Evaluation of the freshwater copepod <i>Acanthocyclops americanus</i> (Marsh, 1983) (Cyclopidae) response to Cd, Cr, Cu, Hg, Mn, Ni and Pb

Alma Sobrino-Figueroa; Sergio H. Álvarez Hernandez; Carlos Álvarez Silva C; Alma Sobrino-Figueroa; Sergio H. Álvarez Hernandez; Carlos Álvarez Silva C

doi:10.3934/environsci.2020029

AIMS Environmental Science

2020, Volume 7, Issue 6: 449-463. doi: 10.3934/environsci.2020029

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Research article

Evaluation of the freshwater copepod Acanthocyclops americanus (Marsh, 1983) (Cyclopidae) response to Cd, Cr, Cu, Hg, Mn, Ni and Pb

1.
Alejandro Villalobos Laboratory, Department of Hydrobiology, Metropolitan Autonomous University. Mexico City, Mexico
2.
Applied Phycology Laboratory, Department of Hydrobiology, Metropolitan Autonomous University. Mexico City, Mexico

Received: 19 August 2020 Accepted: 10 November 2020 Published: 11 November 2020

The toxic effect of cadmium, chromium, copper, mercury, manganese, nickel and lead on adult Acanthocyclops americanuscopepods was evaluated to determine the sensitivity of this species to these metals. Toxicity tests were carried out to determine the LC₅₀, after which bioassays were carried out with environmentally relevant sublethal concentrations in order to measure oxidative damage to cell membranes as well as neurotoxic effects. Cadmium was the most toxic metal and manganese was the least harmful. Copper had the greatest oxidative effect (lipid peroxidation) and nickel had the least effect. A 3% to 79% drop was observed in acetylcholinesterase (AchE) activity, with copper causing the greatest inhibitory effect. A. americanus sensitivity to cadmium, manganese and lead was similar to that recorded for Daphnia magna neonates, but the copepods were less sensitive to chromium, copper, mercury and nickel. The response of A. americanus to exposure to metals makes it possible to propose it as a test organism to evaluate the presence and effect of these elements, particularly cadmium, manganese and lead, in toxicity studies, and possibly for monitoring purposes.
- Acanthocyclops americanus,
- metal toxicity,
- lipoperoxidation,
- neurotoxic effects,
- freshwater copepods
Citation: Alma Sobrino-Figueroa, Sergio H. Álvarez Hernandez, Carlos Álvarez Silva C. Evaluation of the freshwater copepod Acanthocyclops americanus (Marsh, 1983) (Cyclopidae) response to Cd, Cr, Cu, Hg, Mn, Ni and Pb[J]. AIMS Environmental Science, 2020, 7(6): 449-463. doi: 10.3934/environsci.2020029

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Abstract

The toxic effect of cadmium, chromium, copper, mercury, manganese, nickel and lead on adult Acanthocyclops americanuscopepods was evaluated to determine the sensitivity of this species to these metals. Toxicity tests were carried out to determine the LC₅₀, after which bioassays were carried out with environmentally relevant sublethal concentrations in order to measure oxidative damage to cell membranes as well as neurotoxic effects. Cadmium was the most toxic metal and manganese was the least harmful. Copper had the greatest oxidative effect (lipid peroxidation) and nickel had the least effect. A 3% to 79% drop was observed in acetylcholinesterase (AchE) activity, with copper causing the greatest inhibitory effect. A. americanus sensitivity to cadmium, manganese and lead was similar to that recorded for Daphnia magna neonates, but the copepods were less sensitive to chromium, copper, mercury and nickel. The response of A. americanus to exposure to metals makes it possible to propose it as a test organism to evaluate the presence and effect of these elements, particularly cadmium, manganese and lead, in toxicity studies, and possibly for monitoring purposes.

References

[1]	De La Vega-Salazar Y (2003) Situación de los peces dulceacuícolas en México. Revista Ciencias UNAM 72: 20-30.
[2]	SEMARNAT (2016) Informe de la situación del medio ambiente en México. Compendio de estadísticas ambientales, indicadores clave de desempeñ o ambiental y crecimiento verde. Mexico: Semarnat.
[3]	Naranjo EJ, Dirzo R (2009) Impacto de los factores antropogénicos de afectación directa a las poblaciones silvestres de flora y fauna. In: CONABIO, Capital natural de México, Vol. II: Estado de conservación y tendencias de cambio. México: CONABIO 247-276.
[4]	Paulín-Vaca R, Hernández-Silva G, Lugo de la Fuente J (1997) Extracción secuencial de Cd, Co, Cu, Mn, Ni, Pb y Zn en sedimentos de la cuenca alta del Río Lerma. Actas INAGEQ 4: 85-96.
[5]	Avila-Perez P, Zarazua G, Tejeda S, et al. (2007) Evaluation of distribution and bioavailability of Cr, Mn, Fe, Cu, Zn and Pb in the waters of the upper course of the Lerma River. X-Ray Spectrom 36: 361-368.
[6]	Carrion C, Ponce-de Leon C, Cram S, et al. (2012) Potential use of water hyacinth (Eichhornia crassipes) in Xochimilco for metal phytoremediation. Agrociencia 46: 609-620.
[7]	Zarazúa G, Avila-Pérez P, Tejeda S, et al. (2013) Evaluación de los metales pesados Cr, Mn, Fe, Cu, Zn y Pb en sombrerillo de agua (Hydrocotyle ranunculoides) del curso alto del río Lerma, México. Rev Int Contam Ambie 29: 17-24.
[8]	Mercado-Borrayo BM, Heydrich SC, Rosas PI, et al. (2015) Organophosphorus and organochlorine pesticides bioaccumulation by Eichhornia crassipes in irrigation canals in an urban agricultural system. Int J Phytorem 17: 701-708.
[9]	Aldana G, Hernández M, Cramb S, et al. (2018) Trace metal speciation in a wastewater wetland and its bioaccumulation in tilapia Oreochromis niloticus. Chem Speciat Bioavailab 30: 23-32.
[10]	Tchounwou PB, Yedjou CG, Patlolla AK, et al. (2012) Heavy metals toxicity and the environment. EXS 101: 133-164.
[11]	Wu X, Cobbina SJ, Guanghua M, et al. (2016)A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ Sci Pollut Res 23:8244-8259.
[12]	Brito EMS, De la Cruz M, Barróna C, et al. (2015) Impact of hydrocarbons, PCBs and heavy metals on bacterial communities in Lerma River, Salamanca, Mexico: Investigation of hydrocarbon degradation potential. Sci Total Environ 521: 1-10.
[13]	Bojórquez L. Esquivel-Herrera A (2017) Contaminación química de la zona lacustre de Xochimilco. In: Bojórquez L. Contaminación química y biológica de la zona lacustre de Xochimilco.Mexico: UAM, 85-169.
[14]	Norma Oficial Mexicana NOM-001-Semarnat. Que establece los Límites Máximos Permitidos de contaminantes en las descargas de aguas residuales en aguas y bienes nacionales. Publicada en el Diario Oficial de la Federación el 6 de enero de 1997, México.
[15]	Golovanova IL (2008) Effects of heavy metals on the physiological and biochemical status of fishes and aquatic invertebrates. Inland Water Biol 1: 93-101.
[16]	Barata C, Varo I, Navarro JC, et al. (2005) Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol C 140: 175-186.
[17]	Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101: 13-30.
[18]	Chang LW, Suzuki T (1996) Toxicology of Metals. Lewis Publishers, 432-567.
[19]	Pulido MD, Parrish AR (2003) Metal-induced apoptosis: mechanisms. Mutat Res 533: 227-241.
[20]	Forget J, Pavillon JF, Beliaeff B, et al. (1999) Joint action of pollutant combinations (pesticides and metals) on survival (LC₅₀ values) and acetylcholinesterase activity of Tigriopus brevicornis (copepoda, harpacticoida). Environ Toxicol Chem 18: 912-918
[21]	Tsangaris C, Papathanasiou E, Cotou E (2007) Assessment of the impact of heavy metal pollution from a ferro-nickel smelting plant using biomarkers. Ecotoxicol Environ Saf 66: 232-43.
[22]	Enríquez-García C, Nandini S, Sarma SSS (2011) Demographic characteristics of the copepod Acanthocyclops americanus (Sars, 1863), (Copepoda:Cyclopoida) fed mixed algal (Scenedesmus acutus) rotifer (Brachionus havanensis) diet. Hydrobiologia 666: 59-69.
[23]	Elías-Gutiérrez M, Suárez Morales E, Silva Briano M, et al. (2008) Cladocera y Copepoda de las aguas continentales de México. Guía ilustrada. México: UNAM, ECOSUR, SEMARNAT-CONACYT, CONABIO. 57: 67-92.
[24]	Azad M, Agard JBR (2006) Comparative sensitivity of three tropical Cladoceran species (Diaphanosoma brachyurum, Ceriodaphnia rigaudii and Moinodaphnia macleayi) to six chemicals. J Environ Sci Health 41: 2713-2720.
[25]	NMX-AA-087-SCFI-2010 Análisis de agua - Evaluación de toxicidad aguda con Daphnia magna, Straus (Crustacea -Cladocera) - Método de prueba, México, 1-44.
[26]	USEPA (US Environmental Protection Agency) (2002) Methods for Measuring the Acute Toxicity of Effluents and Receiving Waters to Freshwater and Marine Organisms. Washington DC: U.S: Environmental Protection Agency, EPA-821-R-02-012.
[27]	FAO (1986) Manual of methods in aquatic environment research. Part 10. Short-term static bioassays. FAO Fisheries Technical Paper. 247: 1-62.
[28]	APHA, AWWA y WPFC (1994) Métodos estándar para el examen de aguas y aguas de desecho, 64º México: Ed. Interamericana, 124-278.
[29]	Diz FR, Araújo CV, Moreno-Garrido I, et al. (2009) Short-term toxicity tests on the harpacticoid copepod Tisbe battagliai: lethal and reproductive endpoints. Ecotoxicol Environ Saf 72: 1881-1886.
[30]	Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Meth Enzym51: 302.
[31]	Ellman L, Courtey KD, Andreas VJr, et al. (1961) A new rapid calorimetric determination of cholinesterase activity. Biochem Pharmacol 7: 88-98
[32]	Guilhermino L, Lopes MC, Carvalho AP, et al. (1996) Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia magna. Chemosphere 32: 727-738.
[33]	Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Annals Biochem 72: 248-254.
[34]	Hintze JL (1997) NCSS 97: Statistical System for Windows. NCSS. Kaysville, UT.
[35]	Raisuddin S, Kwok KWH, Leung KMY, et al. (2007) The copepod Tigriopus: A promising marine model organism for ecotoxicology and environmental genomics. Aquatic Toxicol 83: 161-173.
[36]	Kulkarni D, Gergs A, Hommen U, et al. (2013) A plea for the use of copepods in freshwater ecotoxicology. Environ Sci Pollut Res 20: 75-85.
[37]	Bo-Mi K, Jae-Sung R, Chang-Bum J, et al. (2014) Heavy metals induce oxidative stress and trigger oxidative stress-mediated heat shock protein (hsp) modulation in the intertidal copepod Tigriopus japonicus. Comp Biochem Physiol Part C 166: 65-74.
[38]	Brown RJ, Rundle SD, Hutchinson TH, et al. (2005) A microplate freshwater copepod bioassay for evaluating acute and chronic effects of chemical. Environ Toxicol Chem 24: 1528-1531.
[39]	Soto E, Oyarce G, Inzunza B, et al. (2003) Acute toxicity of organic and inorganic compounds on the freshwater cyclopoid copepod Eucyclops neumani neumani (Pesta, 1927). Bull Environ Contam Toxicol 70: 1017-1021.
[40]	Devdutt K, Gergs A, Hommen U, et al. (2013) A plea for the use of copepods in freshwater ecotoxicology. Environ Sci Pollut Res 20: 75-85.
[41]	Baudouin MF, Scoppa P (1974) Acute toxicity of various metals of freshwater zooplankton. Bull Environ Contam Toxicol 12: 741-751.
[42]	WongCK, Pak AP (2004) Acute and Subchronic Toxicity of the Heavy Metals Copper, Chromium, Nickel, and Zinc, Individually and in Mixture, to the Freshwater Copepod Mesocyclops pehpeiensis. Bull Environ Contam Toxicol 73: 190-196.
[43]	Lalande M, Pinel-Alloul B (1986) Acute toxicity of cadmium, copper, mercury and zinc to tropocyclops prasinus mexicanus (cyclopoida, copepoda) from three quebec lakes. Environ Toxicol Chem 5: 95-102.
[44]	Abbasi SA, Nipaney PC, Soni R (1988) Studies on environmental management of mercury (II), Chromium (VI) and zinc (II) with respect to the impact on some arthropods and protozoans. Inter J Environmental Studies 32: 181-187.
[45]	Ecotox Database. EPA Available at https://cfpub.epa.gov/ecotox/
[46]	Moraitou-Apostolopoulou M, Verriopoulos G (1982) Individual and combined toxicity of three heavy metals, Cu, Cd and Cr for marine copepod Tisbe holothuriae. Hydrobiologia 87: 83-87
[47]	Lee KW, Raisuddin S, Hwang DS, et al. (2007) Acute Toxicities of Trace Metals and Common Xenobiotics to the Marine Copepod Tigriopus japonicus: Evaluation of Its Use as a Benchmark Species for Routine Ecotoxicity Tests in Western Pacific Coastal Regions. Environ Toxicol 22: 532-538
[48]	Emadeldeen HM (2017) Acute Toxicity of Cadmium and Nickel to Three Marine Copepods. Sci J King Faisal Univer 18: 9-16.
[49]	Pane L, Mariottini GL, Lodi A, et al. (2008) Effects of heavy metals on laboratory reared Tigriopus fulvus Fischer (Copepoda: Harpacticoida). In: Brown SE, Welton WC Heavy Metal Pollution. Nova Science Publishers, Inc, 158-165.
[50]	Hutchinson TH, Williams TD, Eales GJ (994) Toxicity of cadmium, hexavalent chromium and copper to marine fish larvae (Cyprinodon variegatus) and copepods (Tisbe battagliai). Mar Environ Res. 38: 275-290.
[51]	Barka S, Pavillon JF, Amiard JC (2001) Influence of different essential and nonessentialmetals on MTLP levels in the copepod Tigriopus brevicornis. Comp Biochem Physiol C 128: 479-493.
[52]	Mance G(1987) Pollution threat of heavy metals in aquatic environments. London: Elsevier Aplied Science, 45-123.
[53]	Traudt EM, Ranville JF, Meye JS (2017) Effect of age on acute toxicity of cadmium, copper, nickel, and zinc in individual-metal exposures to Daphnia magna neonates. Environ Toxicol Chem 36: 113-119.
[54]	Moldovan OT, Melega IN, Leveib E, et al. (2013) A simple method for assessing biotic indicators and predicting biodiversity in the hyporheic zone of a river polluted with metals. Ecol Indic 24: 123-136.
[55]	El-Shabrawy GM, Elowa SE, Rizk ST, et al. (2005) Impact of industrial pollution on zooplankton community structure in Rosetta Nile Branch at Kafr El-Zayat area Egypt. Afr J Biol Sci 1: 1-14.
[56]	Abdel-Halim AS, Waheed ME, El-ShabrawyGM, Fawzia MF (2013)Sewage pollution and zooplankton assemblages along the Rosetta Nile branch at El Rahawy area, Egypt. Int J Environ Sci Engin 4: 29-45.
[57]	Krupa EG (2007) Structural characteristics of zooplankton of the Shardarinskoe reservoir and their use in water quality assessment. Water Resour 34: 712-717.
[58]	Gagneten AM, Paggi JC (2009) Effects of heavy metal contamination (Cr, Cu, Pb, Cd) and eutrophication on zooplankton in the lower basin of the Salado River (Argentina). Water Air Soil Pollut 198: 317-334.
[59]	United Nations (2009) The globally harmonized system of classification and labelling of chemicals. ST/SG/AC.10/30/Rev.3. Available from: https://www.unece.org/fileadmin/DAM/trans/danger/publi/ghs/ghs_rev04/English/ST-SG-AC10-30-Rev4e.pdf
[60]	Vasseur P, Cossu-Leguille C (2006) Linking molecular interactions to consequent effects of persistent organic pollutants (POPs) upon populations. Chemosphere 62: 1033-42.
[61]	Hagger J, Malcolm JB, Lowe D, et al. (2008) Application of biomarkers for improving risk assessments of chemicals under the Water Framework Directive: A case study. Mar Poll Bull 56: 1111-1118.
[62]	Broeg K, Westernhagen H, Zander S, et al. (2005) The bioeffect assessment index (BAI) a concept for the quantification of effects of marine pollution by an integrated biomarker approach. Mar Poll Bull 50: 495-503.
[63]	Volodymyr I L (2011) Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicol 101: 13-30.
[64]	Wang MH, Wang GZ (2009) Biochemical response of the copepod Tigriopus japonicusMori experimentally exposed to cadmium. Arch Environ Contam Toxicol 57: 707-717
[65]	Wang MH, Wang GZ (2010) Oxidative damage effects in the copepod Tigriopus japonicusMori experimentally exposed to nickel. Ecotoxicol 19: 273-284.
[66]	USEPA (1998). SCE policy issues related to the food quality protection act. Office of pesticide programs science policy on the use of cholinesterase inhibition for risk assessment of organophosphate and carbamate pesticides. Office of Pesticide Programs. Washington DC: US Environmental Protection Agency 20460.
[67]	Dailianis S, Domouhtsidou GP, Raftopoulou E, et al. (2003). Evaluation of neutral red retention assay, micronucleus test, acetylcholinesterase activity and a signal transduction molecule (cAMP) in tissues of Mytilus galloprovincialis (L.), in pollution monitoring. Mar Environ Res 56: 443-470.
[68]	Stefano B, Ilaria C, Silvano F (2008). Cholinesterase activities in the scallop Pecten jacobaeus: Characterization and effects of exposure to aquatic contaminants. Sci Total Environ 392: 99-109.

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