Abstract
To examine the spectrum of selenium toxicity between hardy and less hardy species of the same life stages, short-term and longer-term exposures in juvenile air-breathing fish Channa punctata (Bloch, 1973) and non-air-breathing fish Ctenopharyngodon idella (Cuvier, 1844) were assessed. Acute exposures revealed a greater 96-h median lethal concentration (LC50) for C. punctata (14.67 mg/l) compared to C. idella (7.98 mg/l). During their chronic exposure, both fishes’ hemoglobin content (Hb), red blood cells (RBC), and hematocrit (HCT) markedly decreased (p < 0.05), although their clotting time (CT) significantly increased. At 96 h, immune-modulation was observed where total protein and serum globulin levels in both fishes considerably decreased (p < 0.05) compared to the first exposure at 0 days, although total glucose, triglyceride, cholesterol, and albumin levels in both fishes significantly increased (p < 0.05) at 30 days. The lower cholesterol levels in C. punctata compared to C. idella are suggestive of a disrupted cholesterol transformation pathway. The greater total protein, triglyceride, albumin, and globulin levels in C. punctata compared to C. idella are suggestive of a comparatively robust immune capacity. In essence, selenium toxicity in the wild could manifest as disrupted metabolic pathways and downregulated immune capacity for less hardy species. In general, both fish species displayed significant alterations in their hematological and biochemical responses with increased exposure duration and elevated toxicant concentrations. This comparative investigation could improve the knowledge-spectrum of selenium toxicity in the wild as well as an understanding of secondary stress responses critically evident in hematological and biochemical parameters.
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References
Saha S, Chukwuka AV, Mukherjee D, Saha NC, Adeogun AO (2022) Hydrological connectivity, surface water quality and distribution of fish species within sub-locations of an urban oxbow lake, East India. Watershed Ecology and the Environment 4:44–58
Okonji SO, Achari G, Pernitsky D (2021) Environmental impacts of selenium contamination: a review on current-issues and remediation strategies in an aqueous system. Water 13(11):1473
Gopi N et al (2021) Interactive effects of freshwater acidification and selenium pollution on biochemical changes and neurotoxicity in Oreochromis mossambicus. Comp Biochem Physiol C: Toxicol Pharmacol 250:109161
Gobi N et al (2018) Bioaccumulation, cytotoxicity and oxidative stress of the acute exposure selenium in Oreochromis mossambicus. Ecotoxicol Environ Saf 162:147–159
Wen H, Carignan J (2007) Reviews on atmospheric selenium: emissions, speciation and fate. Atmos Environ 41(34):7151–7165
Young TF, Finley K, Adams WJ, Besser J, Hopkins WD, Jolley D, McNaughton E, Presser TS, Shaw DP, Unrine J (2010) Appendix A: Selected case studies of ecosystem contamination by Se. Ecological Assessment of Selenium in the Aquatic Environment 257–292
Maher B et al (2010) Environmental sources, speciation and partitioning of selenium. Ecological assessment of selenium in the aquatic environment. Taylor & Francis, pp 47–92
Adams WJ et al (2015) Long-term monitoring of arsenic, copper, selenium, and other elements in Great Salt Lake (Utah, USA) surface water, brine shrimp, and brine flies. Environ Monit Assess 187(3):1–13
Chapman PM et al (2010) Ecological assessment of selenium in the aquatic environment. CRC Press
George MW, Wagner LA (2009) Selenium recycling in the United States in 2004, chap. T of Sibley, S.R., Flow studies for recycling metal commodities in the United States: U.S. Geological Survey Circular 1196–T, p T1–T7
Lemly AD (2004) Aquatic selenium pollution is a global environmental safety issue. Ecotoxicol Environ Saf 59(1):44–56
Dhara K et al (2021) Effects of short-term selenium exposure on respiratory activity and proximate body composition of early-life stages of Catla catla, Labeo rohita and Cirrhinus mrigala. Environ Toxicol Pharmacol 1:103805
Fordyce FM (2013) Selenium deficiency and toxicity in the environment. Essentials of medical geology. Springer, pp 375–416
Lindh U (2013) Biological functions of the elements. Essentials of medical geology. Springer, pp 129–177
Sharma VK et al (2017) Assessment of toxicity of selenium and cadmium selenium quantum dots: a review. Chemosphere 188:403–413
Quinnell S, Hulsman K, Davie PJ (2004) Protein model for pollutant uptake and elimination by living organisms and its implications for ecotoxicology. Mar Ecol Prog Ser 274:1–16
Janz DM et al (2010) Selenium toxicity to aquatic organisms. Ecological assessment of selenium in the aquatic environment 141–231
Dhara K, Chukwuka AV, Saha S, Saha NC, Faggio C (2022) Effects of short-term selenium exposure on respiratory activity and proximate body composition of early-life stages of Catla catla, Labeo rohita and Cirrhinus mrigala. Environ Toxicol Pharmacol 90:103805
Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5(7):374–381
Bonga SW (1997) The stress response in fish. Physiol Rev 77(3):591–625
Rebl A, Seibel H, Baßmann B (2021) Blood will tell: what hematological analyses can reveal about fish welfare. Front Vet Sci 8:194
Oberle B, Bringezu S, Hatfield-Dodds S, Hellweg S, Schandl H, Clement J (2019) Global resources outlook: International Resource Panel, United Nations Envio, Paris, France, p 162
Jerome FC, Hassan A, Chukwuka AV (2020) Metalloestrogen uptake, antioxidant modulation and ovotestes development in Callinectes amnicola (blue crab): a first report of crustacea intersex in the Lagos lagoon (Nigeria). Sci Total Environ 704:135235
Saha S, Chukwuka AV, Mukherjee D, Dhara K, Adeogun AO, Saha NC (2022) Effects of short-term sub-lethal diazinon® exposure on behavioural patterns and respiratory function in Clarias batrachus: inferences for adaptive capacity in the wild. Chem Ecol 38(2):180–194
APHA (2012) Standard Methods for the Examination of Water and Waste Water. 22nd Edition, American Public Health Association, American Water Works Association, Water Environment Federation. p 541
USEPA IRIS (2011) Integrated risk information system. Environmental protection agency region I, Washington DC, 20460. http://www.epa.gov/iris/
Finney D (1971) Statistical logic in the monitoring of reactions to therapeutic drugs. Methods Inf Med 10(04):237–245
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. Wiley
Haider MJ, Rauf A (2014) Sub-lethal effects of diazinon on hematological indices and blood biochemical parameters in Indian carp, Cirrhinus mrigala (Hamilton). Braz Arch Biol Technol 57:947–953
Rambhaskar B, Srinivasa Rao K (1987) Comparative haematology of ten species of marine fish from Visakhapatnam Coast. J Fish Biol 30(1):59–66
Mayer G (1955) A method for the reliable determination of clotting time in whole blood. Can Med Assoc J 72(12):927
Pal GK (2006) Textbook of practical physiology. Vol, 2nd edn. Orient Blackswan, p 456
Lewis SM et al (2006) Dacie and Lewis Practical Haematology, 10th edn. Philadelphia: Churchill Livingstone, p 271
Saha S et al (2021) Chronic effects of Diazinon® exposures using integrated biomarker responses in freshwater walking catfish, Clarias batrachus. Appl Sci 11(22):10902
Blaxhall P, Daisley K (1973) Routine haematological methods for use with fish blood. J Fish Biol 5(6):771–781
Chen H et al (2019) Hematological analysis of Ctenopharyngodon idella, Megalobrama amblycephala and Pelteobagrus fulvidraco: Morphology, ultrastructure, cytochemistry and quantification of peripheral blood cells. Fish Shellfish Immunol 90:376–384
Casanovas P et al (2021) Comparative assessment of blood biochemistry and haematology normal ranges between Chinook salmon (Oncorhynchus tshawytscha) from seawater and freshwater farms. Aquaculture 537:736464
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(1–2):248–254
Ha MS, Cho SH, Kim T (2021) Dietary substitution of fish meal by meat meal: Effects on juvenile olive flounder (Paralichthys olivaceus) growth performance, feed utilization, haematology, biochemical profile and disease resistance against Streptococcus iniae. Aquac Nutr 27(6):1888–1902
Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21(6):1316–1322
Saha S, Chukwuka AV, Mukherjee D, Dhara K, Pal P, Saha NC (2022) Physiological (haematological, growth and endocrine) and biochemical biomarker responses in air-breathing catfish, Clarias batrachus under long-term Captan® pesticide exposures. Environ Toxicol Pharmacol 90:103815
Samanta P et al (2018) Ecological risk assessment of a contaminated stream using multi-level integrated biomarker response in Carassius auratus. Environ Pollut 233:429–438
Odedeyi DO, Odo KE (2017) Acute toxicity and haematology of Clarias gariepinus exposed to selenium. International Journal of Aquaculture 7(9):64–70
Adeogun AO, Ibor OR, Chukwuka AV (2013) Acute toxicity of abattoir and saw-mill effluents to juvenile-sized Clarias gariepinus. Zool Ecol 23(1):53–57
Adeogun AO, Chukwuka AV (2012) Toxicity of industrial wastewater acting singly or in joint-ratios on Clarias gariepinus. Am J Environ Sci 8(4):366–375
Kumar N, Krishnani KK, Singh NP (2018) Comparative study of selenium and selenium nanoparticles with reference to acute toxicity, biochemical attributes, and histopathological response in fish. Environ Sci Pollut Res 25(9):8914–8927
Cardwell R et al (1976) Acute toxicity of selenium dioxide to freshwater fishes. Arch Environ Contam Toxicol 4(1):129–144
Kishore D, Shubhajit S, Chukwuka AV et al (2022) Behavioural toxicity and respiratory distress in early life and adult stage of walking catfish Clarias batrachus (Linnaeus) under acute fluoride exposures. Toxicol Environ Health Sci 14:33–46. https://doi.org/10.1007/s13530-021-00115-4
Saha S, Mukherjee D, Saha NC (2018) Evaluation of acute toxicity and behavioral responses of Heteropneustes fossilis (Linn.) exposed to Captan. Int J Life Sci 6(1):205–208
Singh KA, Williams GH (eds) (2009) Textbook of nephro-endocrinology, 2nd edn. Academic Press, New York, p 584
Nagababu E et al (2008) Iron-deficiency anaemia enhances red blood cell oxidative stress. Free Radic Res 42(9):824–829
Khattab N et al (2021) The efficiency of Sclerophrys regularis as a bioindicator. Egypt Acad J Biol Sci B Zool 13(1):91–101
Modra H, Svobodova Z, Kolářová J (1998) Comparison of differential leukocyte counts in fish of economic and indicator importance. Acta Vet Brno 67(4):215–226
Remyla SR et al (2008) Influence of zinc on cadmium induced haematological and biochemical responses in a freshwater teleost fish Catla catla. Fish Physiol Biochem 34(2):169–174
Kavitha C et al (2010) Toxicological effects of arsenate exposure on hematological, biochemical and liver transaminases activity in an Indian major carp, Catla catla. Food Chem Toxicol 48(10):2848–2854
Witeska M, Kościuk B (2003) The changes in common carp blood after short-term zinc exposure. Environ Sci Pollut Res 10(5):284–286
Ovie K-S, Ikomi U (2011) Alterations in some haematological parameters of the African Snakehead: Parachanna africans exposed to cadmium. Notulae Scientia Biologicae 3(4):29–34
Al-Otaibi A et al (2018) Toxicity bioassay and sub-lethal effects of diazinon on blood profile and histology of liver, gills and kidney of catfish, Clarias gariepinus. Braz J Biol 79:326–336
Shamoushaki MMN et al (2012) Effects of organophosphate, diazinon on some haematological and biochemical changes in Rutilus frisii kutum (Kamensky, 1901) male brood stocks. Iran J Fish Sci 11(1):105–117
Rauf A, Arain N (2013) Acute toxicity of diazinon and its effects on hematological parameters in the Indian carp, Cirrhinus mrigala (Hamilton). Turkish J Vet Anim Sci 37(5):535–540
Khoshbavar-Rostami H, Soltani M, Hassan H (2004) Acute toxicity and some haematological and biochemical changes in giant sturgeon (Huso huso) exposed to diazinon. Bull Eur Assoc Fish Pathol 24(2):92–99
Rather IA et al (2017) The sources of chemical contaminants in food and their health implications. Front Pharmacol 8:830
Javed M, Usmani N (2013) Haematological indices of Channa punctatus as an indicator of heavy metal pollution in waste water aquaculture pond, Panethi, India. Afr J Biotechnol 12(5):520–525
Shah SL, Altindağ A (2005) Alterations in the immunological parameters of Tench (Tinca tinca L. 1758) after acute and chronic exposure to lethal and sublethal treatments with mercury, cadmium and lead. Turk J Vet Anim Sci 29(5):1163–1168
Vosylienė MZ (1999) The effect of heavy metals on haematological indices of fish (survey). Acta Zool Litu 9(2):76–82
Witeska M, Jezierska B, Wolnicki J (2006) Respiratory and hematological response of tench, Tinca tinca (L.) to a short-term cadmium exposure. Aquac Int 14(1):141–152
Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Int Scholar Res Notices 2011:1
Malathi K, Kannathasan A, Rajendran K (2012) Comparative haematological studies on fresh water fishes Channa punctatus and Channa striatus (Bloch). Int J Pharm Chem Biol Sci 2(4):644–648
Hidayati NV et al (2020) Assessment of the ecological and human health risks from metals in shrimp aquaculture environments in Central Java, Indonesia. Environ Sci Pollut Res 27(33):41668–41687
Dhara K et al (2021) Comparative acute toxicity of mercury to air breathing fish, Channa gachua (Ham.) and non-air breathing fish Cyprinus carpio (Linn.): Ethological and Haematological Consideration. Indian J Ecol 48(5):1243–1253
Uyanik F, Eren M, Tunçoku G (2001) Effects of supplemental zinc on growth, serum glucose, cholesterol, enzymes and minerals in broilers. Pak J Biol Sci 4:745–747
Martin P, Prasath D, Arivoli S (2008) Biochemical study of freshwater fish Catla catla with reference to mercury chloride. Iran J Environ Health Sci Eng 5(2):109–116
des Santos Carvalho C, Fernandes MN (2008) Effect of copper on liver key enzymes of anaerobic glucose metabolism from freshwater tropical fish Prochilodus lineatus. Comp Biochem Physiol A Mol Integr Physiol 151(3):437–442
Öner M, Atli G, Canli M (2008) Changes in serum biochemical parameters of freshwater fish Oreochromis niloticus following prolonged metal (Ag, Cd, Cr, Cu, Zn) exposures. Environ Toxicol Chem 27(2):360–366
Cicik B, Engin K (2005) The effects of cadmium on levels of glucose in serum and glycogen reserves in the liver and muscle tissues of Cyprinus carpio (L., 1758). Turk J Vet Anim Sci 29(1):113–117
Mohamed F, Gad N (2008) Environmental pollution-induced biochemical changes in tissues of Tilapia zillii, Solea vulgaris and Mugil capito from Lake Qarun, Egypt. Glob Vet 2(6):327–336
Kumari B et al (2017) Toxicology of arsenic in fish and aquatic systems. Environ Chem Lett 15(1):43–64
Jaheed E (2021) Study of blood serum biochemical profile and pathological changes in haemonchosis experimentally induced in goats. Am J BioSci 9(3):95
Arvind A et al (2019) Lipid and lipoprotein metabolism in liver disease. Feingold KR, Anawalt B, Boyce A et al (eds) MDText.com, Inc., South Dartmouth
Javed M et al (2017) Multiple biomarker responses (serum biochemistry, oxidative stress, genotoxicity and histopathology) in Channa punctatus exposed to heavy metal loaded waste water. Sci Rep 7(1):1–11
Fırat Ö, Kargın F (2010) Individual and combined effects of heavy metals on serum biochemistry of Nile tilapia Oreochromis niloticus. Arch Environ Contam Toxicol 58(1):151–157
Zhang J, Spallholz JE (2009) Toxicity of selenium compounds and nano-selenium particles. General, Applied and Systems Toxicology, p 15
Bunglavan SJ, Garg AK, Dass RS, Shrivastava S (2014) Effect of supplementation of different levels of selenium as nanoparticles/sodium selenite on blood biochemical profile and humoral immunity in male Wistar rats. Vet World 7(12):1075–1081
Desai I, Scott M (1965) Mode of action of selenium in relation to biological activity of tocopherols. Arch Biochem Biophys 110(2):309–315
Lemly AD (1998) Pathology of selenium poisoning in fish. Environmental Chemistry of Selenium. Marcel Dekker, New York, pp 281–296
Lemly AD (1999) Selenium transport and bioaccumulation in aquatic ecosystems: a proposal for water quality criteria based on hydrological units. Ecotoxicol Environ Saf 42(2):150–156
Lugert V, Steinhagen D, Reiser S (2020) Lack of knowledge does not justify a lack of action: the case for animal welfare in farmed fish. J Sustain Organ Agric Syst 70:31–34
Rebl A et al (2017) Microarray-predicted marker genes and molecular pathways indicating crowding stress in rainbow trout (Oncorhynchus mykiss). Aquaculture 473:355–365
Near TJ et al (2013) Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proc Natl Acad Sci 110(31):12738–12743
Schreck CB et al (2016) Biology of stress in fish, 1st edn. Academic Press, p 602
Collins S et al (2016) A comparison of blood gases, biochemistry, and hematology to ecomorphology in a health assessment of pinfish (Lagodon rhomboides). PeerJ 4:e2262
Fazio F et al (2013) Comparative study of the biochemical and haematological parameters of four wild Tyrrhenian fish species. Vet Med 58(11):576–581
Wilson R (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124(1–4):67–80
Dhara K, Saha S, Pal P, Chukwuka AV, Panigrahi AK, Saha NC, Faggio C (2022) Biochemical, physiological (haematological, oxygen-consumption rate) and behavioural effects of mercury exposures on the freshwater snail, Bellamya bengalensis. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 251:109195
Morgado RG et al (2018) Joint effects of chlorpyrifos and mancozeb on the terrestrial isopod Porcellionides pruinosus: a multiple biomarker approach. Environ Toxicol Chem 37(5):1446–1457
Serafim A et al (2012) Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems. Ecol Ind 19:215–225
Pal S et al (2018) Acute toxicity and oxidative stress responses in tadpole of skittering frog, Euphlyctis cyanophlyctis (Schneider, 1799) to Sodium Fluoride Exposure. Bull Environ Contam Toxicol 100(2):202–207
Nayak S, Dash SN, Pati SS, Priyadarshini P, Patnaik L (2021) Lipid peroxidation and antioxidant levels in Anabas testudineus (Bloch) under naphthalene (PAH) stress. Aquac Res 52(11):5739–5749
Presser TS, Sylvester MA, Low WH (1994) Bioaccumulation of selenium from natural geologic sources in western states and its potential consequences. Environ Manag 18(3):423–436
Mason R et al (2000) Factors controlling the bioaccumulation of mercury, methylmercury, arsenic, selenium, and cadmium by freshwater invertebrates and fish. Arch Environ Contam Toxicol 38(3):283–297
Fan TW-M et al (2002) Selenium biotransformations into proteinaceous forms by foodweb organisms of selenium-laden drainage waters in California. Aquat Toxicol 57(1–2):65–84
Debruyn AM, Chapman PM (2007) Selenium toxicity to invertebrates: will proposed thresholds for toxicity to fish and birds also protect their prey? Environ Sci Technol 41(5):1766–1770
Gouget B et al (2005) Resistance, accumulation and transformation of selenium by the cyanobacterium Synechocystis sp. PCC 6803 after exposure to inorganic SeVI or SeIV. Radiochim Acta 93(11):683–689
Liu DL et al (1987) Selenium content of marine food chain organisms from the coast of China. Mar Environ Res 22(2):151–165
Orr PL, Guiguer KR, Russel CK (2006) Food chain transfer of selenium in lentic and lotic habitats of a western Canadian watershed. Ecotoxicol Environ Saf 63(2):175–188
Lemly AD (1996) Assessing the toxic threat of selenium to fish and aquatic birds. Environ Monit Assess 43(1):19–35
Ohlendorf HM, Hothem RL, Welsh D (1989) Nest success, cause-specific nest failure, and hatchability of aquatic birds at selenium-contaminated Kesterson Reservoir and a reference site. Condor 91(4):787–796
Adams WJ et al (2003) Analysis of field and laboratory data to derive selenium toxicity thresholds for birds. Environ Toxicol Chem 22(9):2020–2029
Kuchapski KA (2013) Effects of selenium and other surface coal mine influences on fish and invertebrates in Canadian Rockies streams. University of Lethbridge, Dept. of Biological Sciences, Lethbridge
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The authors are grateful to the Department of Zoology at Barasat Government College and The University of Burdwan for providing lab space and infrastructure for this study. The authors are also grateful to the West Bengal Government’s Directorate of Fisheries for allowing one of the authors (Dr. K. Dhara) to conduct the experiment.
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Conceptualization: SS, KD, and NCS; methodology: SS and KD; software: SS and PP; formal analysis: SS and AVC; investigation, SS and KD; resources, NCS and KD; data curation, SS and AVC; writing—original draft preparation: SS and AVC; writing—review and editing: SS and AVC; supervision: NCS. All authors have read and agreed to the published version of the manuscript.
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Saha, S., Dhara, K., Pal, P. et al. Longer-Term Adverse Effects of Selenate Exposures on Hematological and Serum Biochemical Variables in Air-Breathing Fish Channa punctata (Bloch, 1973) and Non-air Breathing Fish Ctenopharyngodon Idella (Cuvier, 1844): an Integrated Biomarker Response Approach. Biol Trace Elem Res 201, 3497–3512 (2023). https://doi.org/10.1007/s12011-022-03449-3
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DOI: https://doi.org/10.1007/s12011-022-03449-3