Abstract
The present study aimed to evaluate the physiological and metabolic stress responses of juvenile Lophiosilurus alexandri submitted to an air exposure test. The subjects consisted of 72 juveniles. Blood samples were taken at: 0 h—fish not exposed to air; 0.5 h—fish shortly after exposure to air for 30 min (prior to returning to the tank); 1.5 h (90 min), 24, 48, and 96 h after the initiation of exposure to air for 30 min. After 96 h, survivorship was 100%. Cortisol and glucose levels were higher at 0.5 h, returning to baseline at 48 and 24 h, respectively. Lactate dehydrogenase levels were highest at 1.5 h after exposure to air, returning to normal values in 24 h. Several changes were recorded in gasometric blood values and electrolytes. With regard to hematology and blood chemistry, exposure to air did not affect globular volume and AST throughout the 96 h of the experiment. The values for alkaline phosphatase were highest at 0, 1.5, and 24 h. Total protein was similar between 0 and 1.5 h and lowest at 96 h, while ALT was highest at 0.5 h. Leukocytes were highest at 0.5, 1.5, 48, and 96 h, while erythrocytes were highest at 96 h. After 96 h, juvenile L. alexandri were able to reestablish the main indicators of stress (cortisol, glucose and lactate dehydrogenase), while other indicators (hematological, biochemical, and gasometric) exhibited compensatory variation for normal physiological re-establishment.
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References
Abreu JS, Takahashi LS, Hoshiba MA, Urbinati EC (2009) Biological indicators of stress in pacu (Piaractus mesopotamicus) after capture. Braz J Biol 69:415–421. https://doi.org/10.1590/S1519-69842009000200026
Adamante WB, Nuñer APO, Barcellos LJG, Soso AB, Finco JA (2008) Stress in Salminus brasiliensis fingerlings due to different densities and times of transportation. Arq Bras Med Vet Zootec 60:755–761. https://doi.org/10.1590/S0102-09352008000300034
Apha (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Works Association, Water Environmental Federation, Washington
Arends RJ, Mancera JM, Munõz JL, Wendelaar-Bonga SE, Flik G (1999) The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J Endocrinol 163:149–157. https://doi.org/10.1677/joe.0.1630149
Baker MR, Gobush KS, Vynne CH (2013) Review of factors influencing stress hormones in fish and wildlife. J Nat Conserv 21:309–318. https://doi.org/10.1016/j.jnc.2013.03.003
Baldisserotto B, Martos-Sitcha JA, Menezes CC, Toni C, Prati RL, Garcia LO, Salbego J, Mancera JM, Martínez-Rodríguez G (2014) The effects of ammonia and water hardness on the hormonal, osmoregulatory and metabolic responses of the freshwater silver catfish Rhamdia quelen. Aquat Toxicol 152:341–352. https://doi.org/10.1016/j.aquatox.2014.04.023
Barcellos LJG, Marqueze A, Trapp M, Quevedo RM, Ferreira D (2010) These effects of fasting on cortisol, blood glucose and liver and muscle glycogen in adult jundiá Rhamdia quelen. Aquaculture 300:231–236. https://doi.org/10.1016/j.aquaculture.2010.01.013
Barton BA (2000) Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. N Am J Aquac 62:12–18. https://doi.org/10.1577/1548-8454(2000)062<0012:SFDITC>2.0.CO;2
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525. https://doi.org/10.1093/icb/42.3.517
Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the responses and effects of corticosteroids. Annu Rev Fish Dis 1:3–26. https://doi.org/10.1016/0959-8030(91)90019-G
Becker AG, Luz RK, Mattioli CC, Nakayama CL, Silva WS, Leme FOP, 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
Begg K, Pankhurst NW (2004) Endocrine and metabolic responses to stress in a laboratory population of the tropical damselfish Acanthochromis polyacanthus. J Fish Biol 64:133–145. https://doi.org/10.1111/j.1095-8649.2004.00290.x
Bezerra RF, Soares MCF, Santos AJG, Carvalho EVMM, Coelho LCBB (2014) Seasonality influence on biochemical and hematological indicators of stress and growth of pirarucu (Arapaima gigas), an Amazonian air-breathing fish. Sci World J 2014:1–6. https://doi.org/10.1155/2014/541278
Brauner CJ, Thorarensen H, Gallaugher P, Farrell AP, Randall DJ (2000) CO2 transport and excretion in rainbow trout (Oncorhynchus mykiss) during graded sustained exercise. Resp Physiol 119:69–82. https://doi.org/10.1016/S0034-5687(99)00091-2
Buttle LG, Uglow RF, Coax IN (1996) The effect of emersion and handling on the nitrogen excretion rates of Clarias gariepinus. J Fish Biol 49:693–701. https://doi.org/10.1111/j.1095-8649.1996.tb00065.x
Chen YH, Chen HH, Jeng SS (2015) Rapid renewal of red blood cells in the common carp following prolonged exposure to air. Fish Sci 81:255–265. https://doi.org/10.1007/s12562-014-0836-5
Cnaani A, Mclean E (2009) Time-course response of cobia (Rachycentron canadum) to acute stress. Aquaculture 289:140–142. https://doi.org/10.1016/j.aquaculture.2008.12.016
Cordeiro NIS, Costa DC, Silva WS, Takata R, Miranda-Filho KC, Luz RK (2016) High stocking density during larviculture and effect of size and diet on production of juvenile Lophiosilurus alexandri Steindachner, 1876 (Siluriformes: Pseudopimelodidae). J Appl Ichthyol 32:61–66. https://doi.org/10.1111/jai.12963
Costa DC, Silva WS, Melillo-Filho R, Miranda-Filho KC, Santos JCE, Luz RK (2015) Capture, adaptation and artificial control of reproduction of Lophiosilurus alexandri: a carnivorous freshwater species. Anim Reprod Sci 159:148–154. https://doi.org/10.1016/j.anireprosci.2015.06.009
Da-Costa DP, Leme FOP, Takata R, Costa DC, Silva WS, Melillo-Filho R, Alves GM, Luz RK (2016) Effects of temperature on growth, survival and physiological parameters in juveniles of a carnivorous neotropical catfish. Aquac Res 47:1706–1715. https://doi.org/10.1111/are.12594
Damsgaard C, Gam LTH, Tuong DD, Thinh PV, Huong-Thanh DT, Wang T, Bayley M (2015a) High capacity for extracellular acid-base regulation in the air-breathing fish Pangasianodon hypophthalmus. J Exp Biol 218:1290–1294. https://doi.org/10.1152/ajpregu.00470.2014
Damsgaard C, Phuong LM, Huong DTT, Jensen FB, Wang T, Bayley M (2015b) High affinity and temperature sensitivity of blood oxygen binding in Pangasianodon hypophthalmus due to lack of chloride-hemoglobin allosteric interaction. Am J Physiol Regul Integr Comp Physiol 308:907–915. https://doi.org/10.1152/ajpregu.00470.2014
Diniz NM, Honorato CA (2012) Algumas alternativas para diminuir os efeitos do estresse em peixes de cultivo—Revisão. Arq Ciênc Vet Zool UNIPAR 15:149–154. https://doi.org/10.25110/arqvet.v15i2.2012.4219
Farrell AP, Stecyk JAW (2007) The heart as a working model to explore themes and strategies for anoxic survival in ectothermic vertebrates. Comp Biochem Physiol A 147:300–312. https://doi.org/10.1016/j.cbpa.2007.01.021
Ferguson RA, Tufts BL (1992) Physiological effects of brief air exposure in exhaustively exercised rainbow trout (Onchorhynchus mykiss): implications for catch-and-release fisheries. Can J Fish Aquat Sci 49:1157–1162. https://doi.org/10.1139/f92-129
Figueiredo RACR, Souza RC, Bezerra KS, Campeche DFB, Campos RML, Souza AM, Melo JFB (2014) Relação proteína/carboidrato no desempenho e metabolismo de juvenis de pacamã (Lophiosilurus alexandri). Arq Bras Med Vet Zootec 66:1567–1576. https://doi.org/10.1590/1678-6454
Flodmark LEW, Urke HA, Halleraker JH, Arnekleiv JV, Vøllestad LA, Poléo ABS (2002) Cortisol and glucose responses in juvenile brown trout subjected to a fluctuating flow regime in an artificial stream. J Fish Biol 60:238–248. https://doi.org/10.1111/j.1095-8649.2002.tb02401.x
Gholipourkanani H, Ahadizadeh S (2013) Use of propofol as an anesthetic and its efficacy on some hematological values of ornamental fish Carassius auratus. SpringerPlus 76:1–5. https://doi.org/10.1186/2193-1801-2-76
Gomes DP, Chaves BW, Becker AG, Baldisserotto B (2011) Water parameters affect anesthesia induced by eugenol in silver catfish, Rhamdia quelen. Aquac Res 42:878–886. https://doi.org/10.1111/j.1365-2109.2011.02864.x
Grundy D (2015) Principles and standards for reporting animal experiments in the journal of physiology and experimental physiology. J Physiol 100:755–758. https://doi.org/10.1113/JP270818
Hala D, Petersen LH, Martinovic D, Huggett DB (2012) Constraints-based stoichiometric analysis of hypoxic stress on steroidogenesis in fathead minnows, Pimephales promelas. J Exp Biol 215:1753–1765. https://doi.org/10.1242/jeb.066027
Houston AH, Murad A (1995) Erythrodynamics in fish: recovery of the goldfish Carassius auratus from acute anemia. Can J Zool 73:411–418. https://doi.org/10.1139/z95-046
Inoue LAKA, Moraes G, Iwama GK, Afonso LOB (2008) Physiological stress responses in the warm-water fish matrinxã (Brycon amazonicus) subjected to a sudden cold shock. Acta Amaz 38:603–609. https://doi.org/10.1590/S0044-59672008000400002
Jain NC (1986) Schalm's veterinary hematology, 4th edn. Lea & Febiger, Philadelphia, p 1221
Joyce W, Gesser H, Bayley M, Wang T (2015) Anoxia and acidosis tolerance of the heart in an air breathing fish (Pangasianodon hypophthalmus). Physiol Biochem Zool 88:648–659. https://doi.org/10.1086/682701
Keen AN, Gamperl AK (2012) Blood oxygenation and cardiorespiratory function in steelhead trout (Oncorhynchus mykiss) challenged with an acute temperature increase and zatebradine induced bradycardia. J Therm Biol 37:201–210. https://doi.org/10.1016/j.jtherbio.2012.01.002
Kitagawa AT, Costa LS, Paulino RR, Luz RK, Rosa PV, Guerra-Santos B, Silva RF (2015) Feeding behavior and the effect of photoperiod on the performance and hematological parameters of the pacamã catfish (Lophiosilurus alexandri). Appl Anim Behav Sci 171:211–218. https://doi.org/10.1016/j.applanim.2015.08.025
Kraul S, Brittain K, Cantrell R, Nagao T, Ako H, Ogasawara A, Kitagawa H (1993) Nutritional factors affecting stress resistance in the larval mahi-mahi Coryphaena hippurus. J World Aquacult Soc 24:186–193. https://doi.org/10.1111/j.1749-7345.1993.tb00007.x
Leclercq E, Davie A, Migaud H (2014) The physiological response of farmed ballan wrasse (Labrus bergylta) exposed to an acute stressor. Aquaculture 434:1–4. https://doi.org/10.1016/j.aquaculture.2014.07.017
Lewis JM, Klein G, Walsh PJ, Currie S (2012) Rainbow trout (Oncorhynchus mykiss) shift the age composition of circulating red blood cells towards a younger cohort when exposed to thermal stress. J Comp Physiol B 182:663–671. https://doi.org/10.1007/s00360-012-0650-2
Lim HK, Hur JW (2018) Effects of acute and chronic air exposure on growth and stress response of juvenile olive flounder, Paralichthys olivaceus. Turk J Fish Aquat Sci 18:143–151. https://doi.org/10.4194/1303-2712-v18_1_16
Luz RK, Portella MC (2005) Tolerance to the air exposition test of Hoplias lacerdae larvae and juvenile during its initial development. Braz Arch Biol Technol 48:567–573. https://doi.org/10.1590/S1516-89132005000500009
Madaro A, Olsen RE, Kristiansen TS, Ebbesson LOE, Flik G, Gorissen MA (2016) A comparative study of the response to repeated chasing stress in Atlantic salmon (Salmo salar L.) par and post-smolts. Comp Biochem Phys A 192:7–16. https://doi.org/10.1016/j.cbpa.2015.11.005
Mariano WS, Oba ET, Santos LRB, Fernandes MN (2009) Respostas fisiológicas de Jeju (Hoplerythrinus unitaeniatus) expostos ao ar atmosférico. Rev Bras Saúde Prod Anim 10:210–223 http://revistas.ufba.br/index.php/rbspa/article/view/1204/776
Martins CIM, Schrama JW, Verreth JAJ (2006) The relationship between individual differences in feed efficiency and stress response in African catfish Clarias gariepinus. Aquaculture 256:588–595. https://doi.org/10.1016/j.aquaculture.2006.02.051
Martins-Da-Rocha R, Carvalho EG, Urbinati EC (2004) Physiological responses associated with capture and crowding stress in matrinxã Brycon cephalus (Gunther, 1869). Aquac Res 35:245–249. https://doi.org/10.1111/j.1365-2109.2004.00998.x
Melillo-Filho R, Takata R, Santos AEH, Silva WS, Ikeda AL, Rodrigues LA, Santos JCE, Salaro AL, Luz RK (2014) Draining system and feeding rate during the initial development of Lophiosilurus alexandri (Steindachner, 1877), a carnivorous freshwater fish. Aquac Res 45:1913–1920. https://doi.org/10.1111/are.12139
Melo KDM, Oliveira GR, Brito TS, Soares DRP, Tessitore AJA, Alvarenga ER, Turra EM, Silva FCO, Teixeira EA (2016) Digestibilidade de ingredientes em dietas para juvenis de pacamã (Lophiosilurus alexandri). Pesq Agropec Bras 51:785–788. https://doi.org/10.1590/S0100-204X2016000600012
Milson WK (2012) New insights into gill chemoreception: receptor distribution and roles in water and air breathing fish. Respir Physiol Neurobiol 184:326–339. https://doi.org/10.1016/j.resp.2012.07.013
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleost: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. https://doi.org/10.1023/A:1008924418720
Paital BJ (2014) Modulation of redox regulatory molecules and electron transport chain activity in muscle of air breathing fish Heteropneustes fossilis under air exposure stress. Comp Physiol B 184:65–76 https://doi-org.ez27.periodicos.capes.gov.br/10.1007/s00360-013-0778-8
Pankhurst NW (2011) The endocrinology of stress in fish: an environmental perspective. Gen Comp Endocrinol 170:265–275. https://doi.org/10.1016/j.ygcen.2010.07.017
Parra D, Fierro-Castro C, Teles M, Tridico R, Tort L, Sunyer JO (2013) Effect of acute stress on IgM and IgT responses in vaccinated fish. Fish Shellfish Immunol 34:1727–1728. https://doi.org/10.1016/j.fsi.2013.03.280
Pickering AD, Pottinger TG, Christie P (1982) Recovery of the brown trout, Salmo trutta L., from acute handling stress: a time-course study. J Fish Biol 20:229–244. https://doi.org/10.1111/j.1095-8649.1982.tb03923.x
Pottinger TG, Carrick TR (1999) A comparison of plasma glucose and plasma cortisol as selection markers for high and low stress responsiveness in female rainbow trout. Aquaculture 175:351–363. https://doi.org/10.1016/S0044-8486(99)00107-6
Pottinger TG, Carrick TR, Appleby A, Yeomans WE (2000) High blood cortisol levels and low cortisol receptor affinity: is the chub, Leuciscus cephalus, and a cortisol resistant teleost? Gen Comp Endocrinol 120:108–117. https://doi.org/10.1006/gcen.2000.7544
Pottinger TG, Carrick TR, Yeomans WE (2002) The three-spined stickleback as an environmental sentinel: effects of stressors on whole-body physiological indices. J Fish Biol 61:207–229. https://doi.org/10.1111/j.1095-8649.2002.tb01747.x
Quabius ES, Krupp G, Secombes CJ (2005) Polychlorinated biphenyl 126 affects expression of genes involved in stress-immune interaction in primary cultures of rainbow trout anterior kidney cells. Environ Toxicol Chem 24:3053–3060. https://doi.org/10.1897/05-110R.1
Randall DJ, Shelton G (1963) The effects of changes in environmental gas concentrations on the breathing and heart rate of a teleost fish. Comp Biochem Physiol 9:229–239. https://doi.org/10.1016/0010-406X(63)90046-X
Rehulka J (2000) Influence of astaxanthin on growth rate, condition, and some blood indices of rainbow trout (Oncorhynchus mykiss). Aquaculture 190:27–47. https://doi.org/10.1016/S0044-8486(00)00383-5
Robertson L, Thomas P, Arnold CR, Trant JM (1987) Plasma cortisol and secondary stress responses of red drum to handling transport, rearing density, and a disease outbreak. Progress Fish Cult 49:1–12. https://doi.org/10.1577/1548-8640(1987)49<1:PCASSR>2.0.CO;2
Robertson L, Thomas P, Arnold CR (1988) Plasma cortisol and secondary stress responses of cultured red drum (Sciaenops ocellatus) to several transportation procedures. Aquaculture 68:115–130. https://doi.org/10.1016/0044-8486(88)90235-9
Roth B, Rotabakk BT (2012) Stress associated with commercial longlining and recreational fishing of saithe (Pollachius virens) and the subsequent effect on blood gases and chemistry. Fish Res 115:110–114. https://doi.org/10.1016/j.fishres.2011.05.003
Salaro AL, Oliveira-Junior JCD, Lima FW, Ferraz RB, Pontes MD, Campelo DAV, Zuanon JAS, Luz RK (2015) Gelatin in replacement of bovine heart in feed training of Lophiosilurus alexandri in different water salinities. An Acad Bras Ciênc 87:2281–2287. https://doi.org/10.1590/0001-3765201520140575
Santos JCE, Luz RK (2009) Effect of salinity and prey concentrations on Pseudoplatystoma corruscans, Prochilodus costatus and Lophiosilurus alexandri larviculture. Aquaculture 287:324–328. https://doi.org/10.1016/j.aquaculture.2008.10.014
Scott GR, Matey V, Mendoza JA, Gilmour KM, Perry SF, Almeida-Val VMF, Val AL (2017) Air breathing and aquatic gas exchange during hypoxia in armoured catfish. J Comp Physiol B 187:117–133. https://doi.org/10.1007/s00360-016-1024-y
Silva WS, Cordeiro NIS, Costa DC, Takata R, Luz RK (2014) Frequência alimentar e taxa de arraçoamento durante o condicionamento alimentar de juvenis de pacamã. Pesq Agrop Brasileira 49:648–651. https://doi.org/10.1590/S0100-204X2014000800009
Sinyakov MS, Haimovich A, Avtalion RR (2017) Acute stress promotes post-injury brain regeneration in fish. Brain Res Rev 1676:28–37. https://doi.org/10.1016/j.brainres.2017.09.009
Sloman KA, Desforges PR, Gilmour KM (2001) Evidence for a mineralocorticoid—like receptor linked to branchial chloride cell proliferation in freshwater rainbow trout, Oncorhynchus mykiss. J Exp Biol 204:3953–3961 http://jeb.biologists.org/content/204/22/3953
Sollid J, Nilsson GE (2006) Plasticity of respiratory structures-adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobio 154:241–251. https://doi.org/10.1016/j.resp.2006.02.006
Souza RHD, Soncini R, Glass ML, Sanches JR, Rantin FT (2001) Ventilation, gill perfusion and blood gases in Dourado, Salminus maxillosus Valenciennes (Teleostei, Characidae), exposed to graded hypoxia. J Comp Physiol B 171:483–489. https://doi.org/10.1007/s003600100198
Stoot LJ, Cairns NA, Cull F, Taylor JJ, Jeffrey JD, Morin F, Mandelman JW, Clark TD, Cooke SJ (2014) Use of portable blood physiology point-of-care devices for basic and applied research on vertebrates: a review. Conserv Physiol 2:1–21. https://doi.org/10.1093/conphys/cou011
Tahmasebi-Kohyani A, Keyvanshokooh S, Nematollahi A, Mahmoudi N, Pasha-Zanoosi H (2012) Effects of dietary nucleotides supplementation on rainbow trout (Oncorhynchus mykiss) performance and acute stress response. Fish Physiol Biochem 38:431–440. https://doi.org/10.1007/s10695-011-9524-x
Takaoka O, Ji SC, Ishimaru K, Lee SW, Jeong GS, Biswas A, Takii K (2014) Dietary medicinal herbs and enzyme treated fishmeal improve stress resistances and growth performance at early juvenile stage of red sea bream Pagrus major. Aquac Res 47:1–8. https://doi.org/10.1111/are.12506
Takata R, Silva WS, Costa DC, Melillo-Filho R, Luz RK (2014) Effect of water temperature and prey concentrations on initial development of Lophiosilurus alexandri Steindachner, 1876 (Siluriformes: Pseudopimelodidae), a freshwater fish. Neotrop Ichthyol 12:853–859. https://doi.org/10.1590/1982-0224-20140063
Talas ZS, Gulhan MF (2009) Effects of various propolis concentrations on biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss). Ecotoxicol Environ Saf 72:1994–1998. https://doi.org/10.1016/j.ecoenv.2009.04.011
Trushenski J, Schwarz M, Takeuchi R, Delbos B, Sampaio LA (2010) Physiological responses of cobia Rachycentron canadum following exposure to low water and air exposure stress challenges. Aquaculture 307:173–177. https://doi.org/10.1016/j.aquaculture.2010.07.015
Val AL, Gomes KRM, de Almeida-Val VMF (2015) Rapid regulation of blood parameters under acute hypoxia in the Amazonian fish Prochilodus nigricans. Comp Biochem Physiol A 184:125–131. https://doi.org/10.1016/j.cbpa.2015.02.020
Volpato GL (2007) Considerações metodológicas sobre o teste de preferência na avaliação do bem-estar em peixes. Rev Bras Zootec 36:53–61. https://doi.org/10.1590/S1516-35982007001000006
Weil L, Barry T, Malison J (2001) Fast growth in rainbow trout correlated with a rapid decrease in post-stress cortisol concentrations. Aquaculture 193:373–380. https://doi.org/10.1016/S0044-8486(00)00482-8
Wood CM (1991) Acid-base and ion balance, metabolism, and their interactions, after exhaustive exercise in fish. J Exp Biol 160:285–308 http://jeb.biologists.org/content/160/1/285
Wood CM, Wilson RW, Gonzalez RJ, Patrick ML, Bergman HL, Narahara A, Val AL (1998) Responses of an Amazonian teleosts, the tambaqui (Colossoma macropomum), to low pH in extremely soft water. Physiol Zool 71:658–670. https://doi.org/10.1086/515977
Wright KA, Woods CMC, Gray BE, Lokman PM (2007) Recovery from acute, chronic and transport stress in the pot-bellied seahorse Hippocampus abdominalis. J Fish Biol 70:1447–1457. https://doi.org/10.1111/j.1095-8649.2007.01422.x
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We are grateful to Danilo Gonçalves Bastos for his technical assistance.
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This work was financially supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brasil), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-Brasil), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG-Brasil). LUZ, R.K. received a research grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq No. 305048/2015-5) and from the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG No. PPM-00250/15).
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All experimental protocols were approved by the Committee for Ethics in Animal Experimentation of the Universidade Federal de Minas Gerais (approval reference number: 280/2016). The study complied with the ethical principles under which Experimental Physiology operates, and the experiments complied with the journal’s animal ethics principles and regulation checklist (Grundy 2015).
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Mattioli, C.C., Takata, R., de Oliveira Paes Leme, F. et al. Physiological and metabolic responses of juvenile Lophiosilurus alexandri catfish to air exposure. Fish Physiol Biochem 45, 455–467 (2019). https://doi.org/10.1007/s10695-018-0576-z
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DOI: https://doi.org/10.1007/s10695-018-0576-z