Abstract
This study analyzed the effects of cadmium (Cd) and lead (Pb) on growth, sexual couples, and histological structures of Artemia franciscana exposed to individual concentrations of these metals and combined. No histological effects were observed at tissue level in digestive, respiratory, nervous, and reproductive systems (i.e., necrosis, loss of regular structure) in individual and mixed applications on A. franciscana for 20 days of exposure. No significant differences (p > 0.05) were determined in final size and growth rate among the organisms exposed to Cd and those of control. For Pb, only the final size (3.59 ± 0.59 mm) of organisms exposed to the highest concentration was significantly lower (p < 0.05) than those of the control (4.53 ± 0.34 mm) group, whereas for the combined experiment, no significant differences (p > 0.05) were observed in final size and growth rate. At all Cd concentrations, mean sexual couples were significantly lower (p < 0.05) than those of the control, as well as for Pb. For the combined experiment (8 μg/L of Cd + 8 μg/L of Pb), sexual couples were not observed, indicating synergism and negative reproduction effects. The results showed that Cd and Pb aquatic environmental regulations (as the Criterion of Continuous Concentration) proposed by the US Environmental Protection Agency (EPA) should include their interactions with other metals.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abatzopoulos TJ, Beardmore JA, Clegg JS, Sorgeloos P (2002) Artemia. Basic and applied biology. Kluwer Academic Publishers, Netherland
Barata C, Baird DJ, Soares AMVM (2002) Demographic responses of a tropical cladoceran to cadmium: effects of food supply and density. Ecol Appl 12:552-564. https://doi.org/10.2307/3060962
Barata C, Baird DJ, Nogueira AJA, Soares AMVM, Riva MC (2006) Toxicity of binary mixtures of metals and pyretroid insecticides to Daphnia magna Straus. Implications for multi-substance risk assessment. Aquat Toxicol 78:1–14. https://doi.org/10.1016/j.aquatox.2006.01.013
Brzóska MM, Moniuszko-Jakoniuk J (2001) Interactions between cadmium and zinc in the organism. Food Chem Toxicol 39:967-980. https://doi.org/10.1016/s0278-6915(01)00048-5
Buikema AL, Niederleener RR, Cairns JJ (1982) Biological monitoring part IV. Toxicity testing. Water Res 16:239–262. https://doi.org/10.1016/0043-1354(82)90188-9
Bur T, Crouau Y, Bianco A, Gandois L, Probst A (2012) Toxicity of Pb and Cd/Pb combination on the springtail Folsomia candida in natural soils: reproduction, growth and bioaccumulation as indicators. Sci Total Environ 414:187–197. https://doi.org/10.1016/j.scitotenv.2011.10.029
Chang M, Wang WN, Wang AL, Tian TT, Wang P, Zheng Y, Liu Y (2009) Effects of cadmium on respiratory burst, intracellular Ca2+ and DNA damage in the white shrimp Litopenaeus vannamei. Comp Biochem Physiol 149C:581–586. https://doi.org/10.1016/j.cbpc.2008.12.011
Chinni S, Khan RN, Yallapragada PR (2001) Larval growth in postlarvae Penaeus indicus on exposure to lead. Bull Environ Contam Toxicol 67:27–34. https://doi.org/10.1007/s001280104
Chinni S, Khan RN, Yallapragada PR (2002) Acute toxicity of lead on tolerance oxygen consumption, ammonia-N excretion, and metal accumulation in P. indicus postlarvae. Ecotoxicol Environ Saf 51:79–84. https://doi.org/10.1006/eesa.2000.2019
Chiodi Boudet LN, Polizzi P, Romero MB, Robles A, Marcovecchio JE, Gerpe MS (2015) Histopathological and biochemical evidence of hepatopancreatic toxicity caused by cadmium in white shrimp, Palaemonetes argentinus. Ecotoxicol. Environ. Saf. 113:231–240. https://doi.org/10.1016/j.ecoenv.2014.11.019
Damasceno EP, Figuerêdo LP, Pimentel MF, Loureiro S, Costa-Lotufo LV (2017) Prediction of toxicity of zinc and nickel mixtures to Artemia sp. at various salinities: From additivity to antagonism. Ecotoxicol Environ Saf 142:322–329. https://doi.org/10.1016/j.ecoenv.2017.04.020
Đukić-Ćosić D, Baralić K, Javorac D, Djordjevic AB, Bulat Z (2020) An overview of molecular mechanisms in cadmium toxicity. Curr Opin Toxicol 19:56–62. https://doi.org/10.1016/j.cotox.2019.12.002
Elumalai M, Antunes C, Guilhermino L (2005) Alterations of reproductive parameters in the crab Carcinus maenas after exposure to metals. Water Air Soil Pollut 160:245–258. https://doi.org/10.1007/s11270-005-2992-9
EPA (2009) National recommended water quality criteria. Aquatic life criteria table. Available from: http://water.epa.gov/scitech/swguidance/standards/criteria/current/upload/nrwqc-2009.pdf. Accessed 11 June 2020
Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative stress. Cur Top Med Chem 1:529–539. https://doi.org/10.2174/1568026013394831
Frías-Espericueta MG, Abad-Rosales SM, Vargas-Jiménez A, Sarabia-Espinoza T, Rodríguez-Salas BA, Osuna-López I, Voltolina D (2016) Synergistic effects of cadmium and zinc on the histology of the gills and hepatopancreas and on the growth and mortality of the post-larvae of Litopenaeus vannamei. Turk J Fish Aquat Sci 16:491–497. https://doi.org/10.4194/1303-2712-v16_2_30
Gao Y, Feng J, Kang L, Xu X, Zhu L (2018) Concentration addition and independent action model: which is better in predicting the toxicity for metal mixtures on zebrafish larvae. Sci Total Environ 610–611:442–450. https://doi.org/10.1016/j.scitotenv.2017.08.058
Geffard O, Geffard A, Chaumot A, Vollat B, Alvarez C, Tusseau-Vuillemin ME, Garric J (2008) Effects of chronic dietary and waterborne cadmium exposures on the contamination level and reproduction of Daphnia magna. Environ Toxicol Chem 27:1128-1134. https://doi.org/10.1897/07-431.1
Guo X, Feng C (2018) Biological toxicity response of Asian clam (Corbicula fluminea) to pollutants in surface water and sediment. Sci Total Environ 631-632:56–70. https://doi.org/10.1016/j.scitotenv.2018.03.019
Howe L, Reichelt-Brushett AJ, Clark MW (2014) Effects of Cd, Co, Cu, Ni, and Zn on asexual reproduction and early development of the tropical sea anemone Aiptasia pulchella. Ecotoxicology 23:1593–1606. https://doi.org/10.1007/s10646-014-1299-2
Jensen A, Forbes VE, Parker ED Jr (2001) Variation in cadmium uptake, feeding rate, and life-history effects in the gastropod Potamopyrgus antipodarum: linking toxicant effects on individuals to the population level. Environ Toxicol Chem 20:2503–2513. https://doi.org/10.1002/etc.5620201116
Kutlu M, Iscan A, Tanatmis M (2008) Structural changes of Artemia parthenogenetica (Bowen and Sterling, 1978) (Branchiopoda: Anostraca) exposed to lead acetate. Food Chem Toxicol 46:3770–3733. https://doi.org/10.1016/j.fct.2008.09.060
Li R, Zhou Y, Ji J, Wang L (2011) Oxidative damages by cadmium and the protective effect of low-molecular-weight chitosan in the freshwater crab (Sinopotamon yangtsekiense Bott 1977). Aquac Res 42:506–515. https://doi.org/10.1111/j.1365-2109.2010.02646.x
Li Y, Chai X, Wu H, Jing W, Wang L (2013) The response of metallothionein and malondialdehyde after exclusive and combined Cd/Zn exposure in the crab Sinopotamon henanense. Plos One 8:e80475. https://doi.org/10.1371/journal.pone.0080475
Manyin T, Rowe CL (2009) Bioenergetics effects of aqueous copper and cadmium on the grass shrimp Palaemonetes pugio: Comp Biochem Physiol 150:65-71. https://doi.org/10.1016/j.cbpc.2009.02.007
Mazzei V, Longo G, Brundo MV, Copat C, Conti GO, Ferrante M (2013) Effects of heavy metal accumulation on some reproductive characters in Armadillium granulatum Brand (Crustacea: Isopoda: Oniscidea). Ecotoxicol Environ Saf 98:66–73. https://doi.org/10.1016/j.ecoenv.2013.09.023
Mitra P, Sharma S, Purohit P, Sharma P (2017) Clinical and molecular aspects of lead toxicity: an update. Crit Rev Cl Sci 54:7–8. https://doi.org/10.1080/10408363.2017.1408562
Moreno R, Medesani DA, Rodríguez M (2003) Inhibition of molting by cadmium in the crab Chasmagnathus granulata (Decapoda: Brachiura). Aquat Toxicol 64:155–164. https://doi.org/10.1016/S0166-445X(03)00029-8
Nunes BS, Carvalho FD, Guilhermino LM, Van Stappen G (2006) Use of the genus Artemia in ecotoxicity testing. Environ Pollut 144:453–462. https://doi.org/10.1016/j.envpol.2005.12.037
Nuñez-Nogueira G, Fernández-Bringas L, Ordiano-Flores A, Gómez-Ponce A, Ponce de León-Hill C, González-Farías F (2012) Accumulation and regulation effects from the metal mixture of Zn, Pb, and Cd in the tropical shrimp Penaeus vannamei. Biol Trace Elem Res 150:208–213. https://doi.org/10.1007/s12011-012-9500-z
Páez-Osuna F, Álvarez-Borrego S, Ruiz-Fernández AC, García-Hernández J, Jara-Marini M, Bergés-Tiznado M, Piñón-Gimate A, Soto-Jiménez MF, Alonso-Rodríguez R, Frías-Espericueta MG, Ruelas-Inzunza JR, Green-Ruiz C, Osuna-Martínez CC, Sanchez-Cabeza JA (2017) Environmental status of the Gulf of California: a pollution review. Earth-Sci Rev 166:181–205. https://doi.org/10.1016/j.earscirev.2017.01.014
Phillips BM, Nicely PA, Hunt JW, Anderson BS, Tjeerdema RS, Palmer SE, Palmer FH, Puckett HM (2003) Toxicity of cadmium-copper-nickel-zinc mixtures to larval purple sea urchins. Bull Environ Contam Toxicol 70:592–599. https://doi.org/10.1007/s00128-003-0026-0
Preston S, Coad N, Townend J, Killham K, Paton GI (2000) Biosensing the acute toxicity of metal interactions: are they additive, synergistic, or antagonistic? Environ Toxicol Chem 19:775–780. https://doi.org/10.1002/etc.5620190332
Rainbow PS (1997) Ecophysiology of trace metal uptake in crustaceans. Estuar Coastal Shelf Sci 44:169–175. https://doi.org/10.1006/ecss.1996.0208
Rainbow PS, Poirier L, Smith BD, Brix KV, Luoma SN (2006) Trophic transfer of trace metals from the polychaete worm Nereis diversicolor to the polychaete N. virens and the decapod crustacean Palaemonetes varians. Mar Ecol Prog Ser 321:167–181. https://doi.org/10.3354/meps321167
Rani A, Kumar A, Lal A, Pant M (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 24:378–399. https://doi.org/10.1080/09603123.2013.835032
Reddy PS, Katyayani RV, Fingerman M (1997) Effects of cadmium and mercury on the ovarian maturation in the red swamp crayfish Procambarus clarkii. Ecotoxicol Environ Saf 37:62–65. https://doi.org/10.1006/eesa.1997.1523
Revathi P, Vasanthi LA, Munuswamy N (2011) Effect of cadmium on the ovarian development in the freshwater prawn Macrobrachium rosenbergii (De Man). Ecotoxicol Environ Saf 74:623–629. https://doi.org/10.1016/j.ecoenv.2010.08.027
Rodríguez EM, López-Greco LS, Fingerman M (2000) Inhibition of ovarian growth by cadmium in the fiddler crab Uca pugilator (Decapoda). Ecotoxicol Environ Saf 46:202–206. https://doi.org/10.1006/eesa.1999.1896
Roesijadi G, Robinson WE (1994) Metal regulation in aquatic animals: mechanism of uptake, accumulation, and release. In: Malins DC (ed), Aquatic toxicology. Molecular, biochemical, and cellular perspectives. Taylor & Francis, Boca Raton, pp 387-411
Salice CJ, Miller TJ (2003) Population-level responses to long-term cadmium exposure in two strains of the freshwater gastropod Biomphalaria glabrata: results from a table-life response experiment. Environ Toxicol Chem 22:678–688. https://doi.org/10.1002/etc.5620220329
Sarabia R, Del Ramo J, Díaz-Mayans J, Torreblanca A (2003) Developmental and reproductive effects of low cadmium on Artemia parthenogenetica. J Environ Sci Health 38A:1065–1071. https://doi.org/10.1081/ese-120019864
Sofyan A, Price DJ, Birge WJ (2007) Effects of aqueous, dietary and combined exposures of cadmium to Ceriodaphnia dubia. Sci Total Environ 385:108–116. https://doi.org/10.1016/j.scitotenv.2006.07.003
Soto-Jiménez MF, Hibdon SA, Rankin CW, Aggarwal J, Ruiz-Fernández AC, Páez-Osuna F, Flegal AR (2006) Chronicling a century of lead pollution in Mexico: stable lead isotopic composition analyses of dated sediment cores. Environ Sci Technol 40:764–770. https://doi.org/10.1021/es048478g
Soto-Jiménez MF, Arellano-Fiore C, Rocha-Velarde R, Jara-Marini ME, Ruelas-Inzunza J, Voltolina D, Frías-Espericueta MG, Quintero-Álvarez JM, Páez-Osuna F (2011a) Biological responses of a simulated marine food chain to lead addition. Environ Toxicol Chem 30:1611–1617. https://doi.org/10.1002/etc.53
Soto-Jiménez MF, Arellano-Fiore C, Rocha-Velarde R, Jara-Marini ME, Ruelas-Inzunza J, Páez-Osuna F (2011b) Trophic transfer of lead through a model marine four-level food chain: Tetraselmis suecica, Artemia franciscana, Litopenaeus vannamei, and Haemulon scudderi. Arch Environ Contam Toxicol 61:280–291. https://doi.org/10.1007/s00244-010-9620-4
Spicer JI, Weber RE (1991) Respiratory impairment in crustaceans and molluscs due to exposure to heavy metals. Comp Biochem Physiol 100C:339-342. https://doi.org/10.1016/0742-8413(91)90005-e
Tkalec M, Stefanic PP, Cvjetko P, Sikic S, Pavlica M, Balen B (2014) The effect of cadmium-zinc interactions on biochemical responses in tobacco seedlings and adult plants. Plos One 9:e87582. https://doi.org/10.1371/journal.pone.0087582
Van Stappen G (1996) Artemia: use of cysts. In: Lavens P, Sorgeloos P (eds) Manual on the production and uses of live food for aquaculture. FAO, Rome, pp 107–123
Voltolina D, Gómez-Villa H, Correa G (2005) Nitrogen removal and recycling by Scenedesmus obliquus in semicontinuous cultures using artificial wastewater and simulated light and temperature cycle. Bioresource Technol 96:359–362. https://doi.org/10.1016/j.biortech.2004.04.004
Wang WX (2002) Interactions of trace metals and different marine food chains. Mar Ecol Prog Ser 243:295–309. https://doi.org/10.3354/meps243295
Wätjen W, Beyersmann D (2004) Cadmium-induced apoptosis in C6 glioma cells: influence of oxidative stress. Biometals 17:65–78. https://doi.org/10.1023/A:1024405119018
Wieczorek J, Baran A, Urbański K, Mazurek R, Klimowicz-Pawlas A (2018) Assessment of the pollution and ecological risk of lead and cadmium in soils. Environm Geochem Health 40:2325–2342. https://doi.org/10.1007/s10653-018-0100-5
Wu JP, Chen HC (2005) Effects of cadmium and zinc on the growth, food consumption, and nutritional conditions of the white shrimp, Litopenaeus vannamei (Boone). Bull Environ Contam Toxicol 74:234–241. https://doi.org/10.1007/s00128-004-0575-x
Wu SM, Tsai PJ, Chou MY, Wang WD (2013) Effects of maternal cadmium exposure on female reproductive functions, gamete quality, and offspring development in zebrafish (Dania rerio). Arch Environ Contam Toxicol 65:521–536
Wu X, Cobbina SJ, Mao G, Xu H, Zhang Z, Yang L (2016) A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ. Sci. Pollut. Res. 23:8244–8259. https://doi.org/10.1007/s11356-016-6333-x
Zaltauskaite J, Sodiene I (2014) Effects of cadmium and lead on the life-cycle parameters of juvenile earthworm Eisenia fetida. Ecotoxicol Environ Saf 103:9–16
Acknowledgements
The authors thank D. Voltolina and Y. Montaño-Ley for their technical help and D. Fischer for the English edition.
Availability of data and materials
Not applicable
Funding
This study was funded by Programa de Fomento y Apoyo a Proyectos de Investigación UAS 2012/059, Programa para el Desarrollo Profesional Docente (CANE year 3), and Consejo Nacional de Ciencia y Tecnología INFRA 2012-01-188029, and INFRA-CONACYT 230061.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, and data collection and analyses were performed by Selene M. Abad-Rosales, Jesús M. Quintero-Alvarez, Carolina Bojórquez, Marely L. López-Morales, Sandy Y. Trujillo-Alvarez, and Jonathan A. Arellano-Sarabia. The first draft of the manuscript was written by Martín G. Frías-Espericueta, Martín F. Soto-Jiménez, J. Isidro Osuna-López, and Marisela Aguilar-Juárez. All authors commented on the previous versions of the manuscript and read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Frías-Espericueta, M.G., Soto-Jiménez, M.F., Abad-Rosales, S.M. et al. Physiological and histological effects of cadmium, lead, and combined on Artemia franciscana. Environ Sci Pollut Res 29, 7344–7351 (2022). https://doi.org/10.1007/s11356-021-16147-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16147-9