{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,28]],"date-time":"2026-10-28T23:16:11Z","timestamp":1793229371603,"version":"4.5.0"},"reference-count":43,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2024,4,16]],"date-time":"2024-04-16T00:00:00Z","timestamp":1713225600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Key Research and Development Project of Shandong Province","award":["2021SFGC0701"],"award-info":[{"award-number":["2021SFGC0701"]}]},{"name":"Key Research and Development Project of Shandong Province","award":["23-1-3HVSF-2-HY"],"award-info":[{"award-number":["23-1-3HVSF-2-HY"]}]},{"name":"Key Research and Development Project of Shandong Province","award":["QDBSH20230102021"],"award-info":[{"award-number":["QDBSH20230102021"]}]},{"name":"Key Research and Development Project of Shandong Province","award":["ZR2023QC196"],"award-info":[{"award-number":["ZR2023QC196"]}]},{"name":"Qingdao Marine Science and Technology Innovation Project","award":["2021SFGC0701"],"award-info":[{"award-number":["2021SFGC0701"]}]},{"name":"Qingdao Marine Science and Technology Innovation Project","award":["23-1-3HVSF-2-HY"],"award-info":[{"award-number":["23-1-3HVSF-2-HY"]}]},{"name":"Qingdao Marine Science and Technology Innovation Project","award":["QDBSH20230102021"],"award-info":[{"award-number":["QDBSH20230102021"]}]},{"name":"Qingdao Marine Science and Technology Innovation Project","award":["ZR2023QC196"],"award-info":[{"award-number":["ZR2023QC196"]}]},{"name":"Qingdao Postdoctoral Science Foundation","award":["2021SFGC0701"],"award-info":[{"award-number":["2021SFGC0701"]}]},{"name":"Qingdao Postdoctoral Science Foundation","award":["23-1-3HVSF-2-HY"],"award-info":[{"award-number":["23-1-3HVSF-2-HY"]}]},{"name":"Qingdao Postdoctoral Science Foundation","award":["QDBSH20230102021"],"award-info":[{"award-number":["QDBSH20230102021"]}]},{"name":"Qingdao Postdoctoral Science Foundation","award":["ZR2023QC196"],"award-info":[{"award-number":["ZR2023QC196"]}]},{"name":"Natural Science Foundation of Shandong Province","award":["2021SFGC0701"],"award-info":[{"award-number":["2021SFGC0701"]}]},{"name":"Natural Science Foundation of Shandong Province","award":["23-1-3HVSF-2-HY"],"award-info":[{"award-number":["23-1-3HVSF-2-HY"]}]},{"name":"Natural Science Foundation of Shandong Province","award":["QDBSH20230102021"],"award-info":[{"award-number":["QDBSH20230102021"]}]},{"name":"Natural Science Foundation of Shandong Province","award":["ZR2023QC196"],"award-info":[{"award-number":["ZR2023QC196"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>(1) Background: In aquaculture, chronic stress due to high stocking density impairs animals\u2019 welfare and results in declined fishery production with low protein quality. However, most previous studies evaluated the effects of high stocking density on trout in freshwater rather than seawater. (2) Methods: Juvenile trout were reared for 84 days in circular tanks under three stocking densities, including low density (\u201cLD\u201d, 9.15 kg\/m3), moderate density (\u201cMD\u201d, 13.65 kg\/m3), and high density (\u201cHD\u201d, 27.31 kg\/m3) in seawater. The final densities of LD, MD, and HD were 22.00, 32.05 and 52.24 kg\/m3, respectively. Growth performance and lipid metabolism were evaluated. (3) Results: Growth performance and feeding efficiency were significantly reduced due to chronic stress under high density in mariculture. The digestive activity of lipids was promoted in the gut of HD fish, while the concentration of triglycerides was decreased in the blood. Furthermore, decreased acetyl-CoA carboxylase (ACC) and fatty acid synthase (FAS), increased hormone-sensitive lipase (HSL) concentrations, and activated hepatic \u03b2-oxidation processes were observed in trout under HD. Redundancy analysis showed that glycerol and HSL can be used as potential markers to evaluate the growth performance of trout in mariculture. (4) Conclusions: We showed that chronic high stocking density led to negative effects on growth performance, reduced de novo synthesis of fatty acids, and enhanced lipolysis.<\/jats:p>","DOI":"10.3390\/biology13040263","type":"journal-article","created":{"date-parts":[[2024,4,16]],"date-time":"2024-04-16T11:13:02Z","timestamp":1713265982000},"page":"263","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Effects of Chronic Stress from High Stocking Density in Mariculture: Evaluations of Growth Performance and Lipid Metabolism of Rainbow Trout (Oncorhychus mykiss)"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-6617-7996","authenticated-orcid":false,"given":"Zhao","family":"Li","sequence":"first","affiliation":[{"name":"Key Laboratory of Mariculture (Ocean University of China), Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qinfeng","family":"Gao","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture (Ocean University of China), Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"},{"name":"Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuanglin","family":"Dong","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture (Ocean University of China), Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"},{"name":"Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kang","family":"Dong","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture (Ocean University of China), Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuling","family":"Xu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture (Ocean University of China), Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaoping","family":"Mei","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture (Ocean University of China), Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhishuai","family":"Hou","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture (Ocean University of China), Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,4,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1093\/embo-reports\/kve236","article-title":"Fish as food aquaculture\u2019s contribution","volume":"2","author":"Tidwell","year":"2001","journal-title":"EMBO Rep."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1038\/s41586-021-03308-6","article-title":"A 20-year retrospective review of global aquaculture","volume":"591","author":"Naylor","year":"2021","journal-title":"Nature"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/S0044-8486(02)00626-9","article-title":"The influence of rearing density on stress response and disease susceptibility of ayu (Plecoglossus altivelis)","volume":"220","author":"Iguchi","year":"2003","journal-title":"Aquaculture"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1506","DOI":"10.1111\/j.1365-2109.2008.02020.x","article-title":"Effects of stocking density on haematological parameters, growth and fin erosion of great sturgeon (Huso huso) juveniles","volume":"39","author":"Rafatnezhad","year":"2008","journal-title":"Aquac. Res."},{"key":"ref_5","unstructured":"Schreck, C.B., and Tort, L. (2016). Biology of Stress in Fish\u2014Fish Physiology, Academic Press."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"141458","DOI":"10.1016\/j.scitotenv.2020.141458","article-title":"What metabolic, osmotic and molecular stress responses tell us about extreme ambient heatwave impacts in fish at low salinities: The case of European seabass, Dicentrarchus labrax","volume":"749","author":"Islam","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Yeh, C.M., Glock, M., and Ryu, S. (2013). An optimized whole-body cortisol quantification method for assessing stress levels in larval zebrafish. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0079406"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.ygcen.2011.06.004","article-title":"Species specificity in the magnitude and duration of the acute stress response in Mediterranean marine fish in culture","volume":"173","author":"Fanouraki","year":"2011","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4805","DOI":"10.1111\/are.14783","article-title":"Terminalia catappa improves growth performance and survival of the Amazon leaf fish (Monocirrhus polyacanthus) larvae submitted to handling stress","volume":"51","author":"Ramos","year":"2020","journal-title":"Aquac. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1007\/s00360-011-0585-z","article-title":"Stress-induced effects on feeding behavior and growth performance of the sea bass (Dicentrarchus labrax): A self-feeding approach","volume":"181","author":"Leal","year":"2011","journal-title":"J. Comp. Physiol. B"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Glover, K.A. (2008). Genetic characterisation of farmed rainbow trout in Norway: Intra- and inter-strain variation reveals potential for identification of escapees. BMC Genet., 9.","DOI":"10.1186\/1471-2156-9-87"},{"key":"ref_12","first-page":"1","article-title":"Researching progresses and prospects in large salmonidae farming in Clod Water of Yellow Sea","volume":"49","author":"Dong","year":"2019","journal-title":"Period. Ocean Univ. China"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"736274","DOI":"10.1016\/j.aquaculture.2020.736274","article-title":"Growth performance and physiological parameters of Colossoma macropomum in a recirculating aquaculture system (RAS): Importance of stocking density and classification","volume":"534","author":"Santos","year":"2021","journal-title":"Aquaculture"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1111\/j.1095-8649.2002.tb00893.x","article-title":"The relationships between stocking density and welfare in farmed rainbow trout","volume":"61","author":"Ellis","year":"2002","journal-title":"J. Fish Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1007\/s10695-016-0229-z","article-title":"Serum biochemical and non-specific immune responses of rainbow trout (Oncorhynchus mykiss) to dietary nucleotide and chronic stress","volume":"42","author":"Yousefi","year":"2016","journal-title":"Fish Physiol. Biochem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.aquaculture.2017.03.036","article-title":"Combined or individual effects of dietary vitamin E and selenium nanoparticles on humoral immune status and serum parameters of rainbow trout (Oncorhynchus mykiss) under high stocking density","volume":"474","author":"Naderi","year":"2017","journal-title":"Aquaculture"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"734908","DOI":"10.1016\/j.aquaculture.2019.734908","article-title":"Effects of dietary tryptophan supplementation and stocking density on growth performance and stress responses in rainbow trout (Oncorhynchus mykiss)","volume":"519","author":"Hoseini","year":"2020","journal-title":"Aquaculture"},{"key":"ref_18","first-page":"17","article-title":"Evaluation of rainbow trout (Oncorhynchus mykiss<) mariculture on the Turkish Black Sea coast","volume":"51","author":"Sahin","year":"1999","journal-title":"Isr. J. Aquac.-Bamidgeh"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"coaa121","DOI":"10.1093\/conphys\/coaa121","article-title":"Fatty acid composition and parasitism of European sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus) populations in the northern Catalan Sea in the context of changing environmental conditions","volume":"8","author":"Bou","year":"2020","journal-title":"Conserv. Physiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1007\/s10499-012-9513-9","article-title":"Stocking density affects growth and metabolic parameters in the brill (Scophthalmus rhombus)","volume":"20","author":"Herrera","year":"2012","journal-title":"Aquac. Int."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1023\/A:1007719928905","article-title":"High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles","volume":"20","author":"Montero","year":"1999","journal-title":"Fish Physiol. Biochem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1162992","DOI":"10.3389\/fnut.2023.1162992","article-title":"Adipose tissue-derived exosomes contribute to obesity-associated liver diseases in long-term high-fat diet-fed mice, but not in short-term","volume":"10","author":"Son","year":"2023","journal-title":"Front. Nutr."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Wang, D., Chen, G., Song, L., Chai, M., Wang, Y., Shui, S., Zhang, H., Sha, Y., and Yao, Y. (2020). Effects of Dietary Protein Levels on Bamei Pig Intestinal Colony Compositional Traits. BioMed Res. Int., 2020.","DOI":"10.22541\/au.159551270.00410123"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Jia, R., Wang, L., Hou, Y., Feng, W., Li, B., and Zhu, J. (2022). Effects of Stocking Density on the Growth Performance, Physiological Parameters, Redox Status and Lipid Metabolism of Micropterus salmoides in Integrated Rice-Fish Farming Systems. Antioxidants, 11.","DOI":"10.3390\/antiox11071215"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1007\/s10695-021-00948-3","article-title":"Stocking density alters growth performance, serum biochemistry, digestive enzymes, immune response, and muscle quality of largemouth bass (Micropterus salmoides) in in-pond raceway system","volume":"47","author":"Ni","year":"2021","journal-title":"Fish Physiol. Biochem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00360-011-0601-3","article-title":"Osmoregulation and epithelial water transport: Lessons from the intestine of marine teleost fish","volume":"182","author":"Whittamore","year":"2012","journal-title":"J. Comp. Physiol. B"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"734937","DOI":"10.1016\/j.aquaculture.2020.734937","article-title":"Growth, osmoregulatory response, adenine nucleotide contents, and liver transcriptome analysis of steelhead trout (Oncorhynchus mykiss) under different salinity acclimation methods","volume":"520","author":"Xiong","year":"2020","journal-title":"Aquaculture"},{"key":"ref_28","unstructured":"Oxford University Press (2023). Official Methods of Analysis of AOAC INTERNATIONAL, Oxford University Press."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e18685","DOI":"10.1016\/j.heliyon.2023.e18685","article-title":"Fresh water resource, scarcity, water salinity challenges and possible remedies: A review","volume":"9","author":"Musie","year":"2023","journal-title":"Heliyon"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"734711","DOI":"10.1016\/j.aquaculture.2019.734711","article-title":"Effects of temperature and photoperiod on rainbow trout (Oncorhynchus mykiss) smoltification and haematopoiesis","volume":"519","author":"Morro","year":"2020","journal-title":"Aquaculture"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/s10695-011-9568-y","article-title":"Cortisol and finfish welfare","volume":"38","author":"Ellis","year":"2012","journal-title":"Fish Physiol. Biochem."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1016\/j.yhbeh.2005.04.008","article-title":"Divergence in behavioural responses to stress in two strains of rainbow trout (Oncorhynchus mykiss) with contrasting stress responsiveness","volume":"48","author":"Schjolden","year":"2005","journal-title":"Horm. Behav."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2486","DOI":"10.1111\/j.1095-8649.2010.02635.x","article-title":"Coping strategies in farmed African catfish Clarias gariepinus. Does it affect their welfare?","volume":"76","author":"Ramli","year":"2010","journal-title":"J. Fish Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.aquaculture.2011.10.021","article-title":"The effects of stocking density and low level sustained exercise on the energetic efficiency of rainbow trout (Oncorhynchus mykiss) reared at 19 \u00b0C","volume":"324\u2013325","author":"Larsen","year":"2012","journal-title":"Aquaculture"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.aquaculture.2009.11.014","article-title":"Metabolic molecular indicators of chronic stress in gilthead seabream (Sparus aurata) using comparative proteomics","volume":"299","author":"Alves","year":"2010","journal-title":"Aquaculture"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.fsi.2022.08.022","article-title":"A different transcriptional landscape sheds light on Russian sturgeon (Acipenser gueldenstaedtii) mechanisms to cope with bacterial infection and chronic heat stress","volume":"128","author":"Castellano","year":"2022","journal-title":"Fish Shellfish Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1124\/jpet.113.205369","article-title":"Differential regulation of hepatic organic cation transporter 1, organic anion-transporting polypeptide 1a4, bile-salt export pump, and multidrug resistance-associated protein 2 transporter expression in lymphocyte-deficient mice associates with interleukin-6 production","volume":"347","author":"Bodeman","year":"2013","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"734607","DOI":"10.1016\/j.aquaculture.2019.734607","article-title":"Short-term stress due to dietary pectin induces cholestasis, and chronic stress induces hepatic steatosis and fibrosis in yellow catfish, Pelteobagrus fulvidraco","volume":"516","author":"Cai","year":"2020","journal-title":"Aquaculture"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"S341","DOI":"10.1016\/j.fertnstert.2013.07.902","article-title":"The ratio of estrogen receptor \u03b1 to \u03b2 is associated with the expression of lipoprotein lipase and hormone-sensitive lipase in human adipose tissue","volume":"100","author":"Yi","year":"2013","journal-title":"Fertil. Steril."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/0065-2571(94)90022-1","article-title":"The multifunctional role of hormone-sensitive lipase in lipid metabolism","volume":"34","author":"Yeaman","year":"1994","journal-title":"Adv. Enzyme Regul."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"96089","DOI":"10.18632\/oncotarget.21716","article-title":"Novel direct AMPK activator suppresses non-small cell lung cancer through inhibition of lipid metabolism","volume":"8","author":"Chen","year":"2017","journal-title":"Oncotarget"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/S0044-8486(00)00325-2","article-title":"Freeze susceptibility in haddock (Melanogrammus aeglefinus)","volume":"188","author":"Ewart","year":"2000","journal-title":"Aquaculture"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.aquaculture.2013.01.032","article-title":"Changes in the activities and mRNA expression levels of lipoprotein lipase (LPL), hormone-sensitive lipase (HSL) and fatty acid synthetase (FAS) of Nile tilapia (Oreochromis niloticus) during fasting and re-feeding","volume":"400\u2013401","author":"Tian","year":"2013","journal-title":"Aquaculture"}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/13\/4\/263\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:28:26Z","timestamp":1760106506000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/13\/4\/263"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,16]]},"references-count":43,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2024,4]]}},"alternative-id":["biology13040263"],"URL":"https:\/\/doi.org\/10.3390\/biology13040263","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,16]]}}}