Changes in speciation, mobility and bioavailability of Cd, Cr and As during the transformation process of pig manure by black soldier fly larvae (Hermetia illucens)

doi:10.1016/S2095-3119(20)63333-0

摘要/Abstract

摘要： 黑水虻幼虫（Hermetia illucens）处理畜禽粪便是一种新兴技术，处理产物虫体和虫粪可分别作为动物饲料和有机肥料，然而粪便中残留的重金属会对黑水虻转化过程产生不利影响。本文研究了Cd、Cr、As在黑水虻转化猪粪过程中对黑水虻幼虫生长的影响，以及重金属迁移和形态变化规律。结果表明，As显著降低了黑水虻幼虫的生物量，而Cr和Cd对幼虫的生长无明显影响。黑水虻幼虫对Cd的生物富集系数（BAFs：2.8-3.7）显著高于Cr（0.44-0.62）和As（0.43-0.45）。在黑水虻幼虫转化猪粪过程中，猪粪中的重金属主要迁移到黑水虻的虫粪中，Cd、Cr、As在虫粪中的残留比例分别为52.6-62.0%、90.3-94.2%和93.0-93.3%。转化后，虫粪中Cd含量显著低于猪粪，而Cr和As的含量与猪粪无显著差异（添加150 mg kg^-1 Cr处理除外）。与猪粪相比，虫粪中的重金属形态（弱酸溶解态、可还原态、可氧化态和残留态）均有明显变化。其中虫粪中Cr的可还原态含量降低，但可氧化态比例增加。Cd主要以弱酸溶解态和还原态存在于猪粪和虫粪中。虫粪中As的弱酸溶解态和还原态比例降低。猪粪经过黑水虻转化后，Cr的生物有效性降低了17.3-23.1%， Cd和As的生物有效性无明显变化（CK组的As除外）。这些发现有助于我们了解黑水虻幼虫在畜禽粪便生物转化过程中的作用以及对转化产物的安全利用。

Abstract:

The black soldier fly larvae (BSFL) (Hermetia illucens) are a good candidate for poultry and livestock manure treatment. The harvested insect bodies and feces can be used as animal feed and organic fertilizer. However, heavy metals have a negative impact on the transformation process of the manure by BSFL. Here we evaluated the effects of Cd, Cr and As in pig manure on the growth of BSFL, as well as the mobility and changes in speciation of the metals during the transformation process. The results showed that As significantly reduced the weight of BSFL, but Cr and Cd had no significant effects on BSFL growth. The bioaccumulation factors (BAFs) at various concentrations of Cd (2.8–3.7) were significantly higher than those of Cr (0.44–0.62) and As (0.43–0.45). The heavy metals in pig manure were mainly transferred to BSFL feces, and the distribution percentages of Cd, Cr and As in the BSFL feces were 52.6–62.0%, 90.3–94.2% and 93.0–93.3%, respectively. Cd concentrations in BSFL feces were significantly lower than those in the pig manure, while there were no significant differences in the concentrations of Cr and As between BSFL feces and pig manure (except for the treatment with the addition of 150 mg Cr kg^–1). The metal speciation (weak acid soluble, reducible, oxidizable and residual fractions) in BSFL feces obviously changed when compared with pig manure. In BSFL feces, the reducible proportion of Cr decreased while the oxidizable proportion increased. Cd mainly existed in the weak acid soluble and reducible states in pig manure and BSFL feces. For As, the proportions of weak acid soluble and reducible states decreased in BSFL feces. After the BSFL transformation process, the bioavailable fraction of Cr decreased by 17.3–23.1%, but those of Cd and As did not change significantly, except for As in the CK group. These findings contribute to our understanding of the roles of BSFL during the biotransformation process of livestock manure as well as the safe utilization of transformed products.

Key words: black soldier fly , heavy metal , mobility , speciation , pig manure

. [J]. Journal of Integrative Agriculture, 2021, 20(5): 1157-1166.

WANG Xiao-bo, WU Nan, CAI Rui-jie, GENG Wei-na, XU Xiao-yan. Changes in speciation, mobility and bioavailability of Cd, Cr and As during the transformation process of pig manure by black soldier fly larvae (Hermetia illucens)[J]. Journal of Integrative Agriculture, 2021, 20(5): 1157-1166.

参考文献

Afazeli H, Jafari A, Rafiee S, Nosrati M. 2014. An investigation of biogas production potential from livestock and slaughterhouse wastes. Renewable and Sustainable Energy Reviews, 34, 380–386.
Al-Momani F A, Massadeh A M. 2005. Effect of different heavy-metal concentrations on Drosophila melanogaster larval growth and development. Biological Trace Element Research, 108, 271–277.
Biancarosa I, Liland N S, Biemans D, Araujo P, Bruckner C G, Waagbø R. 2018. Uptake of heavy metals and arsenic in black soldier fly (Hermetia illucens) larvae grown on seaweed-enriched media. Journal of the Science of Food and Agriculture, 98, 2176–2183.
Blanes-Vidal V, Suh H, Nadimi E S, Løfstrømd P, Ellermann T, Andersen H V, Schwartzb J. 2012. Residential exposure to outdoor air pollution from livestock operations and perceived annoyance among citizens. Environment International, 40, 44–50 .
Braeckman B, Smagghe G, Brutsaert N, Cornelis R, Raes H. 1999. Cadmium uptake and defense mechanism in insect cells. Environmental Research, 80, 231–243.
Cai M, Hu R, Zhang K, Ma S, Zheng L, Yu Z, Zhang J. 2018a. Resistance of black soldier fly (Diptera: Stratiomyidae) larvae to combined heavy metals and potential application in municipal sewage sludge treatment. Environmental Science and Pollution Research, 25, 1559–1567.
Cai M, Ma S, Hu R, Tomberlin J K, Thomashow L S, Zheng L, Li W, Yu Z, Zhang J. 2018b. Rapidly mitigating antibiotic resistant risks in chicken manure by Hermetia illucens bioconversion with intestinal microflora. Environmental Microbiology, 20, 4051–4062.
Chen J, Hou D, Pang W, Nowar E E, Tomberlin J K, Hu R, Chen H, Xie J, Zhang J, Yu Z, Li Q. 2019. Effect of moisture content on greenhouse gas and NH3 emissions from pig manure converted by black soldier fly. Science of the Total Environment, 697, 1–12.
Craig A, Hare L, Tessier A. 1999. Experimental evidence for cadmium uptake via calcium channels in the aquatic insect Chironomus staegeri. Aquatic Toxicology, 44, 255–262.
Diener S, Zurbrügg C, Tockner K. 2015. Bioaccumulation of heavy metals in the black soldier fly, Hermetia illucens and effects on its life cycle. Journal of Insects as Food and Feed, 1, 261–270.
Van der Fels-Klerx H J, Camenzuli L, van der Lee M K, Oonincx D G. 2016. Uptake of cadmium, lead and arsenic by Tenebrio molitor and Hermetia illucens from contaminated substrates. PLoS ONE, 11, e0166186.
Gao Q, Wang X, Wang W, Lei C, Zhu F. 2017. Influences of chromium and cadmium on the development of black soldier fly larvae. Environmental Science and Pollution Research, 24, 8637–8644.
He Z M, Liu Q, Xie G X, Rong X M, Peng J W, Song H X, Li L F, Su S M. 2010. Changes of heavy metals form during aerobic high temperature composting of pig manure and the effect of passivators. Chinese Journal of Applied Ecology, 21, 2659–2665. (in Chinese)
Józefiak D, Józefiak A, Kierończyk B, Rawski M, ?wi?tkiewicz S, D?ugosz J, Engberg R M. 2016. Insects - a natural nutrient source for poultry - a review. Annals of Animal Science, 16, 297–313.
Lalander C, Diener S, Magri M E, Zurbrügg C, Lindström A, Vinnerås B. 2013. Faecal sludge management with the larvae of the black soldier fly (Hermetia illucens) - From a hygiene aspect. Science of the Total Environment, 458, 312–318.
Li Y, Xiong X, Li C, Zhang F, Li W, Han W. 2010. Cadmium in animal production and its potential hazard on Beijing and Fuxin farmlands. Journal of Hazardous Materials, 177, 475–480.
Liu X C, Xiao Z M, Deng T, Jia Z, Tian J, Fan X. 2017. Analysis on arsenic speciation in food and feed: review. Quality and Safety of Agro-Products, 3, 49–54. (in Chinese)
Maroni G, Watson D. 1985. Uptake and binding of cadmium, copper and zinc by Drosophila melanogaster larvae. Insect Biochemistry, 15, 55–63.
Maryanski M, Kramarz P, Laskowski R, Niklinska M. 2002. Decreased energetic reserves, morphological changes and accumulation of metals in carabid beetles (Poecilus cupreus L.) exposed to zinc-or cadmium-contaminated food. Ecotoxicology, 11, 127–139.
Mireji P O, Joseph K, Ahmed H, Impoinvil D E, Mbogo C M, Muturi M N , Hudson N, Kenya E U, Githure J I, Beier J C. 2010. Expression of metallothionein and α-tubulin in heavy metal-tolerant Anopheles gambiae sensu stric to (Diptera: Culicidae). Ecotoxicology and Environmental Safety , 73, 46–50.
Mogren C L, Webb S M, Walton W E, Trumble J T. 2013. Micro x-ray absorption spectroscopic analysis of arsenic localization and biotransformation in Chironomus riparius Meigen (Diptera: Chironomidae) and Culex tarsalis Coquillett (Culicidae). Environmental Pollution, 180, 78–83.
Munir M A M, Liu G, Yousaf B, Mian M M, Ali M U, Ahmed R, Cheema A I, Naushad M. 2020. Contrasting effects of biochar and hydrothermally treated coal gangue on leachability, bioavailability, speciation and accumulation of heavy metals by rapeseed in copper mine tailings. Ecotoxicology and Environmental Safety, 191, 110244.
Nachman K E, Baron P A, Raber G, Francesconi K A, Navas-Acien A, Love D C. 2013. Roxarsone, inorganic arsenic, and other arsenic species in chicken: A U.S. based market basket sample. Environmental Health Perspectives, 121, 818–824.
Nguyen D T, Bouguet V, Spranghers T, Vangansbeke D, De Clercq P. 2015. Beneficial effect of supplementing an artificial diet for Amblyseius swirskii with Hermetia illucens haemolymph. Journal of Applied Entomology, 139, 342–351.
Peng Z, Zhang J, Fanning S, Wang L, Li M, Maheshwari N, Sun J, Li F. 2019. Effects of metal and metalloid pollutants on the microbiota composition of feces obtained from twelve commercial pig farms across China. Science of the Total Environment, 647, 577–586.
Postma J F, VanNugteren P, Buckert-De Jong M B. 1996. Increased cadmium excretion in metal-adapted populations of the midge Chironomus riparius (Diptera). Environmental Toxicology and Chemistry, 15, 332–339.
Sager M. 2007. Trace and nutrient elements in manure, dung and compost samples in Austria. Soil Biology and Biochemistry, 39, 1383–1390.
Sahuquillo A, Rauret G, Bianchi M, Rehnert A, Muntau H. 2003. Mercury determination in solid phases from application of the modified BCR-sequential extraction procedure: A valuable tool for assessing its mobility in sediments. Analytical and Bioanalytical Chemistry, 375, 578–583.
Schmitt E, Belghit I, Johansen J, Leushuis R, Lock E J, Melsen D, Ramasamy Shanmugam R K, Van Loon J, Paul A. 2019. Growth and safety assessment of feed streams for black soldier fly larvae: a case study with aquaculture sludge. Animals, 9, 1–17.
Sizmur T, Tilston E L, Charnock J, Palumbo-Roe B, Watts M J, Hodson M E. 2011. Impacts of epigeic, anecic and endogeic earthworms on metal and metalloid mobility and availability. Journal of Environmental Monitoring, 13, 266–273.
Tian Y Y, Zhang L Y, Dong B, Cao J, Xue J X, Gong L M. 2014. Effects of chromium methionine supplementation on growth performance, serum metabolites, endocrine parameters, antioxidant status, and immune traits in growing pigs. Biological Trace Element Research, 162, 134–141.
Trumble J T, Jensen P D. 2004. Ovipositional response, developmental effects and toxicity of hexavalent chromium to megaselia scalaris, a terrestrial detritivore. Archives of Environmental Contamination and Toxicology, 46, 372–376.
Wang X, Li J, Shang D, Wang C, Cai R, Wu X, Xu X. 2019. Effect of Cu2+, Zn2+, Cd2+ on the growth of Hermetia illucens larvae and accumulation in larvae and feces. Journal of Environmental Entomology, 41, 387–393. (in Chinese)
Wu G X, Ye G Y, Hu C, Cheng J A. 2006. Accumulation of cadmium and its effects on growth, development and hemolymph biochemical compositions in Boettcherisca peregrina larvae (Diptera: Sarcophagidae). Insect Science, 13, 31–39.
Wu N, Wang X, Xu X, Cai R, Xie S. 2020a. Effects of heavy metals on the bioaccumulation, excretion and gut microbiome of black soldier fly larvae (Hermetia illucens). Ecotoxicology and Environmental Safety, 192, 110323.
Wu N, Zhang W Y, Xie S Y, Zeng M, Liu H X, Yang J H, Liu X Y, Yang F. 2020b. Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China. Frontiers of Environmental Science & Engineering, 14, 1.
Zhang F, Li Y, Yang M, Li W. 2012. Content of heavy metals in animal feeds and manures from farms of different scales in Northeast China. International Journal of Environmental Research and Public Health, 9, 2658–2668.
Zhang T, Wang Y, Liu X, Lü J, Li J. 2019. Functions of phosphorus additives on immobilizing heavy metal cadmium in the char through pyrolysis of contaminated biomass. Journal of Analytical and Applied Pyrolysis, 144, 104721.
Zhou B, Tang J, Dai J, Xu H, Yang X, Chen X, Zhang C, Dai J. 2015. Remediating effluent sludge with earthworms: Changes in heavy metal speciation and associated chemical and biological properties. Acta Ecologica Sinica, 35, 6269–6279. (in Chinese)