Fish Physiology and Biochemistry

, Volume 45, Issue 1, pp 455–467 | Cite as

Physiological and metabolic responses of juvenile Lophiosilurus alexandri catfish to air exposure

  • Cristiano Campos Mattioli
  • Rodrigo Takata
  • Fabiola de Oliveira Paes Leme
  • Deliane Cristina Costa
  • Ronald Kennedy LuzEmail author


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.


Physiological stress Blood gasometric analysis Management 



We are grateful to Danilo Gonçalves Bastos for his technical assistance.


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).

Compliance with ethical standards

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).


  1. 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. CrossRefGoogle Scholar
  2. 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. CrossRefGoogle Scholar
  3. Apha (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Works Association, Water Environmental Federation, WashingtonGoogle Scholar
  4. 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. CrossRefGoogle Scholar
  5. Baker MR, Gobush KS, Vynne CH (2013) Review of factors influencing stress hormones in fish and wildlife. J Nat Conserv 21:309–318. CrossRefGoogle Scholar
  6. 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. CrossRefGoogle Scholar
  7. 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. CrossRefGoogle Scholar
  8. Barton BA (2000) Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. N Am J Aquac 62:12–18.<0012:SFDITC>2.0.CO;2 CrossRefGoogle Scholar
  9. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525. CrossRefGoogle Scholar
  10. 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. CrossRefGoogle Scholar
  11. 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. CrossRefGoogle Scholar
  12. 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. CrossRefGoogle Scholar
  13. 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. CrossRefGoogle Scholar
  14. 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. CrossRefGoogle Scholar
  15. 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. Google Scholar
  16. 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. CrossRefGoogle Scholar
  17. Cnaani A, Mclean E (2009) Time-course response of cobia (Rachycentron canadum) to acute stress. Aquaculture 289:140–142. CrossRefGoogle Scholar
  18. 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. CrossRefGoogle Scholar
  19. 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. CrossRefGoogle Scholar
  20. 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. CrossRefGoogle Scholar
  21. 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. CrossRefGoogle Scholar
  22. 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. CrossRefGoogle Scholar
  23. 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. Google Scholar
  24. 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. CrossRefGoogle Scholar
  25. 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. CrossRefGoogle Scholar
  26. 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. CrossRefGoogle Scholar
  27. 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. CrossRefGoogle Scholar
  28. 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. Google Scholar
  29. 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. CrossRefGoogle Scholar
  30. Grundy D (2015) Principles and standards for reporting animal experiments in the journal of physiology and experimental physiology. J Physiol 100:755–758. Google Scholar
  31. 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. CrossRefGoogle Scholar
  32. Houston AH, Murad A (1995) Erythrodynamics in fish: recovery of the goldfish Carassius auratus from acute anemia. Can J Zool 73:411–418. CrossRefGoogle Scholar
  33. 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. CrossRefGoogle Scholar
  34. Jain NC (1986) Schalm's veterinary hematology, 4th edn. Lea & Febiger, Philadelphia, p 1221Google Scholar
  35. 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. CrossRefGoogle Scholar
  36. 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. CrossRefGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. 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. CrossRefGoogle Scholar
  39. 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. CrossRefGoogle Scholar
  40. 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. CrossRefGoogle Scholar
  41. 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. CrossRefGoogle Scholar
  42. 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. CrossRefGoogle Scholar
  43. 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. CrossRefGoogle Scholar
  44. 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 Google Scholar
  45. 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. CrossRefGoogle Scholar
  46. 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. CrossRefGoogle Scholar
  47. 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. CrossRefGoogle Scholar
  48. 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. CrossRefGoogle Scholar
  49. Milson WK (2012) New insights into gill chemoreception: receptor distribution and roles in water and air breathing fish. Respir Physiol Neurobiol 184:326–339. CrossRefGoogle Scholar
  50. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleost: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. Pankhurst NW (2011) The endocrinology of stress in fish: an environmental perspective. Gen Comp Endocrinol 170:265–275. CrossRefGoogle Scholar
  53. 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. CrossRefGoogle Scholar
  54. 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. CrossRefGoogle Scholar
  55. 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. CrossRefGoogle Scholar
  56. 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. CrossRefGoogle Scholar
  57. 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. CrossRefGoogle Scholar
  58. 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. CrossRefGoogle Scholar
  59. 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. CrossRefGoogle Scholar
  60. Rehulka J (2000) Influence of astaxanthin on growth rate, condition, and some blood indices of rainbow trout (Oncorhynchus mykiss). Aquaculture 190:27–47. CrossRefGoogle Scholar
  61. 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.<1:PCASSR>2.0.CO;2 CrossRefGoogle Scholar
  62. 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. CrossRefGoogle Scholar
  63. 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. CrossRefGoogle Scholar
  64. 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. CrossRefGoogle Scholar
  65. Santos JCE, Luz RK (2009) Effect of salinity and prey concentrations on Pseudoplatystoma corruscans, Prochilodus costatus and Lophiosilurus alexandri larviculture. Aquaculture 287:324–328. CrossRefGoogle Scholar
  66. 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. CrossRefGoogle Scholar
  67. 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. CrossRefGoogle Scholar
  68. Sinyakov MS, Haimovich A, Avtalion RR (2017) Acute stress promotes post-injury brain regeneration in fish. Brain Res Rev 1676:28–37. CrossRefGoogle Scholar
  69. 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 Google Scholar
  70. 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. CrossRefGoogle Scholar
  71. 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. CrossRefGoogle Scholar
  72. 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. CrossRefGoogle Scholar
  73. 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. CrossRefGoogle Scholar
  74. 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. Google Scholar
  75. 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. CrossRefGoogle Scholar
  76. 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. CrossRefGoogle Scholar
  77. 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. CrossRefGoogle Scholar
  78. 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. CrossRefGoogle Scholar
  79. Volpato GL (2007) Considerações metodológicas sobre o teste de preferência na avaliação do bem-estar em peixes. Rev Bras Zootec 36:53–61. CrossRefGoogle Scholar
  80. 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. CrossRefGoogle Scholar
  81. Wood CM (1991) Acid-base and ion balance, metabolism, and their interactions, after exhaustive exercise in fish. J Exp Biol 160:285–308 Google Scholar
  82. 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. CrossRefGoogle Scholar
  83. 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. CrossRefGoogle Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Escola de VeterináriaUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Unidade de Pesquisa e Reprodução de PeixesFundação Instituto de Pesca do Estado do Rio de JaneiroNiteróiBrazil
  3. 3.Laboratório de Aquacultura da Escola de Veterinária da Universidade Federal de Minas GeraisBelo HorizonteBrazil

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