Abstract
The effects of fish size and nitrite level on metabolic rate and growth were investigated in the obligate air-breathing snakehead Channa striata, which is an important aquaculture species in Vietnam. Channa striata displayed respiratory size dependence, whereby the standard metabolic rate (SMR) and routine metabolic rate (RMR) decreased progressively in an exponential manner as fish size increased from 50 to 200 g. A mildly elevated nitrite level of 5% of the LC50 96 h (12 mg NO2−/L or safe concentration) induced significant increases in Channa striata SMR and RMR, which were almost double that of the control at the same size. At mild elevation, nitrite caused no significant effect on fish growth and survival during 3 months of rearing. However, both growth and survival rates of fish reared at severely elevated nitrite levels were significantly lower than those of the control; in particular, survival rates were under 50%. While changes in size reduced SMR and RMR, the percentage of air oxygen partitioning remained unchanged. Channa striata upregulation of SMR and RMR and air-breathing regulation were not significantly proven in this study. In summary, maintaining water environments at levels lower than 12 mg NO2−/L with ample oxygenation will not affect the growth and survival rate of snakeheads.
Similar content being viewed by others
References
Affonso EG, Rantin FT (2005) Respiratory responses of the air-breathing fish Hoplosternum littorale to hypoxia and hydrogen sulfide. Comp Biochem Phys C Toxicol Pharmacol 141:275–280. https://doi.org/10.1016/j.cca.2005.07.003
Aggergaard S, Jensen FB (2001) Cardiovascular changes and physiological response during nitrite exposure in rainbow trout. J Fish Biol 59:13–27. https://doi.org/10.1111/j.1095-8649.2001.tb02335.x
Arillo A, Gaino E, Margiocco C, Mensi P, Schenone G (1984) Biochemical and ultrastructural effects of nitrite in rainbow trout: liver hypoxia as the root of the acute toxicity mechanism. Environ Res 34:135–154. https://doi.org/10.1016/0013-9351(84)90083-5
Asifa KP, Viya PV, Chitra KC (2016) Assessment of median lethal concentration (LC50-96h) and behavioral modification of nonylphenol in the cichlid fish, Etroplus maculatus (Bloch, 1795). Int J Adv Lif Sci 9(2):190–195
Boudreaux PJ, Ferrara AM, Fontenot QC (2007) Chloride inhibition of nitrite uptake for non-teleost Actinopterygiian fishes. Comp Biochem Physiol Part A Mol Integr Physiol 147:420–423. https://doi.org/10.1016/j.cbpa.2007.01.016
Boyd CE (2014) Nitrite toxicity affected by species susceptibility, environmental conditions. Glob Aquac Advocate 17:34–36
Bradbury SP, McKim JM, Coats JR (1987) Physiological response of rainbow trout (Salmo gairdneri) to acute fenvalerate intoxication. Pestic Biochem Physiol 27:275–288
Brett J (1965) The relation of size to rate of oxygen consumption and sustained swimming speed of sockeye salmon Oncorhynchus nerka. J Fish Res Board Can 22:1491–1501. https://doi.org/10.1139/f65-128
Cai Y, Summerfelt RC (1992) Effects of temperature and size on oxygen consumption and ammonia excretion by walleye. Aquaculture 104:127–138. https://doi.org/10.1016/0044-8486(92)90143-9
CCREM (1991) Canadian Water Quality Guideline. Canadian Council of Resource and Environmental Ministry, Inland Water Directorate. Environment Canada, Ottawa
Chabot D, Steffensen JF, Farrell A (2016) The determination of standard metabolic rate in fishes. J Fish Biol 88:81–121. https://doi.org/10.1111/jfb.12845
Colt J, Ludwig R, Tchobanoglous G, Cech JJ Jr (1981) The effects of nitrite on the short-term growth and survival of channel catfish, Ictalurus punctatus. Aquaculture 24:111–122. https://doi.org/10.1016/0044-8486(81)90048-X
Duncan WP, de Nazare Paula-Silva M, Almeida-Val VMF (1999) Effects of nitrite on hematology and metabolic parameters of an Amazonian catfish Hoplosternum littorale (Callychthyidae). In: International Congress on the Biology of Fish: Special Adaptations of Tropical Fish (Eds. Nelson J, MacKinlay D.), pp. 29–35. Towson University, Baltimore, MD, United State, July 27–30, 1998. https://repositorio.inpa.gov.br/handle/1/29515
Enders E, Boisclair D, Boily P, Magnan P (2006) Effect of body mass and water temperature on the standard metabolic rate of juvenile yellow perch, Perca flavescens (Mitchill). Environ Biol Fishes 76:399–407. https://doi.org/10.1007/s10641-006-9045-0
Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177. https://doi.org/10.1152/physrev.00050.2003
Frances J, Allan GL, Nowak BF (1998) The effects of nitrite on the short-term growth of silver perch Bidyanus bidyanus. Aquaculture 163:63–72. https://doi.org/10.1016/S0044-8486(98)00219-1
Franklin RK, Loo HS, Osumanu HA (2010) Incorporation of bentazone with Exserohilum rostratum for controlling Cyperus iria. Am J Agri Biol Sci 5:210–214. https://doi.org/10.3844/ajabssp.2010.210.214
Gam LTH, Jensen FB, Damsgaard C, Huong DTT, Phuong NT, Bayley M (2017) Extreme nitrite tolerance in the clown knifefish Chitala ornata is linked to up-regulation of methaemoglobin reductase activity. Aquat Toxicol 187:9–17. https://doi.org/10.1016/j.aquatox.2017.03.013
Graham JB (1997) Air-breathing fishes: evolution, diversity, and adaptation. Academic Press, p 299
Grosell M, Jensen FB (2000) Uptake and effects of nitrite in the marine teleostfish Platichthys flesus. Aquat Toxicol 50:97–107. https://doi.org/10.1016/s0166-445x(99)00091-0
Haya K (1989) Toxicity of pyrethroid insecticides to fish. Environ Toxicol Chem 5:567–576
Huong DTT, Gam LTH, Lek S, Ut VN, Phuong NT (2020) Effects of nitrite at different temperatures on physiological parameters and growth in clown knifefish (Chitala ornata, Gray 1831). Aquaculture 521:735060. https://doi.org/10.1016/j.aquaculture.2020.735060
IJC (International Joint Commission) (1977) New and revised Great lakes water quality objective. Great Lakes Basin. Windsor, IJC, Ottawa
Jensen FB (2003) Nitrite disrupts multiple physiological functions in aquatic animals. Comp Biochem Physiol A Mol Integr Physiol 135:9–24. https://doi.org/10.1016/S1095-6433(02)00323-9
Jensen FB (2007) Nitric oxide formation from nitrite in zebrafish. J Exp Biol 210:3387–3394. https://doi.org/10.1242/jeb.008748
Jensen FB (2009) The dual roles of red blood cells in tissue oxygen delivery: oxygen carriers and regulators of local blood flow. J Exp Biol 212:3387–3393. https://doi.org/10.1242/jeb.023697
Jensen FB, Rohde S (2010) Comparative analysis of nitrite uptake and hemoglobin-nitrite reactions in erythrocytes: sorting out uptake mechanisms and oxygenation dependencies. Am J Physiol Regul 298:R972–R982. https://doi.org/10.1152/ajpregu.00813.2009
Jensen FB, Andersen NA, Heisler N (1987) Effects of nitrite exposure on blood respiratory properties, acid-base and electrolyte regulation in the carp Cyprinus carpio. J Comp Physiol B 157:533–541. https://doi.org/10.1007/BF00700972
Johansen K (1968). Air-breathing fishes. Sci Am, 219: 102–111 https://www.jstor.org/stable/24927540
Kosaka H, Tyuma I (1987) Mechanism of autocatalytic oxidation of oxyhemoglobin by nitrite. Environ Health Perspect 73:147–151. https://doi.org/10.1289/ehp.8773147
Kroupova H, Machova J, Piackova V, Blahova J, Dobsikova R, Novotny L, Svobodova Z (2008) Effects of subchronic nitrite exposure on rainbow trout Oncorhynchus mykiss. Ecotox Environ Safe 71:813–820. https://doi.org/10.1016/j.ecoenv.2008.01.015
Kroupová HK, Valentová O, Svobodová Z, Šauer P, Máchová J (2018) Toxic effects of nitrite on freshwater organisms: a review. Rev Aquac 10:525–542. https://doi.org/10.1111/raq.12184
Kumaraguru AK, Beamish FWH (1983) Bioenergetics of acclimation to permethrin (NRDC-143) by rainbow trout. Comp Biochem Physiol 75:247–252
Lakshmi V, Alam MN (2009) Pollutional effect of a pesticide bayrusil on bimodal oxygen consumption in an air-breathing fish Heteropneustes fossilis (Bloch). Nat Environ Pollut Technol 8(3):529–532
Law on Animal Health, 2015. Vietnam National Assembly, No. 79/2015/QH13 dated on 10/7/2015
Lefevre S, Huong DTT, Wang T, Phuong NT, Bayley M (2011a) Hypoxia tolerance and partitioning of bimodal respiration in the striped catfish Pangasianodon hypophthalmus. Comp Biochem Physiol Part A Mol Integr Physiol 158:207–214. https://doi.org/10.1016/j.cbpa.2010.10.029
Lefevre S, Jensen FB, Huong DTT, Wang T, Phuong NT, Bayley M (2011b) Effects of nitrite exposure on functional haemoglobin levels, bimodal respiration, and swimming performance in the facultative air-breathing fish Pangasianodon hypophthalmus. Aquat Toxicol 104:86–93. https://doi.org/10.1016/j.aquatox.2011.03.019
Lefevre S, Huong DTT, Phuong NT, Wang T, Bayley M (2012a) Effects of hypoxia on the partitioning of oxygen uptake and the rise in metabolism during digestion in the air-breathing fish Channa striata. Aquaculture 364–365:137–142. https://doi.org/10.1016/j.aquaculture.2012.08.019
Lefevre S, Jensen FB, Huong DTT, Wang T, Phuong NT, Bayley M (2012b) Haematological and ion regulatory effects of nitrite in the air-breathing snakehead fish Channa striata. Aquat Toxicol 118–119:48–53. https://doi.org/10.1016/j.aquatox.2012.03.011
Lefevre S, Wang T, Jensen A, Cong NV, Huong DTT, Phuong NT, Bayley M (2014) Air-breathing fishes in aquaculture. What can we learn from physiology? J Fish Biol 84:705–731. https://doi.org/10.1111/jfb.12302
Lefevre S, Findorf I, Bayley M, Huong DTT, Wang T (2016) Increased temperature tolerance of the air-breathing Asian swamp eel Monopterus albus after high-temperature acclimation is not explained by improved cardiorespiratory performance. J Fish Biol 88:418–432. https://doi.org/10.1111/jfb.12696
Lewis WM Jr, Morris DP (1986) Toxicity of nitrite to fish: a review. Trans Am Fish Soc 115:183–195. https://doi.org/10.1577/1548-8659(1986)115%3c183:TONTF%3e2.0.CO;2
Lingaraja T, Venugopalan VK (1978) Pesticide induced Physiological and behavioral changes in an Estuarine teleost Therapon jarbua (Forsk). Fish Technol 15(2):115–119
Logaswamy S, Remia KM (2009) Impact of cypermethrin and ekalux on respiratory and some biochemical activities of a freshwater fish Tilapia mossambica. J Curr Biotica 3(1):65–73
Lokhande MV (2017) Oxygen consumption and behaviour surveillance in the freshwater fish Rasbora daniconius exposed to dimethoate. Int J Fish Aqua Stu 5(2):712–716
Lv X, Xie H, Xia D, Shen C, Luo Y (2018) Mass scaling of the resting and maximum metabolic rates of the black carp. J Comp Physiol B 188:591–598. https://doi.org/10.1007/s00360-018-1154-5
Magesh S, Kumaraguru AK (2006) Acute toxicity of endosulfan to the milkfish, Chanos chanos, of the Southeast Coast of India. Bull Environ Contam Toxicol 76:622–628. https://doi.org/10.1007/s00128-006-0965-3
Maharajan A, Usha R, Ruckmani PSP, Vijaykumar BS, Ganapiriya V, Kumarasamy P (2013) Sublethal effect of profenofos on oxygen consumption and gill histopathology of the Indian major carp, Catla catla (Hamilton). Int J Pure Appl Zool 1(1):196–204
Marigoudar SR, Ahmed RN, David M (2009) Cypermethrin induced respiratory and behavioural responses of the freshwater teleost, Labeo rohita (Hamilton). Veterinarski Arhiv 79(6):583–590
Multappa K, Reddy HRV, Rajesh M, Padmanabha A (2014) Quinalphos induced alteration in respiratory rate and food consumption of freshwater fish Cyprinus carpio. J Env Biol 35(2):395–398
Nwani CD, Nagpure NS, Kumar R, Kushwaha B, Kumar P, Lakra WS (2010) Lethal concentration and toxicity of carbosulfan, glyphosate, and atrazine to freshwater air-breathing fish Channa punctatus (Bloch). Int Aquat Res 2:105–111
Nwani CD, Ama IU, Okoh F, Oji UO, Ogbonyealu RC, Ibiam AA, Ibiam OU (2013a) Acute toxicity of the chloroacetanilide herbicide butachlor and its effects on the behavior of the freshwater Tilapia zillii. Afr J Biotechnol 12(5):499–503. https://doi.org/10.5897/AJB122433
Nwani CD, Ibiam UA, Ibiam OU, Nworie O, Onyishi G, Atama C (2013b) Investigation on acute toxicity and behavioral changes in Tilapia zillii due to glyphosate-based herbicide, forceup. J Anim Plant Sci 23(3):888–892
Patil VK, David M (2008) Behaviour and respiratory dysfunction as an index of malathion toxicity in the freshwater fish, Labeo rohita (Hamilton). Tuk J Fish Aqua Sci 8:233–237
Perrone SJ, Meade TL (1977) Protective effect of chloride on nitrite toxicity to coho salmon (Oncorhynchus kisutch). J Fish Res Board Can 34:486–492. https://doi.org/10.1139/f77-079
Rahman Q, Sadhu DN (2009) Effects of pesticides on aquatic and aerial oxygen consumption in an air-breathing murrel fish Channa gachua. Nat Environ Pollut Technol 8(3):603–608
Saoud PI, Naamani S, Ghanawi J (2014) Effects of acute and chronic nitrite exposure on rabbitfish Siganus rivulatus growth, hematological parameters, and gill histology. J Aquac Res Development 5(6):263–272. https://doi.org/10.4172/2155-9546100063
Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment, 5th edn. Cambridge University Press, p 607
Siikavuopio SI, Sæther BS (2006) Effects of chronic nitrite exposure on growth in juvenile Atlantic cod, Gadus morhua. Aquaculture 255:351–356. https://doi.org/10.1016/j.aquaculture.2005.11.058
Somdare PO, Nwani CD, Nwadinigwe AO, Nwani JC, Odo GE, Ugbor ON, Ukonze JA, Ezeibe ABCA (2015) Fenthion induced toxicity and histopathological changes in gill tissue of freshwater African catfish, Clarias gariepinus (Burchell, 1822). Afr J Biotechnol 14(25):2103–2113. https://doi.org/10.5897/AJB2015.14696
Stormer J, Jensen FB, Rankin JC (1996) Uptake of nitrite, nitrate, and bromide in rainbow trout Oncorhynchus mykiss: Effects on ionic balance. Can J Fish Aquat Sci 53:1943–1950. https://doi.org/10.1139/f96-142
Subramanian MA (2004) Toxicology. MJP Publishers, Chennai
Tiwari M, Nagpure NS, Saksena DN, Kumar R, Singh SP, Kushwaha B, Lakra WS (2011) Evaluation of acute toxicity levels and ethological responses under heavy metal cadmium exposure in freshwater teleost, Channa punctata (Bloch). Int J Aqu Sci 2(1):36–47
Tomasso J (1994) Toxicity of nitrogenous wastes to aquaculture animals. Rev Fish Sci Aquac 2:291–314. https://doi.org/10.1080/10641269409388560
Tuong DD, Ngoc TB, Huynh VTN, Huong DTT, Phuong NT, Hai TN, Wang T, Bayley M (2018) Clown knifefish Chitala ornata oxygen uptake and its partitioning in present and future temperature environments. Comp Biochem Physiol Part A Mol Integr Physiol 216:52–59. https://doi.org/10.1016/j.cbpa.2017.11.018
Vleeming W, Van De Kuil A, te Biesebeek JD, Meulenbelt J, Boink ABTJ (1997) Effect of nitrite on blood pressure in anaesthetized and free-moving rats. Food Chem Toxicol 35:615–619. https://doi.org/10.1016/S0278-6915(97)00015-X
Voslárová E, Pistekova V, Svobodova Z, Bedanova I (2008) Nitrite toxicity to Danio rerio: Effects of subchronic exposure on fish growth. Acta Vet Brno 77:455–460. https://doi.org/10.2754/avb200877030455
Yager TK, Summerfelt RC (1993) Effects of fish size and feeding frequency on metabolism of juvenile walleye. Aquacult Eng 12:19–36. https://doi.org/10.1016/0144-8609(93)90024-6
Zhang Y, Huang Q, Liu S, He D, Wei G, Luo Y (2014) Intraspecific mass scaling of metabolic rates in grass carp Ctenopharyngodon idellus. J Comp Physiol B 184:347–354. https://doi.org/10.1007/s00360-014-0802-7
Acknowledgements
This study was funded in part by the Can Tho University Improvement Project VN14-P6, supported by a Japanese ODA loan.
Author information
Authors and Affiliations
Corresponding author
Additional information
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
Phu, T.Q., Hang, B.T.B., Tuong, D.D. et al. Effects of size and nitrite exposure on respiration, oxygen partitioning, and growth of obligate air-breathing fish Channa striata. Fish Sci 88, 149–159 (2022). https://doi.org/10.1007/s12562-021-01562-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-021-01562-1