Concentration and speciation of arsenic in an insect feeding on the leaves of Pteris vittata

Abstract

•Ÿ Hawk moth showed foraging preference to P. vittata fronds with low As concentation.

•Ÿ Hawk moth can not exclude As by excretion.

•Ÿ The main As speciation of hawk moth is As(III)-SH.

The development of an effective and green bioinsecticide is a research hotspot. This study demonstrated the possibility of using an arsenic (As) hyperaccumulator as a bioinsecticide. When the As concentration in the Pteris vittata fronds exceeded 138 mg kg⁻¹, the larva of the hawk moth (Theretra clotho) displayed apparent preference to lower-As-concentration P. vittata fronds. The As concentration in the larva body was as high as 850 mg kg^–1 Such high concentration of As in the larva body might have been the case that T. clotho lacks a process to exclude As. The larval frass showed an As concentration of only 1%–4% of that in the larva body. The predominant As species in the larva body and frass was As(III)-SH. The percentage of As(III)-SH was slightly higher in the frass than that in the larval body. Chelation with thiols may be a universal detoxification mechanism for As in both plants and insects. In general, the adoption of P. vittata as a bioinsecticide should be feasible. However, the exact processes to achieve this goal still need further study. The mechanism of different animals to detoxify As is another interesting research topic.

Graphical abstract

Keywords

Arsenic speciation / Bioinsecticide / Hawk moth / Herbivore / Hyperaccumulator

References

[1] Andrahennadi, R., Pickering, I.J., 2008. Arsenic accumulation, biotransformation and localisation in bertha armyworm moths. Environmental Chemistry 5, 413–419

[2] Barbafieri, M., Pedron, F., Petruzzelli, G., Rosellini, I., Franchi, E., Bagatin, R., Vocciante, M., 2017. Assisted phytoremediation of a multi-contaminated soil: Investigation on arsenic and lead combined mobilization and removal. Journal of Environmental Management 203, 316–329

[3] Cai, W., Chen, T.B., Lei, M., Wan, X.M., 2020. Effective strategy to recycle arsenic accumulated biomass of Pteris vittata with high benefits. Science of the Total Environment 756, 143890

[4] Champeau, O., Cavanagh, J.A.E., Sheehan, T.J., Tremblay, L.A., Harding, J.S., 2017. Acute toxicity of arsenic to larvae of four New Zealand freshwater insect taxa. New Zealand Journal of Marine and Freshwater Research 51, 443–454

[5] Chen, T., Lei, M., Wan, X., Yang, J., Zhou, X., 2018. Arsenic Hyperaccumulator Pteris vittata L. and Its Application to the Field. In: Luo, Y., Tu, C., eds. Twenty Years of Research and Development on Soil Pollution and Remediation in China. Springer Singapore, Singapore, pp. 465–476.

[6] Chen, T.B., Wei, C.Y., Huang, Z.C., Huang, Q.F., Lu, Q.G., Fan, Z.L., 2002. Arsenic hyperaccumulator Pteris vittata L. and its arsenic accumulation. Chinese Science Bulletin 47, 902–905

[7] Geiszinger, A., Goessler, W., Kuehnelt, D., Francesconi, K., Kosmus, W., 1998. Determination of arsenic compounds in earthworms. Environmental Science & Technology 32, 2238–2243

[8] Hörger, A.C., Fones, H.N., Preston, G.M., 2013. The current status of the elemental defense hypothesis in relation to pathogens. Frontiers in Plant Science 4, 395

[9] Hughes, M.F., Beck, B.D., Chen, Y., Lewis, A.S., Thomas, D.J., 2011. Arsenic exposure and toxicology: a historical perspective. Toxicological Sciences 123, 305–332

[10] Jaffe, B.D., Ketterer, M.E., Shuster, S.M., 2018. Elemental allelopathy by an arsenic hyperaccumulating fern, Pteris vittata L. Journal of Plant Ecology 11, 553–559

[11] Kim, E.J., Yoo, J.C., Baek, K., 2014. Arsenic speciation and bioaccessibility in arsenic-contaminated soils: sequential extraction and mineralogical investigation. Environmental Pollution 186, 29–35

[12] Ko, E., Choi, M., Shin, S., 2020. Bottom-line mechanism of organochlorine pesticides on mitochondria dysfunction linked with type 2 diabetes. Journal of Hazardous Materials 393, 122400

[13] Langdon, C.J., Piearce, T.G., Meharg, A.A., Semple, K.T., 2001a. Resistance to copper toxicity in populations of the earthworms Lumbricus rubellus and Dendrodrilus rubidus from contaminated mine wastes. Environmental Toxicology and Chemistry 20, 2336–2341

[14] Langdon, C.J., Piearce, T.G., Meharg, A.A., Semple, K.T., 2001b. Survival and behaviour of the earthworms Lumbricus rubellus and Dendrodrilus rubidus from arsenate-contaminated and non-contaminated sites. Soil Biology & Biochemistry 33, 1239–1244

[15] Li, X.W., Lei, M., Chen, T.B., Wan, X.M., 2009. Roles of sulfur in the arsenic tolerant plant Adiantum capillus-veneris and the hyperaccumulator Pteris vittata. Journal of the Korean Society for Applied Biological Chemistry 52, 498–502

[16] Ma, J., Lei, E., Lei, M., Liu, Y., Chen, T., 2018. Remediation of arsenic contaminated soil using malposed intercropping of Pteris vittata L. and maize. Chemosphere 194, 737–744

[17] Ma, L.Q., Komar, K.M., Tu, C., Zhang, W., Cai, Y., Kennelley, E.D., 2001. A fern that hyperaccumulates arsenic. Nature 409, 579–579

[18] Manara, A., Fasani, E., Furini, A., DalCorso, G., 2020. Evolution of the metal hyperaccumulation and hypertolerance traits. Plant, Cell & Environment 43, 2969–2986

[19] Mathews, S., Ma, L.Q., Rathinasabapathi, B., Stamps, R.H., 2009. Arsenic reduced scale-insect infestation on arsenic hyperaccumulator Pteris vittata L. Environmental and Experimental Botany 65, 282–286

[20] Mehltreter, K., Rojas, P., Palacios-Rios, M., 2003. Moth larvae-damaged giant leather-fern Acrostichum danaeifolium as host for secondary colonization by ants. American Fern Journal 93, 49–55

[21] Nagamine, K., Hojoh, K., Nagata, S., Shintani, Y., 2019. Rearing Theretra oldenlandiae (Lepidoptera: Sphingidae) larvae on an artificial diet. Journal of Insect Science 19, 5

[22] Purwani, K.I., Ermavitalini, D., Nurhidayati, T., Nurhatika, S., Bagus, T., 2015. Exploration of Potential Plants As a Bio-Insecticide at Its Surabaya Campus. In: Setyobudi, R.H., Nuringtyas, T.R., Burlakovs, J., Mel, M., Adinurani, P.G., VincevicaGaile, Z., eds. International Conference on Biological Sciences. Knowledge E, Dubai, pp. 662–662.

[23] Ramasamy, S., Sotelo, P., Lin, M.Y., Heng, C.H., Kang, S., Sarika, S., 2020. Validation of a bio-based integrated pest management package for the control of major insect pests on Chinese mustard in Cambodia. Crop Protection (Guildford, Surrey) 135, 8

[24] Rathinasabapathi, B., Rangasamy, M., Froeba, J., Cherry, R.H., McAuslane, H.J., Capinera, J.L., Srivastava, M., Ma, L.Q., 2007. Arsenic hyperaccumulation in the Chinese brake fern (Pteris vittata) deters grasshopper (Schistocerca americana) herbivory. New Phytologist 175, 363–369

[25] Sharma, A., Shukla, A., Attri, K., Kumar, M., Kumar, P., Suttee, A., Singh, G., Barnwal, R.P., Singla, N., 2020. Global trends in pesticides: A looming threat and viable alternatives. Ecotoxicology and Environmental Safety 201, 110812

[26] Skaldina, O., Ciszek, R., Peräniemi, S., Kolehmainen, M., Sorvari, J., 2020. Facing the threat: common yellowjacket wasps as indicators of heavy metal pollution. Environmental Science and Pollution Research International 27, 29031–29042

[27] Su, Y.H., McGrath, S.P., Zhu, Y.G., Zhao, F.J., 2008. Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytologist 180, 434–441

[28] Wan, X., Lei, M., Chen, T., Ma, J., 2017a. Micro-distribution of arsenic species in tissues of hyperaccumulator Pteris vittata L. Chemosphere 166, 389–399

[29] Wan, X., Lei, M., Chen, T., Yang, J., 2017b. Intercropped Pteris vittata L. and Morus alba L. presents a safe utilization mode for arsenic-contaminated soil. Science of the Total Environment 579, 1467–1475

[30] Watts, M.J., Button, M., Brewer, T.S., Jenkin, G.R.T., Harrington, C.F., 2008. Quantitative arsenic speciation in two species of earthworms from a former mine site. Journal of Environmental Monitoring 10, 753–759

[31] Zhang, W., Cai, Y., Tu, C., Ma, L.Q., 2002. Arsenic speciation and distribution in an arsenic hyperaccumulating plant. Science of the Total Environment 300, 167–177

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