Abstract
This study aimed to evaluate hematological, biochemical, and gasometric parameters of tambaqui juveniles (Colossoma macropomum) exposed to hypoxia and subsequent recovery. Six animals were subjected to normoxia (basal) treatment with dissolved oxygen (DO) 6.27 ± 0.42 mg L−1. Water flow and aeration were reduced for 3 days (hypoxia), during which DO was 0.92 ± 0.37 mg L−1. Water flow and aeration were then reestablished with DO remaining similar to basal. The treatments were as follows: normoxia (basal); 24 h after initiating hypoxia (24H); 72 h after initiating hypoxia (72H); 24 h after reestablishing normoxia (24R); 48 h after reestablishing normoxia (48R); and 96 after reestablishing normoxia (96R). The highest glucose level was recorded at 24H (P < 0.05); the highest lactate level was at 72R; and the highest blood pH was at 24H and 72H (P < 0.05). The highest concentration of PvCO2 was at 24H (P < 0.05), while at 96R it was equivalent to basal (P > 0.05). The variable PvO2 was only higher than basal at 24R (P < 0.05). Juvenile C. macropomum managed to reestablish the main stress indicators (glucose and lactate) at 96R, while the other indicators varied during the study, with homeostatic physiology being reestablished during the recovery period.
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References
Abdel-Tawwab M, Monier MN, Hoseinifar SH, Faggio C (2019) Fish response to hypoxia stress: growth, physiological, and immunological biomarkers. Fish Physiol Biochem:1–17. https://doi.org/10.1007/s10695-019-00614-9
Affonso EG, Polez VLP, Correa CF, Mazon AF, Araujo MRR, Moraes G, Rantin FT (2002) Blood parameters and metabolites in the teleost fish Colossoma macropomum exposed to sulfide or hypoxia. Comp Biochem Physiol C Toxicol Pharmacol 133:375–382. https://doi.org/10.1016/S1532-0456(02)00127-8
Almeida-Val VMF, Val AL, Hochachka PW (1993) Hypoxia tolerance in Amazonfishes: status of an under-explored biological “goldmine”. In Surviving Hypoxia: Mechanisms of Control and Adaptation (Hochachka PW, Lutz PL, Sick T, Rosenthal M, van den Thillart G eds) 435 – 445. Boca Raton, FL: CRC Press.
Araújo-Luna R, Ribeiro L, Bergheim A, Pousão-Ferreira P (2018) The impact of different rearing condition on gilthead seabream welfare: dissolved oxygen levels and stocking densities. Aquac Res 49:3845–3855. https://doi.org/10.1111/are.13851
Ashley PJ (2007) Fish welfare: current issues in aquaculture. Appl Anim Behav Sci 104:199–235. https://doi.org/10.1016/j.applanim.2006.09.001
Bacca H, Huvet A, Fabioux C, Daniel JY, Delaporte M, Pouvreau S, Van Wormhoudt A, Moal J (2005) Molecular cloning and seasonal expression of oyster glycogen phosphorylase and glycogen synthase genes. Comp Biochem Physiol B Biochem Mol Biol 140:635–646. https://doi.org/10.1016/j.cbpc.2005.01.005
Baldissera MD, Souza CF, Boaventura TP, Nakayama CL, Baldisserotto B, Luz RK (2018) Purinergic signaling as a potential target of hypoxia stress-induced impairment of the immune system in freshwater catfish Lophiosilurus alexandri. Aquaculture 496:197–202. https://doi.org/10.1016/j.aquaculture.2018.07.025
Baldisserotto B (2003). Osmoregulatory adaptations of freshwater teleosts. 179-201. In: Val AL, BG Kapoor (Eds.). Fish Adaptations. Enfield, Science Publishers, 418p.
Baptista RB, Souza-Castro N, Almeida-Val VMF (2016) Acute hypoxia up-regulates HIF-1α and VEGF mRNA levels in Amazon hypoxia-tolerant Oscar (Astronotus ocellatus). Fish Physiol Biochem 42:1307–1318. https://doi.org/10.1007/s10695-016-0219-1
Bartrons R, Caro J (2007) Hypoxia, glucose metabolism and the Warburg’s effect. J Bioenerg Biomembr 39:223–229. https://doi.org/10.1007/s10863-007-9080-3
Becker AG, Luz RK, Mattioli CC, Nakayama CL, Silva WDS, Leme FDOP, Mendes HCPM, Heinzmann BM, Baldisserotto B (2017) Can the essential oil of Aloysia triphylla have anesthetic effect and improve the physiological parameters of the carnivorous freshwater catfish Lophiosilurus alexandri after transport? Aquaculture 481:184–190. https://doi.org/10.1016/j.aquaculture.2017.09.007
Benfey TJ, Biron M (2000) Acute stress response in triploid rainbow trout (Oncorhynchus mykiss) and brook trout (Salvelinus fontinalis). Aquaculture 184:167–176. https://doi.org/10.1016/S0044-8486(99)00314-2
Bernier NJ, Gorissen M, Flik G (2012) Differential effects of chronic hypoxia and feed restriction on the expression of leptin and its receptor, food intake regulation and the endocrine stress response in common carp. J Exp Biol 215:2273–2282. https://doi.org/10.1242/jeb.066183
Bie M, Marcon J, van den Thillart G, Almeida-Val V (1998) Hypoxia tolerance of Amazon fish: respirometry and energy metabolism of the cichlid Astronotus ocellatus. Comp Biochem Physiol A Mol Integr Physiol 120:151–156. https://doi.org/10.1016/S1095-6433(98)10023-5
Brauner CJ, Thorarensen H, Gallaugher P, Farrell AP, Randall DJ (2000) CO2 transport and excretion in rainbow trout (Oncorhynchus mykiss) during graded sustained exercise. Respir Physiol 119:69–82. https://doi.org/10.1016/s0034-5687(99)00091-2
Caldwell CA, Hinshaw J (1994) Physiological and haematological responses in rainbow trout subjected to supplemental dissolved oxygen in fish culture. Aquaculture 126:183–193. https://doi.org/10.1016/0044-8486(94)90259-3
Carvalho CS, Fernandes MN (2006) Effect of temperature on copper toxicity and hematological responses in the neotropical fish Prochilodus scrofa at low and high pH. Aquaculture 251:109–117. https://doi.org/10.1016/j.aquaculture.2005.05.018
Chagas EC, Val AL (2006) Ascorbic acid reduces the effects of hypoxia on the Amazon fish Tambaqui. J Fish Biol 69:608–612. https://doi.org/10.1111/j.1095-8649.2006.01094.x
Cook DG, Herbert NA (2012) The physiological and behavioural response of juvenile kingfish (Seriola lalandi) differs between escapable and inescapable progressive hypoxia. J Exp Mar Biol Ecol 413:138–144. https://doi.org/10.1016/j.jembe.2011.12.006
Das PC, Ayyappan S, Jena JK (2006) Haematological changes in the three Indian major carps, Catla catla (Hamilton), Labeo rohita (Hamilton) and Cirrhinus mrigala (Hamilton) exposed to acidic and alkaline water pH. Aquaculture 256:80–87. https://doi.org/10.1016/j.aquaculture.2006.02.019
Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Bio 33:245–303
Douxfils J, Deprez M, Mandiki SNM, Milla S, Henrotte E, Mathieu C, Silvestre F, Vandecan M, Rougeot C, Mélard C, Dieu M, Raes M, Kestemont P (2012) Physiologic al and proteomic responses to single and repeated hypoxia in juvenile Eurasian perch under domestication- clues to physiological acclimation and humoral immune modulations. Fish Shellfish Immunol 33:1112–1122
Duncan WLP (1998). Estresse metabólico e dano celular em Colossoma macropomum e Hoplosternum litoralle exposto ao petróleo. Dissertação de Mestrado, Instituto Nacional de Pesquisas da Amazônia (INPA), 117 p.
Fitzgibbon QP, Strawbridge A, Seymour RS (2007) Metabolic scope, swimming performance and the effects of hypoxia in the mulloway, Argyrosomus japonicus (Pisces: Sciaenidae). Aquaculture 270:358–368. https://doi.org/10.1016/j.aquaculture.2007.04.038
Florindo LH, Leite CA, Kalinin AL, Reid SG, Milsom WK, Rantin FT (2006, 209) The role of branchial and orobranchial O2 chemoreceptors in the control of aquatic surface respiration in the neotropical fish Tambaqui (Colossoma macropomum): progressive responses to prolonged hypoxia. J Exp Biol:1709–1715. https://doi.org/10.1242/jeb.02199
Gaylord TG, Teague AM, Barrows FT (2006) Taurine supplementation of all-plant protein diets for rainbow trout (Oncorhynchus mykiss). J World Aquacult Soc 37:509–517. https://doi.org/10.1111/j.1749-7345.2006.00064.x
Genz J, Jyde MB, Svendsen JC, Steffensen JF, Ramløv H (2013) Excess post-hypoxic oxygen consumption is independent from lactate accumulation in two cyprinid fishes. Comp Biochem Physiol A Mol Integr Physiol 165:54–60. https://doi.org/10.1016/j.cbpa.2013.02.002
Gomes DP, Chaves BW, Becker AG, Baldisserotto B (2011) Water parameters affect anaesthesia induced by eugenol in silver catfish, Rhamdia quelen. Aquac Res 42:878–886. https://doi.org/10.1111/j.1365-2109.2011.02864.x
Hwang PP, Lee TH, Lin LY (2011) Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp 301:28–47. https://doi.org/10.1152/ajpregu.00047.2011
Jung SH, Sim DS, Park MS, Jo Q, Kim Y (2003) Effects of formalin on haematological and blood chemistry in olive flounder, Paralichthys olivaceus (Temminck et Schlegel). Aquac Res 34:1269–1275. https://doi.org/10.1046/j.1365-2109.2003.00936.x
Li M, Wang X, Qi C, Li E, Du Z, Qin JG, Chen L (2018) Metabolic response of Nile tilapia (Oreochromis niloticus) to acute and chronic hypoxia stress. Aquaculture 495:187–195. https://doi.org/10.1016/j.aquaculture.2018.05.031
Long Y, Yan J, Song G, Li X, Li X, Li Q, Cui Z (2015) Transcriptional events co-regulated by hypoxia and cold stresses in Zebrafish larvae. BMC Genomics 16:385. https://doi.org/10.1186/s12864-015-1560-y
Mattioli CC, Takata R, FDOP L, Costa DC, Luz RK (2019a) Response of juvenile Lophiosilurus alexandri to osmotic and thermic shock. Fish Physiol Biochem 46:51–61. https://doi.org/10.1007/s10695-019-00696-5
Mattioli CC, Takata R, Leme FDOP, Costa DC, Luz RK (2019b) Physiological and metabolic responses of juvenile Lophiosilurus alexandri catfish to air exposure. Fish Physiol Biochem 45:455–467. https://doi.org/10.1007/s10695-018-0576-z
McDonald G, Milligan L (1997) Ionic, osmotic and acid-base regulation in stress. Fish Stress Health Aquacult 62:119–145
Messina M, Piccolo G, Tulli F, Messina CM, Cardinaletti G, Tibaldi E (2013) Lipid composition and metabolism of European sea bass (Dicentrarchus labrax L.) fed diets containing wheat gluten and legume meals as substitutes for fish meal. Aquaculture 376:6–14. https://doi.org/10.1016/j.aquaculture.2012.11.005
Moreira AG, Coelho AA, Albuquerque LF, Moreira RT, Farias WR (2015) Efeito do eugenol como agente mitigador do estresse no transporte de juvenis de tilápia do Nilo. Pesqui Vet Bras 35:893–898. https://doi.org/10.1590/S0100-736X2015001100004
Muusze B, Marcon J, van den Thillart G, Almeida-Val V (1998) Hypoxia tolerance of Amazon fish: respirometry and energy metabolism of the cichlid Astronotus ocellatus. Comp Biochem Physiol A Mol Integr Physiol 120:151–156. https://doi.org/10.1016/S1095-6433(98)10023-5
Nelson DL, Cox MM (2014) Princípios de bioquímica de Lehninger, 6th edn. Artmed, Porto Alegre, p 2014
Nguyen THP, Mather PB, Hurwood DA (2017) Effects of sub lethal salinity and temperature levels and their interaction on growth performance and hematological and hormonal levels in tra catfish (Pangasianodon hypophthalmus). Aquac Int 25:1057–1071. https://doi.org/10.1007/s10499-016-0097-7
Ni M, Wen H, Li J, Chi M, Bu Y, Ren Y, Zhang M, Song Z, Ding H (2014) The physiological performance and immune responses of juvenile Amur sturgeon (Acipenser schrenckii) to stocking density and hypoxia stress. Fish Shellfish Immunol 36:325–335. https://doi.org/10.1016/j.fsi.2013.12.002
Ortuno J, Esteban MA, Meseguer J (2001) Effects of short-term crowding stress on the gilthead seabream (Sparus aurata L.) innate immune response. Fish Shellfish Immunol 11:187–197. https://doi.org/10.1006/fsim.2000.0304
Pavlidis M, Futter WC, Katharios P, Divanach P (2007) Blood cell profile of six Mediterranean mariculture fish species. J Appl Ichthyol 23:70–73. https://doi.org/10.1111/j.1439-0426.2006.00771.x
Payne AH, Hales DB (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25:947–970. https://doi.org/10.1210/er.2003-0030
Rantin FT, Kalinin AL (2004) Cardiorespiratory function and aquatic surface respiration in Colossoma macropomum exposed to graded and acute hypoxia. In: Val AL, de Almeida-Val VMF, Randall DJ (eds) Physiology and biochemistry of the fishes of the Amazon. INPA, Manaus, pp 169–180
Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol 214:191–199. https://doi.org/10.1242/jeb.047951
Robertson LM, Val AL, Almeida-Val VF, Wood CM (2015) Ionoregulatory aspects of the osmorespiratory compromise during acute environmental hypoxia in 12 tropical and temperate teleosts. Physiol Biochem Zool 88:357–370. https://doi.org/10.1086/681265
Saint-Paul U (1984) Physiological adaptation to hypoxia of a neotropical characoid fish Colossoma macropomum, Serrasalmidae. Environ Biol Fishes 11:53–62. https://doi.org/10.1007/BF00001845
Segner H, Sundh H, Buchmann K, Douxfils J, Sundell KS, Mathieu C, Ruane N, Jutfelt F, Toften H, Vaughan L (2012) Health of farmed fish: its relation to fish welfare and its utility as welfare indicator. Fish Physiol Biochem 38:85–105
Shahsavani D, Mohri M, Kanani HG (2010) Determination of normal values of some blood serum enzymes in Acipenser stellatus Pallas. Fish Physiol Biochem 36:39–43. https://doi.org/10.1007/s10695-008-9277-3
Silva RD, Rocha LO, Fortes BDA, Vieira D, Fioravanti MCS (2012) Parâmetros hematológicos e bioquímicos da tilápia-do-Nilo (Oreochromis niloticus L.) sob estresse por exposição ao ar. Pesqui Vet Bras 32:99–107. https://doi.org/10.1590/S0100-736X2012001300017
de Souza ADSL, Peret AC, Hamoy M, de Souza RAL, Torres MF, Barbas LAL (2019) Propofol and essential oil of Nepeta cataria induce anaesthesia and marked myorelaxation in tambaqui Colossoma macropomum: implications on cardiorespiratory responses. Aquaculture 500:160–169
Speers-Roesch B, Sandblom E, Lau GY, Farrell AP, Richards JG (2009) Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia. Am J Physiol Regul Integr Comp 298:104–119. https://doi.org/10.1152/ajpregu.00418.2009
Sundin L, Reid SG, Rantin FT, Milsom WK (2000) Branchial receptors and cardiorespiratory reflexes in a neotropical fish, the tambaqui (Colossoma macropomum). J Exp Biol 203:1225–1239
Thrall MA, Baker DC, Campbell TW, DeNicola D, Fettman MJ, Lassen ED, Rebar A, Weiser G (2015) Hematologia e Bioquímica Clínica Veterinária, 2nd edn. GUANABARA Koogan, Rio de Janeiro, pp 529–537
Tolussi CE, Hilsdorf AWS, Caneppele D, Moreira RG (2010) The effects of stocking density in physiological parameters and growth of the endangered teleost species piabanha, Brycon insignis (Steindachner, 1877). Aquaculture 310:221–228. https://doi.org/10.1016/j.aquaculture.2010.10.007
Val AL (1996) Surviving low oxygen levels: lessons from fishes of the Amazon. Physiol Trop Fish 21:59–73 Academic Press;1ª edition
Val AL, Gomes KRM, Almeida-Val VMF (2015) Rapid regulation of blood parameters under acute hypoxia in the Amazonian fish Prochilodus nigricans. Comp Biochem Physiol A Mol Integr Physiol 184:125–131. https://doi.org/10.1016/j.cbpa.2015.02.020
Voet D, Voet JG (2013) Metabolismo dos aminoácidos. In: Voet D, Voet JG (eds) Bioquímica, 4° edn. Artmed, Porto Alegre – RS, pp 1019–1087
Wang J, Lu DQ, Jiang B, Luo HL, Lu GL, Li AX (2018) The effect of intermittent hypoxia under different temperature on the immunomodulation in Streptococcus agalactiae vaccinated Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 79:181–192. https://doi.org/10.1016/j.fsi.2018.04.040
Weber RE (1996). Hemoglobin adaptations in Amazonian and temperate fish with special reference to hypoxia, allosteric effectors and functional heterogeneity. In AL Val, VM Almeida-Val, DJ Randall (eds), Physiology and Biochemistry of the Fishes of the Amazon. I.N.P.A., Manaus, Brazil,75-90.
Welker TL, MCnulty ST, Klesius PH (2007) Effect of sublethal hypoxia on the immune response and susceptibility of channel catfish, Ictalurus punctatus, to enteric septicemia. J World Aquacult Soc 38:12–23. https://doi.org/10.1111/j.1749-7345.2006.00069.x
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625
Wilson RW, Wood CM, Gonzalez R, Patrick ML, Bergman HL, Narahara AB, Val AL (1999) Ion and acid-base balance in three species of Amazonian fish during gradual acidification of extremely soft water. Physiol Biochem Zool 72:277–285. https://doi.org/10.1086/316672
Wood CM, Wilson RW, Gonzalez RJ, Patrick ML, Bergman HL, Narahara A, Val AL (1998) Responses of an Amazonian teleost, the tambaqui (Colossoma macropomum) to low pH in extremely soft water. Physiol Zool 71:658–670. https://doi.org/10.1086/515977
Wood CM, De Souza Netto JG, Wilson JM, Duarte RM, Val AL (2017) Nitrogen metabolism in tambaqui (Colossoma macropomum), a neotropical model teleost: hypoxia, temperature, exercise, feeding, fasting, and high environmental ammonia. J Comp Physiol B 187:135–151. https://doi.org/10.1007/s00360-016-1027-8
Wood CM, Gonzalez RJ, Ferreira MS, Braz-Mota S, Val AL (2018) The physiology of the Tambaqui (Colossoma macropomum) at pH 8.0. J Comp Physiol B 188:393–408. https://doi.org/10.1007/s00360-017-1137-y
Xiao W (2015) The hypoxia signaling pathway and hypoxic adaptation in fishes. Sci China Life Sci 58:148–155. https://doi.org/10.1007/s11427-015-4801-z
Yang S, Yan T, Wu H, Xiao Q, Fu HM, Luo J, Zhou J, Zhao LL, Wang Y, Yang SY, Sun JL, Ye X, Li SJ (2017) Acute hypoxic stress: effect on blood parameters, antioxidant enzymes, and expression of HIF-1alpha and GLUT-1 genes in largemouth bass (Micropterus salmoides). Fish Shellfish Immunol 67:449–458. https://doi.org/10.1016/j.fsi.2017.06.035
Funding
The present research was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brazil), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-Brazil - Procad 88887.200588/2018-00), and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG-Brazil). R.K. LUZ received a research grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq No. 308547/2018-7).
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The experiment was carried out at Laboratório de Aquacultura of Universidade Federal de Minas Gerais (LAQUA), Brazil, and was approved by the Comitê de Ética em Uso de Animais (Ethics Committee on Animal Use) of UFMG (protocol 296/2019).
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do Carmo Neves, L., Favero, G.C., Beier, S.L. et al. Physiological and metabolic responses in juvenile Colossoma macropomum exposed to hypoxia. Fish Physiol Biochem 46, 2157–2167 (2020). https://doi.org/10.1007/s10695-020-00868-8
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DOI: https://doi.org/10.1007/s10695-020-00868-8
Keywords
- Hypoxic stress
- Stress physiology
- Native fish
- Tambaqui