This study investigated how the time interval between the last EMS (netting) and the acute confinement stress (AC stress) at the end of the experiment can influence growth, haematology, blood biochemistry, immunological response, antioxidant system, liver enzymes, and stress response of oscar (Astronotus ocellatus; 5.7 ± 0.8 g). Nine experimental treatments were tested, as follows: Control, Stress28 (EMS in weeks two and eight), Stress27 (EMS in weeks two and seven), Stress26 (EMS in weeks two and six), Stress25 (EMS in weeks two and five), Stress24 (EMS in week two and four), Stress23 (EMS in week two and three), Stress78 (EMS in week seven and eight), and Stress67 (EMS in week six and seven). After the nine-week experimental period, while it was not significant, fish exposed to Stress78 (26.78 g) and Stress67 (30.05 g) had the lowest growth rates. After AC stress, fish exposed to Stress78 (63.33%) and Control (60.00%) showed the lowest survival rate. The Stress78 fish displayed low resilience, illustrated by values of blood performance, LDL, total protein, lysozyme, ACH50, immunoglobin, complement component 4, complement component 3, cortisol, superoxide dismutase, catalase, and alanine aminotransferase. In conclusion, gathering consecutive stress and not enough recovery time in the Stress78 group negatively affected stress responsiveness and the health of oscar.

Agriculture and Food Livestock and Aquaculture Program Bribie Island Research Centre Woorim QLD 4507 Australia

Department of Animal Marine and Aquatic Biology and Biotechnology Faculty of Life Sciences and Biotechnology Shahid Beheshti University Tehran 1983969411 Iran

Department of Fisheries Faculty Marine Science Tarbiat Modares University Noor 46414 356 Iran

Institute for Marine and Antarctic Studies University of Tasmania Hobart TAS 7005 Australia

Nelson Marlborough Institute of Technology 322 Hardy Street Private Bag 19 Nelson 7010 New Zealand

South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Faculty of Fisheries and Protection of Waters Institute of Aquaculture and Protection of Waters University of South Bohemia in České Budějovice Na Sádkách 37005 České Budějovice Czech Republic

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Ghosi Mobaraki M.R., Abedian Kenari A., Bahrami Gorji S., Esmaeili M. Effect of dietary fish and vegetable oil on the growth performance, body composition, fatty acids profile, reproductive performance and larval resistance in pearl gourami (Trichogaster leeri) Aquac. Nutr. 2020;26:894–907. doi: 10.1111/anu.13048. DOI

Martos-Sitcha J.A., Mancera J.M., Prunet P., Magnoni L.J. Welfare and Stressors in Fish: Challenges Facing Aquaculture. Front. Media SA. 2020;11:162. doi: 10.3389/fphys.2020.00162. PubMed DOI PMC

Schreck C.B., Tort L. Fish Physiology. Volume 35. Elsevier; Amsterdam, The Netherlands: 2016. The concept of stress in fish; pp. 1–34.

Esmaeili M., Hosseini H., Zare M., Sobhan R., Akhavan Rombenso A. Early Mild Stress along with Lipid Improves the Stress Responsiveness of Oscar (Astronotus ocellatus) Aquac. Nutr. 2022;2022:8991678. doi: 10.1155/2022/8991678. PubMed DOI PMC

Pattanaik S.S., Sawant P.B., KA M.X., Srivastava P.P., Dube K., Sawant B.T., Chadha N. Dietary carotenoprotien extracted from shrimp shell waste augments growth, feed utilisation, physio-metabolic responses and colouration in Oscar, Astronotus ocellatus (Agassiz, 1831) Aquaculture. 2021;534:736303. doi: 10.1016/j.aquaculture.2020.736303. DOI

Wood C.M., Kajimura M., Sloman K.A., Scott G.R., Walsh P.J., Almeida-Val V.M., Val A.L. Rapid regulation of Na+ fluxes and ammonia excretion in response to acute environmental hypoxia in the Amazonian oscar, Astronotus ocellatus. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 2007;292:R2048–R2058. doi: 10.1152/ajpregu.00640.2006. PubMed DOI

Matey V., Iftikar F.I., De Boeck G., Scott G.R., Sloman K.A., Almeida-Val V.M., Val A.L., Wood C.M. Gill morphology and acute hypoxia: Responses of mitochondria-rich, pavement, and mucous cells in the Amazonian oscar (Astronotus ocellatus) and the rainbow trout (Oncorhynchus mykiss), two species with very different approaches to the osmo-respiratory compromise. Can. J. Zool. 2011;89:307–324.

De Boeck G., Wood C.M., Iftikar F.I., Matey V., Scott G.R., Sloman K.A., de Nazaré Paula da Silva M., Almeida-Val V.M., Val A.L. Interactions between hypoxia tolerance and food deprivation in Amazonian oscars, Astronotus ocellatus. J. Exp. Biol. 2013;216:4590–4600. doi: 10.1242/jeb.082891. PubMed DOI

Baptista R.B., Souza-Castro N., Almeida-Val V.M.F. Acute hypoxia up-regulates HIF-1α and VEGF mRNA levels in Amazon hypoxia-tolerant Oscar (Astronotus ocellatus) Fish Physiol. Biochem. 2016;42:1307–1318. doi: 10.1007/s10695-016-0219-1. PubMed DOI

Madaro A., Olsen R.E., Kristiansen T.S., Ebbesson L.O., Nilsen T.O., Flik G., Gorissen M. Stress in Atlantic salmon: Response to unpredictable chronic stress. J. Exp. Biol. 2015;218:2538–2550. doi: 10.1242/jeb.120535. PubMed DOI

Vindas M.A., Madaro A., Fraser T.W., Höglund E., Olsen R.E., Øverli Ø., Kristiansen T.S. Coping with a changing environment: The effects of early life stress. R. Soc. Open Sci. 2016;3:160382. doi: 10.1098/rsos.160382. PubMed DOI PMC

Auperin B., Geslin M. Plasma cortisol response to stress in juvenile rainbow trout is influenced by their life history during early development and by egg cortisol content. Gen. Comp. Endocrinol. 2008;158:234–239. doi: 10.1016/j.ygcen.2008.07.002. PubMed DOI

Zare M., Esmaeili N., Hosseini H., Akhavan S., Rombenso A. How do optimum dietary protein and early mild stress events prepare fish for a stressful future? Stress responsiveness of oscar (Astronotus ocellatus) Aquac. Nutr. 2023 in press . PubMed PMC

Zare M., Esmaeili M., Hosseini H., Choupani S.m.H., Akhavan S., Rombenso A. Fish meal replacement and early mild stress improve stress responsiveness of oscar (Astronotus ocellatus) in future stressful events. Animals. 2023;13:1314. doi: 10.3390/ani13081314. PubMed DOI PMC

Ahmadi-Noorbakhsh S., Mirabzadeh Ardakani E., Sadighi J., Aldavood S.J., Farajli Abbasi M., Farzad-Mohajeri S., Ghasemi A., Sharif-Paghaleh E., Hatami Z., Nikravanfard N. Guideline for the care and use of laboratory animals in Iran. Lab Anim. 2021;50:303–305. doi: 10.1038/s41684-021-00871-3. PubMed DOI

Hosseinpour Aghaei R., Abedian Kenari A., Yazdani Sadati M.A., Esmaeili M. The effect of time-dependent protein restriction on growth factors, nonspecific immunity, body composition, fatty acids and amino acids in the Siberian sturgeon (Acipenser baerii) Aquac. Res. 2018;49:3033–3044. doi: 10.1111/are.13764. DOI

Esmaeili M., Abedian Kenari A., Rombenso A. Immunohematological status under acute ammonia stress of juvenile rainbow trout (Oncorhynchus mykiss Walbaum, 1792) fed garlic (Allium sativum) powder-supplemented meat and bone meal-based feeds. Comp. Clin. Pathol. 2017;26:853–866. doi: 10.1007/s00580-017-2457-8. DOI

Zaretabar A., Ouraji H., Kenari A.A., Yeganeh S., Esmaeili M., Amirkolaee A.K. One step toward aquaculture sustainability of a carnivorous species: Fish meal replacement with barley protein concentrate plus wheat gluten meal in Caspian brown trout (Salmo trutta caspius) Aquac. Rep. 2021;20:100714. doi: 10.1016/j.aqrep.2021.100714. DOI

AOAC . Official Methods of Analysis of the AOAC International. Volume 18 The Association; Gaithersburg, ML, USA: 2000.

Kenari A.A., Mahmoudi N., Soltani M., Abediankenari S. Dietary nucleotide supplements influence the growth, haemato-immunological parameters and stress responses in endangered Caspian brown trout (Salmo trutta caspius Kessler, 1877) Aquac. Nutr. 2013;19:54–63. doi: 10.1111/j.1365-2095.2012.00938.x. DOI

Řehulka J., Minařík B., Řehulková E. Red blood cell indices of rainbow trout Oncorhynchus mykiss (Walbaum) in aquaculture. Aquac. Res. 2004;35:529–546. doi: 10.1111/j.1365-2109.2004.01035.x. DOI

Wintrobe M. The volume and hemoglobin content of the red blood corpuscle: Simple method of calculation, normal findings, and value of such calculations in the anemias. Am. J. Med. Sci. 1929;177:513–522. doi: 10.1097/00000441-192904000-00006. DOI

Esmaeili M. Blood Performance: A New Formula for Fish Growth and Health. Biology. 2021;10:1236. doi: 10.3390/biology10121236. PubMed DOI PMC

Clerton P., Troutaud D., Verlhac V., Gabaudan J., Deschaux P. Dietary vitamin E and rainbow trout (Oncorhynchus mykiss) phagocyte functions: Effect on gut and on head kidney leucocytes. Fish Shellfish. Immunol. 2001;11:1–13. doi: 10.1006/fsim.2000.0287. PubMed DOI

Amar E.C., Kiron V., Satoh S., Okamoto N., Watanabe T. Effects of dietary β-carotene on the immune response of rainbow trout Oncorhynchus mykiss. Fish. Sci. 2000;66:1068–1075. doi: 10.1046/j.1444-2906.2000.00170.x. DOI

Hosseini H., Pooyanmehr M., Foroughi A., Esmaeili M., Ghiasi F., Lorestany R. Remarkable positive effects of figwort (Scrophularia striata) on improving growth performance, and immunohematological parameters of fish. Fish Shellfish. Immunol. 2022;120:111–121. doi: 10.1016/j.fsi.2021.11.020. PubMed DOI

Asgari M., Abedian Kenari A., Esmaeili M., Rombenso A. Effects of hydroalcoholic extract of honeybee pollen on growth performance, flesh quality, and immune and stress response of rainbow trout (Oncorhynchus mykiss) Aquac. Nutr. 2020;26:1505–1519. doi: 10.1111/anu.13098. DOI

Pickering A., Pottinger T., Christie P. Recovery of the brown trout, Salmo trutta L., from acute handling stress: A time-course study. J. Fish Biol. 1982;20:229–244. doi: 10.1111/j.1095-8649.1982.tb03923.x. DOI

Kavitha P., Rao J.V. Oxidative stress and locomotor behaviour response as biomarkers for assessing recovery status of mosquito fish, Gambusia affinis after lethal effect of an organophosphate pesticide, monocrotophos. Pestic. Biochem. Physiol. 2007;87:182–188. doi: 10.1016/j.pestbp.2006.07.008. DOI

Douxfils J., Mandiki S., Marotte G., Wang N., Silvestre F., Milla S., Henrotte E., Vandecan M., Rougeot C., Mélard C. Does domestication process affect stress response in juvenile Eurasian perch Perca fluviatilis? Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2011;159:92–99. doi: 10.1016/j.cbpa.2011.01.021. PubMed DOI

Ericsson M., Fallahsharoudi A., Bergquist J., Kushnir M.M., Jensen P. Domestication effects on behavioural and hormonal responses to acute stress in chickens. Physiol. Behav. 2014;133:161–169. doi: 10.1016/j.physbeh.2014.05.024. PubMed DOI

Esmaeili M., Carter C.G., Wilson R., Walker S.P., Miller M.R., Bridle A.R., Symonds J.E. Protein metabolism in the liver and white muscle is associated with feed efficiency in Chinook salmon (Oncorhynchus tshawytscha) reared in seawater: Evidence from proteomic analysis. Comp. Biochem. Physiol. Part D Genom. Proteom. 2022;42:100994. doi: 10.1016/j.cbd.2022.100994. PubMed DOI

Barton B.A., Schreck C.B., Barton L.D. Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Dis. Aquat. Org. 1987;2:173–185. doi: 10.3354/dao002173. DOI

Peters G., Schwarzer R. Changes in hemopoietic tissue of rainbow trout under influence of stress. Dis. Aquat. Org. 1985;1:1–10. doi: 10.3354/dao001001. DOI

Shearer K.D. Factors affecting the proximate composition of cultured fishes with emphasis on salmonids. Aquaculture. 1994;119:63–88. doi: 10.1016/0044-8486(94)90444-8. DOI

Herrera M., Mancera J.M., Costas B. The use of dietary additives in fish stress mitigation: Comparative endocrine and physiological responses. Front. Endocrinol. 2019;10:447. doi: 10.3389/fendo.2019.00447. PubMed DOI PMC

Fazio F. Fish hematology analysis as an important tool of aquaculture: A review. Aquaculture. 2019;500:237–242. doi: 10.1016/j.aquaculture.2018.10.030. DOI

Ravardshiri M., Bahram S., Javadian S.R., Bahrekazemi M. Cinnamon Promotes Growth Performance, Digestive Enzyme, Blood Parameters, and Antioxidant Activity of Rainbow Trout (Oncorhynchus mykiss) in Low-Carbohydrate Diets. Turk. J. Fish. Aquat. Sci. 2021;21:309–322. doi: 10.4194/1303-2712-v21_7_01. DOI

Montazeri H., Abedian Kenari A., Esmaeili M. Soybean-based diets plus probiotics improve the profile of fatty acids, digestibility, intestinal microflora, growth performance, and the innate immunity of beluga (Huso huso) Aquac. Res. 2021;52:152–166. doi: 10.1111/are.14877. DOI

Hosseini H., Esmaeili M., Zare M., Rombenso A. Egg enrichment with n-3 fatty acids in farmed hens in sub-optimum temperature: A cold-temperament additive mix alleviates adverse effects of stress on performance and health. J. Anim. Physiol. Anim. Nutr. 2021;106:1333–1334. doi: 10.1111/jpn.13659. PubMed DOI

Saleh N.E., Mourad M.M., El-Banna S.G., Abdel-Tawwab M. Soybean protein concentrate as a fishmeal replacer in weaning diets for common sole (Solea solea) post-larvae: Effects on the growth, biochemical and oxidative stress biomarkers, and histopathological investigations. Aquaculture. 2021;544:737080. doi: 10.1016/j.aquaculture.2021.737080. DOI

Zhao H., Wu Z., Zhou Y., Guo D., Wang H., Chen X. Hepatic lipid metabolism and oxidative stress responses of grass carp (Ctenopharyngodon idella) fed diets of two different lipid levels against Aeromonas hydrophila infection. Aquaculture. 2019;509:149–158. doi: 10.1016/j.aquaculture.2019.05.029. DOI

Spickett C.M., Forman H.J. Lipid Oxidation in Health and Disease. CRC Press; Boca Raton, FL, USA: 2015.

Bae Y.-S., Shin E.-C., Bae Y.-S., Van Eden W. Stress and immunity. Front. Media SA. 2019;10:245. PubMed PMC

Holzer P., Farzi A., Hassan A.M., Zenz G., Jačan A., Reichmann F. Visceral inflammation and immune activation stress the brain. Front. Immunol. 2017;8:1613. doi: 10.3389/fimmu.2017.01613. PubMed DOI PMC

Tort L. Stress and immune modulation in fish. Dev. Comp. Immunol. 2011;35:1366–1375. doi: 10.1016/j.dci.2011.07.002. PubMed DOI

Pottinger T. Changes in blood cortisol, glucose and lactate in carp retained in anglers’ keepnets. J. Fish Biol. 1998;53:728–742. doi: 10.1006/jfbi.1998.0737. DOI

Hoseinifar S.H., Yousefi S., Van Doan H., Ashouri G., Gioacchini G., Maradonna F., Carnevali O. Oxidative stress and antioxidant defense in fish: The implications of probiotic, prebiotic, and synbiotics. Rev. Fish. Sci. Aquac. 2020;29:198–217. doi: 10.1080/23308249.2020.1795616. DOI

Li Z.-H., Zlabek V., Velisek J., Grabic R., Machova J., Randak T. Modulation of antioxidant defence system in brain of rainbow trout (Oncorhynchus mykiss) after chronic carbamazepine treatment. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2010;151:137–141. doi: 10.1016/j.cbpc.2009.09.006. PubMed DOI

Hegazi M.M., Attia Z.I., Ashour O.A. Oxidative stress and antioxidant enzymes in liver and white muscle of Nile tilapia juveniles in chronic ammonia exposure. Aquat. Toxicol. 2010;99:118–125. doi: 10.1016/j.aquatox.2010.04.007. PubMed DOI

Tejpal C., Pal A., Sahu N., Kumar J.A., Muthappa N., Vidya S., Rajan M. Dietary supplementation of L-tryptophan mitigates crowding stress and augments the growth in Cirrhinus mrigala fingerlings. Aquaculture. 2009;293:272–277. doi: 10.1016/j.aquaculture.2008.09.014. DOI

Liu F., Shi H.-z., Guo Q.-s., Yu Y.-b., Wang A.-m., Lv F., Shen W.-b. Effects of astaxanthin and emodin on the growth, stress resistance and disease resistance of yellow catfish (Pelteobagrus fulvidraco) Fish Shellfish. Immunol. 2016;51:125–135. doi: 10.1016/j.fsi.2016.02.020. PubMed DOI

Dawood M.A., Gewaily M.S., Monier M.N., Younis E.M., Van Doan H., Sewilam H. The regulatory roles of yucca extract on the growth rate, hepato-renal function, histopathological alterations, and immune-related genes in common carp exposed with acute ammonia stress. Aquaculture. 2021;534:736287. doi: 10.1016/j.aquaculture.2020.736287. DOI

Sun Z., Tan X., Liu Q., Ye H., Zou C., Xu M., Zhang Y., Ye C. Physiological, immune responses and liver lipid metabolism of orange-spotted grouper (Epinephelus coioides) under cold stress. Aquaculture. 2019;498:545–555. doi: 10.1016/j.aquaculture.2018.08.051. DOI

Hoseini S.M., Gupta S.K., Yousefi M., Kulikov E.V., Drukovsky S.G., Petrov A.K., Mirghaed A.T., Hoseinifar S.H., Van Doan H. Mitigation of transportation stress in common carp, Cyprinus carpio, by dietary administration of turmeric. Aquaculture. 2022;564:737380. doi: 10.1016/j.aquaculture.2021.737380. DOI

The crosstalk between photoperiod and early mild stress on juvenile oscar (Astronotus ocellatus) after acute stress

Does Dietary Sodium Alginate with Low Molecular Weight Affect Growth, Antioxidant System, and Haemolymph Parameters and Alleviate Cadmium Stress in Whiteleg Shrimp (Litopenaeus vannamei)?