Abstract
There is a lack of information regarding the effects on biochemical markers in invertebrates diet-exposed to inorganic mercury. In the present study, juvenile black tiger prawn (Penaeus monodon) were fed with food dosed with mercuric chloride (low: 0.2 mg kg−1; medium: 0.77 mg kg−1; high: 1.41 mg kg−1; higher: 2.52 mg kg−1) and control (0.03 mg kg−1) over 12 days. At the end of exposure periods, ventral nerve cord, compound eyes and muscle were dissected for biochemical marker analyses (acetylcholinesterase – AChE; lipoperoxidation – LPO; glutathione S-transferase – GST; catalase – CAT). Prawn muscle showed an increase in total mercury concentration over time for low and high treatments, but did not show an accumulation in comparison to controls. AChE activity tended to decrease over time in all tissues. CAT activity increased over time in controls and lower dose treatments but was suppressed in the higher treatment relative to controls on day 12; indicating that inorganic mercury is impacting the normal stress response by reducing the capacity to degrade hydrogen peroxide. In contrast, no effect was observed in LPO and GST activity. A depuration treatment was performed and compared to medium treatment; only AChE and GST activities from muscle showed significant difference, with AChE activity from depuration treatment lower than medium treatment, while the opposite was observed in GST activity. Overall, the low mercury accumulation observed over 12 days of exposure may have limited the biochemical stress responses, which could also have limited the detection of differences in the depuration treatment relative to medium treatment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdullah AR, Kumar A, Chapman JC (1994) Inhibition of acetylcholinesterase in the australian freshwater shrimp (Paratya australiensis) by profenofos. Environ Toxicol Chem 13:1861–1866. https://doi.org/10.1002/etc.5620131118
Ahmad NI et al. (2015) The mercury levels in crustaceans and cephalopods from Peninsular Malaysia. Environ Sci Pollut Res 22:12960–12974. https://doi.org/10.1007/s11356-015-4415-9
Australia New Zealand Food Authority (2000) Australia New Zealand Food Standards Code - Standard 1.4.1 - Contaminants and Natural Toxicants
Bainy ACD, Saito E, Carvalho PSM, Junqueira VBC (1996) Oxidative stress in gill, erythrocytes, liver and kidney of Nile tilapia (Oreochromis niloticus) from a polluted site. Aquat Toxicol 34:151–162. https://doi.org/10.1016/0166-445X(95)00036-4
Barbieri E, Passos EA, Garcia CAB (2005) Use of metabolism to evaluate the sublethal toxicity of mercury on Farfantepaneus brasiliensis larvae (Latreille 1817, Crustacean). J Shellfish Res 24:1229–1233
Berntssen MHG, Aatland A, Handy RD (2003) Chronic dietary mercury exposure causes oxidative stress, brain lesions, and altered behaviour in Atlantic salmon (Salmo salar) parr. Aquat Toxicol 65:55–72. https://doi.org/10.1016/s0166-445x(03)00104-8
Boudou A, Ribeyre F (1985) Experimental study of trophic contamination of Salmo gairdneri by two mercury compounds — HgCl2 and CH3HgCl — analysis at the organism and organ levels. Water Air Soil Pollut 26:137–148. https://doi.org/10.1007/BF00292064
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
Brandão F et al. (2015) Unravelling the mechanisms of mercury hepatotoxicity in wild fish (Liza aurata) through a triad approach: bioaccumulation, metabolomic profiles and oxidative stress. Metallomics 7:1352–1363. https://doi.org/10.1039/C5MT00090D
Cambier S, Bénard G, Mesmer-Dudons N, Gonzalez P, Rossignol R, Brèthes D, Bourdineaud JP (2009) At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio). Int J Biochem Cell Biol 41:791–799. https://doi.org/10.1016/j.biocel.2008.08.008
Cappello T et al. (2016a) Insights into the mechanisms underlying mercury-induced oxidative stress in gills of wild fish (Liza aurata) combining 1H NMR metabolomics and conventional biochemical assays. Sci Total Environ 548:13–24. https://doi.org/10.1016/j.scitotenv.2016.01.008
Cappello T, Pereira P, Maisano M, Mauceri A, Pacheco M, Fasulo S (2016b) Advances in understanding the mechanisms of mercury toxicity in wild golden grey mullet (Liza aurata) by 1H NMR-based metabolomics. Environ Pollut 219:139–148. https://doi.org/10.1016/j.envpol.2016.10.033
Chen JC, Liu PC, Lei SC (1990) Toxicities of ammonia and nitrite to Penaeus monodon adolescents. Aquaculture 89:127–137. https://doi.org/10.1016/0044-8486(90)90305-7
Ciacci C et al. (2012) Effects of sublethal, environmentally relevant concentrations of hexavalent chromium in the gills of Mytilus galloprovincialis. Aquat Toxicol 120-121:109–118. https://doi.org/10.1016/j.aquatox.2012.04.015
Čolović MB, Krstić DZ, Lazarević-Pašti TD, Bondžić AM, Vasić VM (2013) Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11:315–335. https://doi.org/10.2174/1570159X11311030006
Costa JRMA, Mela M, de Assis HCD, Pelletier E, Randi MAF, Ribeiro CAD (2007) Enzymatic inhibition and morphological changes in Hoplias malabaricus from dietary exposure to lead (II) or methylmercury. Ecotox Environ Safe 67:82–88
Depew DC et al. (2012) Toxicity of dietary methylmercury to fish: derivation of ecologically meaningful threshold concentrations. Environ Toxicol Chem 31:1536–1547. https://doi.org/10.1002/etc.1859
Devi M, Fingerman M (1995) Inhibition of acetylcholinesterase activity in the central nervous system of the red swamp crayfish, Procambarus clarkii, by mercury, cadmium, and lead. Bull Environ Contam Toxicol 55:746–750. https://doi.org/10.1007/BF00203762
Elahi M, Esmaili-Sari A, Bahramifar N (2012) Total mercury levels in selected tissues of some marine crustaceans from Persian Gulf, Iran: variations related to length, weight and sex. Bull Environ Contam Toxicol 88:60–64. https://doi.org/10.1007/s00128-011-0451-4
Ellman GL, Courtney KD, Andres Jr V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Elumalai M, Antunes C, Guilhermino L (2007) Enzymatic biomarkers in the crab Carcinus maenas from the Minho River estuary (NW Portugal) exposed to zinc and mercury. Chemosphere 66:1249–1255. https://doi.org/10.1016/j.chemosphere.2006.07.030
Evans DW, Kathman RD, Walker WW (2000) Trophic accumulation and depuration of mercury by blue crabs (Callinectes sapidus) and pink shrimp (Penaeus duorarum). Mar Environ Res 49:419–434. https://doi.org/10.1016/s0141-1136(99)00083-5
FAO (2016) The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all, Rome
Feng C et al. (2015) Specific pathways of dietary methylmercury and inorganic mercury determined by mercury speciation and isotopic composition in zebrafish (Danio rerio). Environ Sci Technol 49:12984–12993. https://doi.org/10.1021/acs.est.5b03587
Fossi MC, Savelli C, Casini S, Franchi E, Mattei N, Corsi I (1997) Multi response biomarker approach in the crab Carcinus aestuarii experimentally exposed to benzo a pyrene, polychlorobiphenyls and methyl mercury. Biomarkers 2:311–319. https://doi.org/10.1080/135475097231544
Frasco MF, Colletier J-P, Weik M, Carvalho F, Guilhermino L, Stojan J, Fournier D (2007) Mechanisms of cholinesterase inhibition by inorganic mercury. FEBS J 274:1849–1861. https://doi.org/10.1111/j.1742-4658.2007.05732.x
Frasco MF, Fournier D, Carvalho F, Guilhermino L (2006) Cholinesterase from the common prawn (Palaemon serratus) eyes: Catalytic properties and sensitivity to organophosphate and carbarnate compounds. Aquat Toxicol 77:412–421. https://doi.org/10.1016/j.auqatox.2006.01.011
Frasco MF, Fournier D, Carvalho F, Guilhermino L (2008) Does mercury interact with the inhibitory effect of dichlorvos on Palaemon serratus (Crustacea: Decapoda) cholinesterase? Sci Total Environ 404:88–93. https://doi.org/10.1016/j.scitotenv.2008.06.012
Gentès S et al. (2015) Specific effects of dietary methylmercury and inorganic mercury in zebrafish (Danio rerio) determined by genetic, histological, and metallothionein responses. Environ Sci Technol 49:14560–14569. https://doi.org/10.1021/acs.est.5b03586
Guo H, Miao YT, Xian JA, Qian K, Wang AL (2015) Expression profile of antioxidant enzymes in hemocytes from freshwater prawn Macrobrachium rosenbergii exposed to an elevated level of copper. Bull Environ Contam Toxicol 95:447–451. https://doi.org/10.1007/s00128-015-1618-1
Handy RD, Penrice WS (1993) The influence of high oral doses of mercuric chloride on organ toxicant concentrations and histopathology in rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol C Pharmacol Toxicol 106:717–724. https://doi.org/10.1016/0742-8413(93)90232-A
Harada M (1995) Minamata disease: Methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol 25:1–24. https://doi.org/10.3109/10408449509089885
Harayashiki CAY, Reichelt-Brushett A, Cowden K, Benkendorff K (2018) Effects of oral exposure to inorganic mercury on the feeding behaviour and biochemical markers in yellowfin bream (Acanthopagrus australis). Mar Environ Res 134:1–15. https://doi.org/10.1016/j.marenvres.2017.12.018
Harayashiki CAY, Reichelt-Brushett AJ, Liu L, Butcher P (2016) Behavioural and biochemical alterations in Penaeus monodon post-larvae diet-exposed to inorganic mercury. Chemosphere 164:241–247. https://doi.org/10.1016/j.chemosphere.2016.08.085
Huang W, Cao L, Ye ZJ, Yin XB, Dou SZ (2010) Antioxidative responses and bioaccumulation in Japanese flounder larvae and juveniles under chronic mercury exposure. Comp Biochem Physiol C Toxicol Pharmacol 152:99–106
Keen JH, Habig WH, Jakoby WB (1976) Mechanism for the several activities of the glutathione S-transferases. J Biol Chem 251:6183–6188
Kidd K, Clayden M, Jardine T (2012) Bioaccumulation and biomagnification of mercury through food webs. In: Liu G, Cai Y, O’Driscoll N (eds) Environmental chemistry and toxicology of mercury. John Wiley & Sons, Inc, New Jersey, p 453–499.
Kim BM, Rhee JS, Jeong CB, Seo JS, Park GS, Lee YM, Lee JS (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 Toxicol Pharmacol 166:65–74. https://doi.org/10.1016/j.cbpc.2014.07.005
Male YT, Reichelt-Brushett AJ, Pocock M, Nanlohy A (2013) Recent mercury contamination from artisanal gold mining on Buru Island, Indonesia – potential future risks to environmental health and food safety. Mar Pollut Bull 77:428–433. https://doi.org/10.1016/j.marpolbul.2013.09.011
Mela M, Neto FF, Yamamoto FY, Almeida R, Grotzner SR, Ventura DF, Ribeiro CAD (2014) Mercury distribution in target organs and biochemical responses after subchronic and trophic exposure to Neotropical fish Hoplias malabaricus. Fish Physiol Biochem 40:245–256. https://doi.org/10.1007/s10695-013-9840-4
Monteiro DA, Rantin FT, Kalinin AL (2010) Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã, Brycon amazonicus (Spix and Agassiz, 1829). Ecotoxicology 19:105–123
Monteiro DA, Rantin FT, Kalinin AL (2013) Dietary intake of inorganic mercury: bioaccumulation and oxidative stress parameters in the neotropical fish Hoplias malabaricus. Ecotoxicology 22:446–456
Motoh H (1985) Biology and ecology of Penaeus monodon. Paper presented at the Proceedings of the First International Conference on the Culture of Penaeid Prawns/Shrimps, Iloilo City, Philippines
Oakes KD, Van Der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463. https://doi.org/10.1016/S0166-445X(02)00204-7
Oliveri E et al. (2016) Mobility of mercury in contaminated marine sediments: Biogeochemical pathways. Mar Chem 186:1–10. https://doi.org/10.1016/j.marchem.2016.07.002
Padula D, Greenfield H, Cunningham J, Kiermeier A, McLeod CW (2016) Australian seafood compositional profiles: A pilot study. Vitam D Mercury Content Food Chem 193:106–111. https://doi.org/10.1016/j.foodchem.2014.11.057
Peng X, Liu F, Wang WX (2016) Organ-specific accumulation, transportation, and elimination of methylmercury and inorganic mercury in a low Hg accumulating fish. Environ Toxicol Chem 35:2074–2083. https://doi.org/10.1002/etc.3363
Rana SVS, Singh R, Verma S (1995) Mercury-induced lipid peroxidation in the liver, kidney, brain and gills of a fresh water fish. Channa punctatus Jpn J Ichthyol 42:255–259
Ratn A, Prasad R, Awasthi Y, Kumar M, Misra A, Trivedi SP (2018) Zn2+ induced molecular responses associated with oxidative stress, DNA damage and histopathological lesions in liver and kidney of the fish, Channa punctatus (Bloch, 1793). Ecotox Environ Safe 151:10–20. https://doi.org/10.1016/j.ecoenv.2017.12.058
Reichelt-Brushett AJ et al. (2017) Geochemistry and mercury contamination in receiving environments of artisanal mining wastes and identified concerns for food safety. Environ Res 152:407–418. https://doi.org/10.1016/j.envres.2016.07.007
Rumisha C, Mdegela RH, Kochzius M, Leermakers M, Elskens M (2016) Trace metals in the giant tiger prawn Penaeus monodonand mangrove sediments of the Tanzania coast: is there a risk to marine fauna and public health? Ecotox Environ Safe 132:77–86. https://doi.org/10.1016/j.ecoenv.2016.05.028
Seebaugh DR, Wallace WG, L’Amoreaux WJ, Stewart GM (2012) Assimilation of elements and digestion in grass shrimp pre-exposed to dietary mercury. Arch Environ Contam Toxicol 63:230–240
Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219. https://doi.org/10.1111/j.1432-1033.1993.tb18025.x
Singaram G, Harikrishnan T, Chen FY, Bo J, Giesy JP (2013) Modulation of immune-associated parameters and antioxidant responses in the crab (Scylla serrata) exposed to mercury. Chemosphere 90:917–928
Sofia HAH, Sugiharto E (2016) Acute and chronic toxicity of mercury exposure in seafood and human populations near a small-scale gold mining area. Int J Public Health Sci 5:257–266. https://doi.org/10.11591/.v5i3.4794
Suresh A, Sivaramakrishna B, Victoriamma PC, Radhakrishnaiah K (1992) Comparative study on the inhibition of acetylcholinesterase activity in the freshwater fish Cyprinus carpio by mercury and zinc. Biochem Int 26:367–375
Tu HT, Silvestre F, Scippo ML, Thome JP, Phuong NT, Kestemont P (2009) Acetylcholinesterase activity as a biomarker of exposure to antibiotics and pesticides in the black tiger shrimp (Penaeus monodon). Ecotox Environ Safe 72:1463–1470. https://doi.org/10.1016/j.ecoenv.2009.04.008
Walker TI (1988) Mercury concentrations in edible tissues of elasmobranchs, teleosts, crustaceans and molluscs from south-eastern Australian waters. Mar Freshw Res 39:39–49. https://doi.org/10.1071/MF9880039
Walker TR (2016) Mercury concentrations in marine sediments near a former mercury cell chlor-alkali plant in eastern Canada. Mar Pollut Bull 107:398–401. https://doi.org/10.1016/j.marpolbul.2016.03.033
Wang L, Wu YL, Wang JX, Liu N, Wang Q (2014) Physiological changes and acetylcholinesterase activity in the cladoceran Moina macrocopa (Straus, 1820) exposed to mercury and sodium dodecyl sulfate. Crustaceana 87:1678–1690. https://doi.org/10.1163/15685403-00003388
Wang WX, Wong RSK (2003) Bioaccumulation kinetics and exposure pathways of inorganic mercury and methylmercury in a marine fish, the sweetlips Plectorhinchus gibbosus. Mar Ecol Prog Ser 261:257–268
Wang X, Wu F, Wang WX (2017) In vivo mercury demethylation in a marine fish (Acanthopagrus schlegeli). Environ Sci Technol 51:6441–6451. https://doi.org/10.1021/acs.est.7b00923
Weis JS (2014) Physiological, developmental and behavioral effects of marine pollution.. Springer, Netherlands
Yamuna A, Bhavan PS, Geraldine P (2012) Glutathione S-transferase and metallothionein levels in the freshwater prawn Macrobrachium malcolmsonii exposed to mercury. J Environ Biol 33:133–137
Quintaneiro C, Monteiro M, Soares AMVN, Ranville J, Nogueira AJA (2014) Cholinesterase activity on Echinogammarus meridionalis (Pinkster) and Atyaephyra desmarestii (Millet): characterisation and invivo effects of copper and zinc Ecotoxicology 23:449–458. https://doi.org/10.1007/s10646-014-1204-z
van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review Environmental Toxicology and Pharmacology 13:57–149. https://doi.org/10.1016/S1382-6689(02)00126-6
Zaman K, Pardini RS (1996) An overview of the relationship between oxidative stress and mercury and arsenic Toxic Substance Mechanisms 15:151
Acknowledgements
C. Harayashiki was granted the Science without Border Scholarship from CAPES Foundation (Brazil; Process number BEX 1466/13-5). This work has been supported by Southern Cross University and the Environmental Analytical Laboratory.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Harayashiki, C.A.Y., Reichelt-Brushett, A., Butcher, P. et al. Ingestion of inorganic mercury by juvenile black tiger prawns (Penaeus monodon) alters biochemical markers. Ecotoxicology 27, 1225–1236 (2018). https://doi.org/10.1007/s10646-018-1975-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-018-1975-8