of Limpopo province, South Africa. Int J Environ Res Public Health 11:2569–2579

    Article  CAS  Google Scholar 

  • Sheppard DC, Tomberlin JK, Joyce JA, Kiser BC, Sumner SM (2002) Rearing methods for the black soldier fly (Diptera: Stratiomyidae). J Med Entomol 39:695–698

    Article  Google Scholar 

  • Tandukar M, Pavlostathis SG (2015) Co-digestion of municipal sludge and external organic wastes for enhanced biogas production under realistic plant constraints. Water Res 87:432–445

    Article  CAS  Google Scholar 

  • Wang C, Hu X, Chen M-L, Y-H W (2005) Total concentrations and fractions of Cd, Cr, Pb, Cu, Ni and Zn in sewage sludge from municipal and industrial wastewater treatment plants. J Hazard Mater 119:245–249

    Article  CAS  Google Scholar 

  • Weng H-X, Ma X-W, F-X F, Zhang J-J, Liu Z, Tian L-X, Liu C (2014) Transformation of heavy metal speciation during sludge drying: mechanistic insights. J Hazard Mater 265:96–103

    Article  CAS  Google Scholar 

  • Xiao Z, Yuan X, Jiang L, Chen X, Li H, Zeng G, Leng L, Wang H, Huang H (2015) Energy recovery and secondary pollutant emission from the combustion of co-pelletized fuel from municipal sewage sludge and wood sawdust. Energy 91:441–450

    Article  CAS  Google Scholar 

  • Zheng L, Hou Y, Li W, Yang S, Li Q, Yu Z (2012a) Biodiesel production from rice straw and restaurant waste employing black soldier fly assisted by microbes. Energy 47:225–229

    Article  CAS  Google Scholar 

  • Zheng L, Li Q, Zhang J, Yu Z (2012b) Double the biodiesel yield: rearing black soldier fly larvae, Hermetia illucens, on solid residual fraction of restaurant waste after grease extraction for biodiesel production. Renew Energ 41:75–79

    Article  CAS  Google Scholar 

  • Zheng L, Crippen TL, Holmes L, Singh B, Pimsler ML, Benbow ME, Tarone AM, Dowd S, Yu Z, Vanlaerhoven SL, Wood TK, Tomberlin JK (2013) Bacteria mediate oviposition by the black soldier fly, Hermetia illucens (L.), (Diptera: Stratiomyidae). Sci Rep-UK 3:2563

    Article  Google Scholar 

  • Zhou F, Tomberlin JK, Zheng L, Yu Z, Zhang J (2013) Developmental and waste reduction plasticity of three black soldier fly strains (Diptera: Stratiomyidae) raised on different livestock manures. J Med Entomol 50:1224–1230

    Article  Google Scholar 

Download references

Acknowledgements

The authors kindly acknowledge Dr. Linda S. Thomashow from the USDA-ARS (in USA) for the manuscript revision.

Funding

This work is supported in part by grants from the National Natural Science Foundation of China (41603110), The Special Fund for Agro-scientific Research in the Public Interest from the Ministry of Agriculture, China (201303094), and Postdoctoral Science Foundation of China (2015M572165).

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Correspondence to Jibin Zhang.

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Responsible editor: Philippe Garrigues

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Cai, M., Hu, R., Zhang, K. et al. Resistance of black soldier fly (Diptera: Stratiomyidae) larvae to combined heavy metals and potential application in municipal sewage sludge treatment. Environ Sci Pollut Res 25, 1559–1567 (2018). https://doi.org/10.1007/s11356-017-0541-x

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