Abstract
Perchlorate (ClO4 −) pollution is widespread in the natural environment, but the effects of ClO4 − on the terrestrial insects are rarely studied. Here, when phytophagous insect Spodoptera litura larvae were fed on the diets with different ClO4 − concentrations, changes in their life-history traits were recorded; ClO4 − accumulations in feces and insect body were detected. The results demonstrated that ClO4 − bioaccumulation in insect at the different developmental stages was ranked in the order: adults > pupae > the 4th > 5th > 6th instar larvae. Besides, ClO4 − accumulations in the feces were ranked in the order: the 6th > 5th > 4th instar larvae. The ClO4 − accumulations in female pupae and adults were significantly higher than that in males. ClO4 − bioaccumulation in insect prolonged larval development time and caused a skewed sex ratio (the percentage of males at metamorphosis significantly decreased) under 100 to 200 mg ClO4 −/kg treatment. Therefore, ClO4 − accumulations in S. litura body presented developmental stage-, sex-specific pattern, and the sex-specific ClO4 − accumulations resulted in difference of sex ratio. These effects were observed at concentrations reported in natural environments contaminated with ClO4 −, suggesting that this contaminant may pose a threat to the normal development and growth of this insect species.
Similar content being viewed by others
References
Attanasio R, Scinicariello F, Blount BC, Valentin-Blasini L, Rogers KA, Nguyena DC, Murray HE (2011) Pendrin mediates uptake of perchlorate in a mammalian in vitro system. Chemosphere 84:1484–1488
Chen QJ, Li GH, Pang Y (2000) A simple artificial diet for mass rearing of some noctuid species. Entomological Knowledge 37:325–327 (in Chinese)
Cheng QQ, Perlmutter L, Smith PN, Mcmurry ST, Jackson WA (2004) A study on perchlorate exposure and absorption in beef cattle. J Agr Food Chem 52:3456–3461
Cid N, Ibáñez C, Palanques A, Prat N (2010) Patterns of metal bioaccumulation in two filter-feeding macroinvertebrates: exposure distribution, inter-species differences and variability across developmental stages. Sci Total Environ 408:2795–2806
Devkota B (1992) Wirkung einer Dauerbelastung von Schwerme-tallen (Hg, Cd, Pb) auf Feldheuschrecken-Generationen (Insecta, Orthoptera, Acrididae). University of Hannover, Dissertation
Devkota B, Schmidt GH (2000) Accumulation of heavy metals in food plants and grasshoppers from the Taigetos Mountains, Greece. Agr Ecosyst Environ 78:85–91
Gan ZW, Sun HW, Wang RN, Deng YY (2014) Occurrence and exposure evaluation of perchlorate in outdoor dust and soil in mainland China. Sci Total Environ 470–471:99–106
Goleman WL, Carr JA, Anderson TA (2002a) Environmentally relevant concentrations of ammonium perchlorate inhibit thyroid function and alter sex ratios in developing Xenopus laevis. Environ Toxicol Chem 21:590–597
Goleman WL, Urquidi LJ, Anderson TA (2002b) Environmentally relevant concentrations of ammonium perchlorate inhibit development and metamorphosis in Xenopus laevis. Environ Toxicol Chem 21:424–430
Grantz DA, Burkey KO, Jackson WA, Vu HB, McGrath MT, Harvey G (2014) Perchlorate content of plant foliage reflects a wide range of species-dependent accumulation but not ozone-induced biosynthesis. Environ Pollut 184:690–696
Groenendijk D, Kraak MHS, Admiraal W (1999) Efficient shedding of accumulated metals during metamorphosis in metal-adapted populations of the midge Chironomus riparius. Environ Toxicol Chem 18:1225–1231
He HZ, Gao HS, Chen GK, Li HS, Lin H, Shu ZZ (2013) Effects of perchlorate on growth of four wetland plants and its accumulation in plant tissues. Environ Sci Pollut Res 20:7301–7308
Heliöväara K, Väisänen R (1990) Heavy-metal contents in pupae of Bupalus piniarius (Lepidoptera: Geometridae) and Panolis flammea (Lepidoptera: Noctuidae) near an industrial source. Environ Entomol 19:481–485
Hirsch HVB, Mercer J, Sambaziotis H, Huber M, Stark DT, Torno-Morley T, Hollocher K, Ghiradella H, Ruden DM (2003) Behavioral effects of chronic exposure to low levels of lead in Drosophila melanogaster. Neurotoxicology 24:435–442
Jackson WA, Joseph P, Laxman P, Tan K, Smith PN, Yu L, Anderson TA (2005) Perchlorate accumulation in forage and edible vegetation. J Agr Food Chem 53:369–373
Kafel A, Zawisza-Raszka A, Szulińska E (2012) Effects of multigenerational cadmium exposure of insects (Spodoptera exigua larvae) on anti-oxidant response in haemolymph and developmental parameters. Environ Pollut 162:8–14
Kirk AB, Smith EE, Tian K, Anderson TA, Dasgupta PK (2003) Perchlorate in milk. Environ Sci Technol 37:4979–4981
Landrum M, Cañas JE, Coimbatore G, Cobb GP, Jackson WA, Zhang BH, Anderson TA (2006) Effects of perchlorate on earthworm (Eisenia fetida) survival and reproductive success. Sci Total Environ 363:237–244
Lee JW, Oh SH, Oh JE (2012) Monitoring of perchlorate in diverse foods and its estimated dietary exposure for Korea populations. J Hazard Mater 243:52–58
McLain DK, Pratt AE, Shure DJ (2015) Size dependence of courtship effort may promote male choice and strong assortative mating in soldier beetles. Behav Ecol Sociobiol 69:883–894
Mukhi S, Torres L, Patiño R (2007) Effects of larval-juvenile treatment with perchlorate and co-treatment with thyroxine on zebrafish sex ratios. Gen Comp Endocr 150:486–494
Nerenberg R (2013) Breathing perchlorate. Science 6128:38–39
Nzengung VA, Wang CH, Harvey G (1999) Plant-mediated transformation of perchlorate into chloride. Environ Sci Technol 33:1470–1478
Osman W, El-Samad LM, Mokhamer ELH, El-Touhamy A, Shonouda M (2015) Ecological, morphological, and histological studies on Blaps polycresta (Coleoptera: Tenebrionidae) as biomonitors of cadmium soil pollution. Environ Sci Pollut Res 22:14104–14115
Park JW, Rinchard J, Liu FJ, Anderson TA, Kendall RJ, Theodorakis CW (2006) The thyroid endocrine disruptor perchlorate affects reproduction, growth, and survival of mosquitofish. Ecotox Environ Safe 63:343–352
Punithavalli M, Sharma AN, Rajkumar MB (2014) Seasonality of the common cutworm Spodoptera litura in a soybean ecosystem. Phytoparasitica 42:213–222
Redick-Harris MS (2006) Effects of in ovo exposure to sodium perchlorate on development, growth and reproduction of fence lizards (Sceloporus SP.). Dissertation, Oklahoma State University
Shi YL, Zhang P, Wang YW, Shi JB, Cai YQ, Mou SF, Jiang GB (2007) Perchlorate in sewage sludge, rice, bottled water and milk collected from different areas in China. Environ Int 33:955–962
Shu YH, Zhou JL, Lu K, Li KQ, Zhou Q (2015) Response of the common cutworm Spodoptera litura to lead stress: changes in sex ratio, Pb accumulations, midgut cell ultrastructure. Chemosphere 139:441–451
Smith PN, Yu L, McMurry ST, Anderson TA (2004) Perchlorate in water, soil, vegetation, and rodents collected from the Las Vegas Wash, Nevada, USA. Environ Pollut 132:121–127
Smith PN (2006) The ecotoxicology of perchlorate in the environment, Chapter 7. Springer, Texas, pp 153–168
Smith LJD, Ptacek CJ, Blowes DW, Groza LG, Moncur MC (2015) Perchlorate in lake water from an operating diamond mine. Environ Sci Technol 49:7589–7596
Sun HX, Tang WC, Chen H, Chen W, Zhang M, Liu X, Zhang GR (2013) Food utilization and growth of cutworm Spodoptera litura Fabricius larvae exposed to nickel, and its effect on reproductive potential. Chemosphere 93:2319–2326
Sorensen MA, Jensen PD, Walton WE, Trumble JT (2006) Acute and chronic activity of perchlorate and hexavalent chromium contamination on the survival and development of Culex quinquefasciatus Say (Diptera: Culicidae). Environ Pollut 144:759–764
Stone D, Jepson P, Laskowski R (2002) Trends in detoxification enzymes and heavy metal accumulation in ground beetles (Coleoptera: Carabidae) inhabiting a gradient of pollution. Comp Biochem Phys Part C 132:105–112
Teder T (2014) Sexual size dimorphism requires a corresponding sex difference in development time: a meta-analysis in insects. Funct Ecol 28:479–486
U.S. EPA (2005) Determination of perchlorate in drinking water using inline column concentration/matrix elimination ion chromatography with suppressed conductivity detection. EPA 815-R-05-009 (Method 314.1): 1-38
Urbansky ET, Magnuson ML, Kelty CA, Brown SK (2000) Perchlorate uptake by salt cedar (Tamarix ramosissima) in the Las Vegas Wash riparian ecosystem. Sci Total Environ 256:227–232
Ye L, You H, Yao J, Kang X, Tang L (2013) Seasonal variation and factors influencing perchlorate in water, snow, soil and corns in northeastern China. Chemosphere 90:2493–2498
Yu L, Canas JE, Cobb GP, Jackson WA, Anderson TA (2004) Uptake of perchlorate in terrestrial plants. Ecotox Environ Safe 58:44–49
Zhang YP, Sun G, Yang ML, Wu HH, Zhang JZ, Song SJ, Ma EB, Guo YP (2011) Chronic accumulation of cadmium and its effects on antioxidant enzymes and malondialdehyde in Oxya chinensis (Orthoptera: Acridoidea). Ecotox Environ Safe 74:1355–1362
Acknowledgments
This work was partly supported by the Natural Science Foundation of China (Project No. 41271469 and Project No. 31200308) and National Basic Research Program of China (973 Program; Project No. 2011CB100400).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Elena Maestri
Junhao Qin and Yinghua Shu contributed equally to this work.
Rights and permissions
About this article
Cite this article
Qin, J., Shu, Y., Li, Y. et al. Effects of perchlorate bioaccumulation on Spodoptera litura growth and sex ratio. Environ Sci Pollut Res 23, 8881–8889 (2016). https://doi.org/10.1007/s11356-016-6124-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-6124-4