Abstract
Metal pollution of aquatic ecosystems continues to be a worldwide concern, and many studies have previously been conducted evaluating metal toxicity to aquatic organisms. However, these studies have mainly been focused on temperate species and only evaluated aqueous exposure, whereas aquatic organisms under real-world conditions are also exposed to metals through their diet. Toxicity tests were conducted evaluating the effects of Cr on cell density and biochemical composition of the microalga Chlorella vulgaris. Additionally, the toxic effects of Cr on the temperate Ceriodaphnia dubia and the tropical Ceriodaphnia silvestrii cladocerans were investigated through three contamination routes: contaminated medium (CM), contaminated food (CF; C. vulgaris), and the combination of both situations (CMF; contaminated medium and food). The toxicity tests with the cladocerans evaluated the metal effects on survival, number of newborns, and feeding activity. Exposure to 48 µg L−1 total dissolved Cr reduced cell density and increased protein, carbohydrate, and lipid content in C. vulgaris. The increase in the biochemical composition and hence food quality of the microalgae after Cr exposure have contributed to the absence of toxic effects to the cladocerans in the CF treatment. No toxic effects were observed to the temperate cladoceran at any treatment. The tropical cladoceran C. silvestrii showed reduced filtration, ingestion and reproduction rates in the CM and CMF treatments at a Cr concentration below national and international standards. Implications for considering different exposure pathways in ecotoxicological studies, (tropical) risk assessments and indications for future research are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data analyzed during this study are available from the corresponding author on reasonable request.
References
ABNT (2011) Brazilian association of technical standards. Aquatic ecotoxicology–chronic toxicity–test method with algae (Chlorophyceae). ABNT NBR12648, Rio de Janeiro. (in Portuguese)
ABNT (2017) Brazilian association of technical standards. Aquatic ecotoxicology–chronic toxicity–test method with Ceriodaphnia spp ABNT NBR13373, Rio de Janeiro. (in Portuguese)
Afkar E, Ababna H, Fathi AA (2010) Toxicological response of the green alga Chlorella vulgaris, to some heavy metals. Am J Environ Sci 6:230–237. https://doi.org/10.3844/ajessp.2010.230.237
Alho LOG, Gebara RC, Paina KA, Sarmento H, Melão MGG (2019) Responses of Raphidocelis subcapitata exposed to Cd and Pb: Mechanisms of toxicity assessed by multiple endpoints. Ecotoxicol Environ Saf 169:950–959. https://doi.org/10.1016/j.ecoenv.2018.11.087
Alho LOG, Gebara RC, Mansano AS, Rocha GS, Melão MGG (2022) Individual and combined effects of manganese and chromium on a freshwater chlorophyceae. Environ Toxicol Chem 41:1004–1015. https://doi.org/10.1002/etc.5285
Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem. https://doi.org/10.1155/2019/6730305
Aoyama I, Okamura H (1993) Interactive toxic effect and bioconcentration between cadmium and chromium using continuous algal culture. Environ Toxicol 8:255–269. https://doi.org/10.1002/tox.2530080303
APHA (1995) American Public Health Association, standard methods for the examination of water and wastewater. American Public Health Association; American Water Work Association; Water Control Federation, Washington, DC
Arzate-Cárdenas MA, Martínez-Jerónimo F (2011) Age-altered susceptibility in hexavalent chromium-exposed Daphnia schodleri (Anomopoda: Daphniidae): integrated biomarker response implementation. Aquat Toxicol 105:528–534. https://doi.org/10.1016/j.aquatox.2011.08.006
Arzate-Cárdenas MA, Martínez-Jerónimo F (2012) Energy resource reallocation in Daphnia schodleri (Anomopoda: Daphniidae) reproduction induced by exposure to hexavalent chromium. Chemosphere 87:326–332. https://doi.org/10.1016/j.chemosphere.2011.12.014
Ayres M, Ayres M Jr, Ayres DL, Santos AS (2007) BioEstat 5.0: statistical applications in the field of biological and medical sciences. Editora Gráfica Ltda, Mamirauá
De Azevedo FA, Chasin AAM (2003) Metals. Toxicity management. Atheneu InterTox, Rio de Janeiro
Bakshi A, Panigrahi AK (2018) A comprehensive review on chromium induced alterations in 42 freshwater fishes. Toxicol Rep 5:440–447. https://doi.org/10.1016/j.toxrep.2018.03.007
Barata C, Markich S, Baird DJ, Soares AMVM (2002) The relative importance of water and food as cadmium sources to Daphnia magna Straus. Aquat Toxicol 61:143–154. https://doi.org/10.1016/S0166-445X(02)00052-8
Baudin JP, Fritsch AF (1989) Relative contributions of food and water in the accumulation of 60Co by freshwater fish. Water Res 23:817–823. https://doi.org/10.1016/0043-1354(89)90004-3
Becker C, Boersma M (2005) Differential effects of phosphorus and fatty acids on Daphnia magna growth and reproduction. Limnol Oceanogr 50:388–397. https://doi.org/10.4319/lo.2005.50.1.0388
Botté A, Zaidi M, Guery J, Fichet D, Leigne V (2022) Aluminium in aquatic environments: abundance and ecotoxicological impacts. Aquat Ecol 56:751–773. https://doi.org/10.1007/s10452-
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bradley MC, Baird DJ, Calow P (1991) Mechanisms of energy allocation to reproduction in the cladoceran Daphnia magna Straus. Biol J Linn Soc 44:325–333. https://doi.org/10.1111/j.1095-8312.1991.tb00623.x
Bricelj VM, Bass AE, Lopez GR (1984) Absorption and gut passage time of microalgae in a suspension feeder: an evaluation of the 51Cr: 14C twin tracer technique. Mar Ecol Prog Ser 17:57–63. https://doi.org/10.3354/meps017057
Brown MR, Miller KA (1992) The ascorbic acid content of eleven species of microalgae used in marine culture. J Appl Phycol 4:205–215. https://doi.org/10.1007/BF02161206
Casali-Pereira MP, Daam MA, Resende JC, Vasconcelos AM, Espíndola ELG, Botta CMR (2015) Toxicity of Vertimec 18 EC (active ingredient abamectin) to the neotropical cladoceran Ceriodaphnia silvestrii. Chemosphere 139:558–564. https://doi.org/10.1016/j.chemosphere.2015.08.006
Chia MA, Lombardi AT, Melão MGG, Parrish CC (2013) Lipid composition of Chlorella vulgaris (Trebouxiophyceae) as a function of different cadmium and phosphate concentrations. Aquat Toxicol 128–129:171–182. https://doi.org/10.1016/j.aquatox.2012.12.004
Chia MA, Lombardi AT, Melão MGG, Parrish CC (2017) Phosphorus levels determine changes in growth and biochemical composition of Chlorella vulgaris during cadmium stress. J Appl Phycol 29:1883–1891. https://doi.org/10.1007/s10811-017-1111-9
Choi J-Y, Kim S-K, Chang K-H, Kim M-C, La Chang G-H, Joo G-J, Jeong K-S (2014) Population growth of the cladoceran Daphnia magna: a quantitative analysis the effects of different algal food. PLoS ONE. https://doi.org/10.1371/journal.pone.0095591
Coetzee JJ, Bansal N, Chirwa EMN (2020) Chromium in environment, its toxic effect from chromite-mining and ferrochrome industries, and its possible bioremediation. Expo Health 12:51–62. https://doi.org/10.1007/s12403-018-0284-z
CONAMA (2005) National environmental council, resolution n° 357, 17 march 2005 CONAMA resolution, establish provisions for the classification of water bodies as well as environmental directives for their framework, established conditons and makes other provisions, pp. 58–63. Brasília
Czerpak R, PIotrowska A, Szulecka K (2006) Jasmonic acid affects changes in the growth and some components content in Chlorella vulgaris. Acta Physiol Plant 28:195–203. https://doi.org/10.1007/BF02706531
Daam MA (2022) Toward a tiered regulatory framework for the prospective aquatic effect assessment of pesticides in (Neo)tropical areas. Integr Environ Assess Manag. https://doi.org/10.1002/ieam.4702
Damasceno de Oliveira LL, Nunes B, Antunes SC, Campitelli-Ramos R, Rocha O (2018) Acute and chronic effects of three pharmaceutical drugs on the tropical freshwater cladoceran Ceriodaphnia silvestrii. Water Air Soil Pollut 229:116. https://doi.org/10.1007/s11270-018-3765-6
De Forest DK, Meyer JS (2015) Critical review: toxicity of dietborne metals to aquatic organisms. Crit Rev Environ Sci Technol 45:1176–1241. https://doi.org/10.1080/10643389.2014.955626
De Schamphelaere KAC, Canli M, Lierde VV, Forrez I, Vanhaecke F, Janssen CR (2004) Reproductive toxicity of dietary zinc to Daphnia magna. Aquat Toxicol 70:233–244. https://doi.org/10.1016/j.aquatox.2004.09.008
EC (2006) Annex 3 to the commission staff working document accompanying the report from the commission in accordance with article 3.7 of the groundwater directive 2006/118/EC on the establishment of groundwater threshold values. European Commission, Brussels, Belgium https://ec.europa.eu/environment/water/water-framework/groundwater/pdf/com_swd_annex_iii.pdf
Elahi A, Arooj I, Bukhari DA, Rehman A (2020) Successive use of microorganisms to remove chromium from wastewater. Appl Microbiol Biotechnol 104:3729–3743. https://doi.org/10.1007/s00253-020-10533-y
EU (2005) Chromium trioxide, sodium chromate, sodium dichromate, ammonium dichromate, potassium dichromate. In: European union risk assessment report 3rd priority List, vol 53. Institute for Health and Consumer Protection, European Chemical Bureau, Ispra, Ialy
Evens R, De Schamphelaere K, De Laender F, Janssen C (2012) The effects of Zn-contaminated diets on Daphnia magna reproduction may be related to Zn-induced changes of the dietary P content rather than to the dietary Zn content itself. Aquat Toxicol 110–111:9–16. https://doi.org/10.1016/j.aquatox.2011.11.018
Expósito N, Carafa R, Kumar V, Sierra J, Schuhmacher M, Papiol G (2021) Performance of Chlorella vulgaris exposed to heavy metal mixtures: linking measured endpoints and mechanisms. Int J Environ Res Public Health 18:1037. https://doi.org/10.3390/ijerph18031037
Ferain A, De Saeyer N, Larondelle Y, Rees JF, Debier C, De Schamphelaere KAC (2018) Body lipid composition modulates acute cadmium toxicity in Daphnia magna adults and juveniles. Chemosphere 205:328–338. https://doi.org/10.1016/j.chemosphere.2018.04.091
Freitas EC, Rocha O (2014) Acute and chronic toxicity of chromium and cadmium to the tropical cladoceran Pseudosida ramosa and the implications for ecotoxicological studies. Environ Toxicol 29:176–186. https://doi.org/10.1002/tox.20784
Gauld DT (1951) The grazing rate of planktonic copepods. J Mar Biol Assoc UK 29:695–706. https://doi.org/10.1017/S0025315400052875
Geffard O, Geffard A, Chaumot A, Vollat B, Alvarez C, Tusseau-Vuillemin MH, 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
Gorbi G, Corradi MG (1993) Chromium toxicity on two linked trophic levels I. Effects of contaminated algae on Daphnia magna. Ecotoxicol Environ Saf 25:64–71. https://doi.org/10.1006/eesa.1993.1007
Gorbi G, Corradi MG, Torelli A, Bassi M (1996) Comparison between a normal and a Cr-tolerant strain of Scenedesmus acutus as a food source to Daphnia magna. Ecotoxicol Environ Saf 35:109–111. https://doi.org/10.1006/eesa.1996.0089
Gorbi G, Corradi MG, Invidia M, Rivara L, Bassi M (2002) Is Cr(VI) toxicity to Daphnia magna modified by food availability or algal exudates? The hypothesis of a specific chromium/algae/exudates interaction. Water Resour 36:1917–1926. https://doi.org/10.1016/S0043-1354(01)00403-1
Goulden CE, Place AR (1993) Lipid accumulation and allocation in daphniid cladocera. Bull Mar Sci 53:106–114
Gunnarsson JS, Castillo LE (2018) Ecotoxicology in tropical regions. Environ Sci Pollut Res 25:13203–13206. https://doi.org/10.1007/s11356-018-1887-4
Gusso-Choueri PK, Choueri RB, Lombardi AT, Melão MGG (2012) Effects of dietary copper on life-history traits of a tropical freshwater cladoceran. Arch Environ Contam Toxicol 62:589–598. https://doi.org/10.1007/s00244-011-9725-4
Gutierrez MF, Gagneten AM, Paggi JC (2010) Copper and chromium alter life cycle variables and the equiproportional development of the freshwater copepod Notodiaptomus conifer (SARS). Water Air Soil Pollut 213:275–286. https://doi.org/10.1007/s11270-010-0383-3
Gutierrez MF, Gagneten AM, Paggi JC (2012) Exposure to sublethal chromium and endosulfan alter the diel vertical migration (DVM) in freshwater zooplankton crustaceans. Ecotoxicology 21:37–47. https://doi.org/10.1007/s10646-011-0761-7
Hörcsik ZT, Oláh V, Balogh Á, Meszaros I, Simon dr L, Lakatos G (2006) Effect of chromium(VI) on growth, element and photosynthetic pigment composition of Chlorella pyrenoidosa. Acta Biol Marisiensis 50:19–23
Ismaiel MMS, Said AA (2018) Tolerance of Pseudochlorella pringsheimii to Cd and Pb stress: role of antioxidants and biochemical contents in metal detoxification. Ecotoxicol Environ Saf 30:704–712. https://doi.org/10.1016/j.ecoenv.2018.08.088
Ismail H, Mills S, Recknagel F (2019) Feeding evaluation of microcrustacea (Cladocera): responses to variations in cell volume of green and blue-green algae. Appl Ecol Environ Sci 17:7715–7725. https://doi.org/10.15666/aeer/1704_77157725
Jeyasingh PD, Pulkkinen K (2019) Does differential iron supply to algae affect Daphnia life history? An ionome-wide study. Oecologia 191:51–60. https://doi.org/10.1007/s00442-019-04482-1
Jouany JM, Vasseur P, Ferard JF (1982) Ecotoxicité directe et intégrée du chrome hexavalent sur deux niveaux trophiques associés: Chlorella vulgaris et Daphnia magna. Environ Pollut 27:207–221. https://doi.org/10.1016/0143-1471(82)90026-5
Kafil M, Berninger F, Koutra E, Kornaros M (2022) Utilization of the microalga Scenedesmus quadricauda for hexavalent chromium bioremediation and biodiesel production. Bioresour Technol 346:126665. https://doi.org/10.1016/j.biortech.2021.126665
Kilham SS, Kreeger DA, Goulden CE, Lynn SG (1997) Effects of algal food quality on fecundity and population growth rates of Daphnia. Freshw Biol 38:639–647. https://doi.org/10.1046/j.1365-2427.1997.00232.x
Koch U, von Elert E, Straile D (2009) Food quality triggers the reproductive mode in the cyclical parthenogen Daphnia (Cladocera). Oecologia 159:317–324. https://doi.org/10.1007/s00442-008-1216-6
Kunz PY, Kienle C, Gerhardt A (2010) Gammarus spp. in aquatic ecotoxicology and water quality assessment: toward integrated multilevel tests. Rev Environ Contam Toxicol 205:1–76. https://doi.org/10.1007/978-1-4419-5623-1_1
Latib NL, Yusoff FMd, Nagao N, Nizar H (2020) Growth of tropical cladocerans Ceriodaphnia cornuta G.O. Sars, 1885 and Moina micrura Kurz, 1875 fed with different diets. J Environ Biol 41:1224–1229. https://doi.org/10.22438/jeb/41/5(SI)/MS_14
Lesser E, Sheikh FN, Sikder M, Croteau M, Franklin N, Baalousha M, Ismail NS (2022) Water chemistry, exposure routes, and metal forms determine the bioaccumulation dynamics of silver (ionic and nanoparticulate) in Daphnia magna. Environ Toxicol Chem 41:726–738. https://doi.org/10.1002/etc.5271
Liang SXT, Wong LS, Dhanapal ACTA, Djearamane S (2020) Toxicity of metals and metallic nanoparticles on nutritional properties of microalgae. Water Air Soil Pollut 231:52. https://doi.org/10.1007/s11270-020-4413-5
Liu D, Wong PTS, Dutra BJ (1973) Determination of carbohydrate in Lake sediment by a modified phenol-sulfuric acid method. Water Res 7:741–746. https://doi.org/10.1016/0043-1354(73)90090-0
Liu Y, Jj Z, Hong Y (2017) Effects of metal ions on the cultivation of an oleaginous microalga Chlorella sp. Environ Sci Pollut Res 24:26594–26604. https://doi.org/10.1007/s11356-017-0258-x
Mano H, Iwasaki Y, Shinohara N (2022) Effect-based water quality assessment of rivers receiving discharges from legacy mines by using acute and chronic bioassays with two cladoceran species. Water Supply 22:3603–3616. https://doi.org/10.2166/ws.2022.003
Mansano AS, Souza JP, Cancino-Bernardi J, Venturini FP, Marangoni VS, Zucolotto V (2018) Toxicity of copper oxide nanoparticles to neotropical species Ceriodaphnia silvestrii and Hyphessobrycon eques. Environ Pollut 243:723–733. https://doi.org/10.1016/j.envpol.2018.09.020
Merga LB, Van den Brink PJ (2021) Ecological effects of imidacloprid on a tropical freshwater ecosystem and subsequent recovery dynamics. Sci Total Environ 784:147167. https://doi.org/10.1016/j.scitotenv.2021.147167
Miller PA, Lanno RP, McMaster ME, Dixon DG (1993) Relative contributions of dietary and waterborne copper to tissue copper burdens and waterborne-copper tolerance in rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 50:1683–1689. https://doi.org/10.1139/f93-189
Moreira RA, Mansano AS, Silva LC, Rocha O (2014) A comparative study of the acute toxicity of the herbicide atrazine to cladocerans Daphnia magna, Ceriodaphnia silvestrii and Macrothrix flabelligera. Acta Limnol Bras 26:1–8. https://doi.org/10.1590/S2179-975X2014000100002
Müller-Navarra D, Lampert W (1996) Seasonal patterns of food limitation in Daphnia galeata: separating food quantity and food quality effects. J Plankton Res 18:1137–1157. https://doi.org/10.1093/plankt/18.7.1137
Nainggolan E, Aryandari R, Fadholi H, Nugroho A, Suyono E (2015) Effects of chromium on chlorophyll-a, carbohydrate and protein contents in Tetraselmis sp. (Butcher 1959). KnE Life Sci 2:556. https://doi.org/10.18502/kls.v2i1.216
Nandini SS, Sarma SSS (2003) Population growth of some genera of cladocerans (Cladocera) in relation to algal food (Chlorella vulgaris) levels. Hydrobiologia 491:211–219. https://doi.org/10.1023/A:1024410314313
Ni IH, Wang WX, Tarn YK (2000) Transfer of Cd, Cr and Zn from zooplankton prey to mudskipper Periophthalmus cantonensis and glassy Ambassis urotaenia fishes. Mar Ecol Prog Ser 194:203–210
Nichols PB, Couch JD, Al Hamdani SH (2000) Selected physiological responses of Salvinia minima to different concentrations of chromium. Aquat Bot 68:313–319. https://doi.org/10.1590/S1677-04202008000100007
Nusch EA (1980) Comparison of different methods for chlorophyll and phaeopigments determination. Arch Hydrobiol 14:14–36
Oliveira-Neto AL (2000) Toxicity of some heavy metals (Cd, Cr, Pb) in lacustrine planktonic organisms from the subtropical region. Ph.D. thesis. Universidade de São Paulo, São Carlos, Brazil
Pancha I, Chokshi K, Maurya R, Trivedi K, Patidar SK, Ghosh A, Mishra S (2015) Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 189:341–348. https://doi.org/10.1016/j.biortech.2015.04.017
Pang B, Zeng M, Zhang W, Ye F, Shang C (2021) Influence of heavy metals on the growth of Chlorella vulgaris. J Biobased Mater Bioenergy 15:374–379. https://doi.org/10.1166/jbmb.2021.2051
Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer-Verlag, New York, pp 4–20
Pérez-Legaspi IA, Garatachia-Vargas M, Garcia-Villar AM, Rubio-Franchini I (2017) Sensitivity of the tropical cladoceran Ceriodaphnia cornuta to heavy metals. Revista Internacional De Contaminación Ambiental 33:49–56. https://doi.org/10.20937/rica.2017.33.01.04
Pham TL (2019) Effect of silver nanoparticles on tropical freshwater and marine microalgae. J Chem. https://doi.org/10.1155/2019/9658386
Pinto E, Sigaud-kutner TCS, Leitão MAS, Okamoto O, Morse D, Colepicolo E (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018. https://doi.org/10.1111/j.0022-3646.2003.02-193.x
Rai UN, Singh NK, Upadhyay AK, Verma S (2013) Chromate tolerance and accumulation in Chlorella vulgaris L.: role of antioxidant enzymes and biochemical changes in detoxification of metals. Bioresour Technol 136:604–609. https://doi.org/10.1016/j.biortech.2013.03.043
Rand GM (1995) Fundamentals of aquatic toxicology: effects, environmental fate, and risk assessment. Taylor Francis, Washington
Raymundo LB, Rocha O, Moreira RA, Miguel M, Daam MA (2019) Sensitivity of tropical cladocerans to chlorpyrifos and other insecticides as compared to their temperate counterparts. Chemosphere 220:937–942. https://doi.org/10.1016/j.chemosphere.2019.01.005
Regaldo L, Reno U, Gervasio S, Troiani H, Gagneten AM (2014) Effect of metals on Daphnia magna and cladocerans representatives of the Argentinean fluvial littoral. J Environ Biol 689–697
Rocha GS, Lombardi AT, Melão MGG (2016) Effect of copper contaminated food on the life cycle and secondary production of Daphnia laevis. Ecotoxicol Environ Saf 133:235–242. https://doi.org/10.1016/j.ecoenv.2016.07.011
Rodgher S, Espíndola ELG (2008a) Effects of interactions between algal densities and cadmium concentrations on Ceriodaphnia dubia fecundity and survival. Ecotoxicol Environ Saf 71:765–773. https://doi.org/10.1016/j.ecoenv.2007.08.012
Rodgher S, Espíndola ELG (2008b) The influence of algal densities on the toxicity of chromium for Ceriodaphnia dubia Richard (Cladocera, Crustacea). Braz J Biol 68:341–348. https://doi.org/10.1590/S1519-69842008000200015
Rodgher S, Lombardi AT, Melão MGG (2009) Evaluation onto life cycle parameters of Ceriodaphnia silvestrii submitted to 36 days dietary copper exposure. Ecotoxicol Environ Saf 13372:1748–1753. https://doi.org/10.1016/j.ecoenv.2009.03.009
Rodgher S, De Paulo FC, Costa MG, Contador TM, Rocha GS, Espíndola ELG (2020) Effects of phosphorus and zinc on the neotropical cladoceran Ceriodaphnia silvestrii by dietary routes. Water Air Soil Pollut. https://doi.org/10.1007/s11270-019-4370-z
Rodríguez MC, Barsanti L, Passarelli V, Evangelista V, Conforti V, Gualtieri P (2007) Effects of chromium on photosynthetic and photoreceptive apparatus of the alga Chlamydomonas reinhardtii. Environ Res 105:234–239. https://doi.org/10.1016/j.envres.2007.01.011
Rodriguez E, Santos C, Lucas E, Pereira M (2011) Evaluation of chromium(VI) toxicity to Chlorella vulgaris Beijerinck cultures. Fresenius Environ Bull 20:334–339
Sadeq SA, Beckerman AP (2019) The chronic effects of copper and cadmium on life history traits across cladocera species: a meta-analysis. Arch Environ Contam Toxicol 76:1–16. https://doi.org/10.1007/s00244-018-0555-5
Shakya M, Silvester E, Rees G, Rajapaksha KH, Faou P, Holland A (2022) Changes to the amino acid profile and proteome of the tropical freshwater microalga Chlorella sp. in response to copper stress. Ecotoxicol Environ Saf 233:113336. https://doi.org/10.1016/j.ecoenv.2022.113336
Silva JC, Echeveste P, Lombardi AT (2018) Higher biomolecules yield in phytoplankton under copper exposure. Ecotoxicol Environ Saf 161:57–63. https://doi.org/10.1016/j.ecoenv.2018.05.059
Silva LCM, Moreira RA, Pinto TJS, Ogura AP, Yoshii MPC, Lopes LFP, Montagner CC, Goulart BV, Daam MA, Espíndola ELG (2020) Acute and chronic toxicity of 2,4-D and fipronil formulations (individually and in mixture) to the Neotropical cladoceran Ceriodaphnia silvestrii. Ecotoxicology 29:1462–1475. https://doi.org/10.1007/s10646-020-02275-4
Sobrino-Figueroa A, Álvarez Hernandez SH, Silva CCA (2020) Evaluation of the freshwater copepod Acanthocyclops americanus (Marsh, 1983) (Cyclopidae) response to Cd, Cr, Cu, Hg, Mn, Ni and Pb. AIMS Environ Sci 7:449–463. https://doi.org/10.3934/environsci.2020029
Sodré EdO, Bozelli RL (2019) How planktonic microcrustaceans respond to environment and affect ecosystem: a functional trait perspective. Int Aquat Res 11:207–223. https://doi.org/10.1007/s40071-019-0233-x
Sofyan A, Shaw JR, Birge WJ (2006) Metal transfer from algae to cladocerans and the relative importance of dietary metal exposure. Environ Toxicol Chem 25:1034–1041. https://doi.org/10.1016/j.scitotenv.2006.07.003
Souza JP, Melo DC, Lombardi AT, Melão MGG (2014) Effects of dietborne cadmium on life history and secondary production of a tropical freshwater cladoceran. Ecotoxicology 23:1764–1773. https://doi.org/10.1007/s10646-014-1341-4
Sterner RW, Schulz KL (1998) Zooplankton nutrition: recent progress and a reality check. Aquat Ecol 32:261–279. https://doi.org/10.1023/A:1009949400573
Taipale SJ, Aalto SL, Galloway AWE, Kuoppamäki K, Nzobeuh P, Peltomaa E (2019) Eutrophication and browning influence Daphnia nutritional ecology. Inland Waters 9:374–394. https://doi.org/10.1080/20442041.2019.1574177
Tan Q-G, Wang W-X (2011) Contrasting patterns of cadmium bioaccumulation in freshwater cladocerans. Limnol Oceanogr 56:257–267. https://doi.org/10.4319/lo.2011.56.1.0257
Tessier AJ, Goulden CE (1982) Estimating food limitation in cladoceran populations. Limnol Oceanogr 27:707–717. https://doi.org/10.4319/lo.1982.27.4.0707
Thompson PA, Couture P (1993) Physiology of carbon assimilation in a green alga during exposure to and recovery from cadmium. Ecotoxicol Environ Saf 26:205–215. https://doi.org/10.1006/eesa.1993.1050
USEPA (2002) U.S. Environmental protection agency method 1002.0: Daphnid, Ceriodaphnia dubia, survival and reproduction test; chronic toxicity. 4th edition
USGS (2021) U.S. Geological survey mineral commodity summaries 2021 U.S. Geological survey, p 200. https://doi.org/10.3133/mcs2021
Vaiopoulou E, Gikas P (2020) Regulations for chromium emissions to the aquatic environment in Europe and elsewhere. Chemosphere 254:126876. https://doi.org/10.1016/j.chemosphere.2020.126876
Volgusheva A, Todorenko D, Baizhumanov A, Chivkunova O, Solovchenko A, Antal T (2022) Cadmium- and chromium-induced damage and acclimation mechanisms in Scenedesmus quadricauda and Chlorella sorokiniana. J Appl Phycol 34:1435–1446. https://doi.org/10.1007/s10811-022-02747-6
Wang WX (2013) Dietary toxicity of metals in aquatic animals: recent studies and perspectives. Chin Sci Bull 58:203–213. https://doi.org/10.1007/s11434-012-5413-7
WHO (2017) World Health Organization, guidelines for drinking-water quality: fourth edition incorporating the first addendum. Geneva: World Health Organization. CC BY-NC-SA 3.0 IGO
Widjaja A, Chien CC, Ju YH (2009) Study of increasing lipid production from fresh water microalgae Chlorella vulgaris. J Taiwan Inst Chem Eng 40:13–20. https://doi.org/10.1016/j.jtice.2008.07.007
Wilding J, Maltby L (2006) Relative toxicological importance of aqueous and dietary metal exposure to a freshwater crustacean: implications for risk assessment. Environ Toxicol Chem 25:1795–1801. https://doi.org/10.1897/05-316r1.1
Wu MN, Wang XC, Ma XY (2016) Phytotoxicity comparison of organic contaminants and heavy metals using Chlorella vulgaris. Desalin Water Treat 57:20809–20816. https://doi.org/10.1080/19443994.2015.1110537
Zhou J, Du N, Li D, Qin J, Li H, Chen G (2021) Combined effects of perchlorate and hexavalent chromium on the survival, growth and reproduction of Daphnia carinata. Sci Total Environ 769:144676. https://doi.org/10.1016/j.scitotenv.2020.144676
Acknowledgements
This work was supported by São Paulo Research Foundation (Fundação de Amparo a Pesquisa do Estado de São Paulo–FAPESP) for their financial support (Process number: 2011/07218-6). M.D. received support from the Portuguese Foundation for Science and Technology (FCT) through the strategic projects UIDB/04085/2020 (CENSE) and LA/P/0121/2020 (CHANGE).
Author information
Authors and Affiliations
Contributions
BHV, RNH and ELGE designed and performed the experiments. BHV, SR, ATL, M da GGM, MAD and ELGE analyzed the data. The first draft of the manuscript was written by BHV, SR, MAD and ELGE and all authors commented on previous versions of the manuscript. All authors reviewed the paper and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval
Not applicable.
Additional information
Handling Editor: Ted Harris
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Vieira, B.H., Rodgher, S., Haneda, R.N. et al. Importance of different exposure routes on the toxicity of chromium to planktonic organisms. Aquat Ecol (2023). https://doi.org/10.1007/s10452-023-10054-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10452-023-10054-6