{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T05:09:02Z","timestamp":1789016942596,"version":"build-2803163510"},"reference-count":48,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T00:00:00Z","timestamp":1788825600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100014103","name":"Key Technology Research and Development Program of Shandong Province","doi-asserted-by":"crossref","award":["2023LZGC019"],"award-info":[{"award-number":["2023LZGC019"]}],"id":[{"id":"10.13039\/100014103","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100014103","name":"Key Technology Research and Development Program of Shandong Province","doi-asserted-by":"crossref","award":["2023CXGC010410"],"award-info":[{"award-number":["2023CXGC010410"]}],"id":[{"id":"10.13039\/100014103","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Agriculture Industry System of Shandong Province","award":["SDAIT-22-03"],"award-info":[{"award-number":["SDAIT-22-03"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Apostichopus japonicus is a temperate marine echinoderm whose growth and reproduction are strongly influenced by temperature. We compared adult sea cucumbers exposed to stepwise warming (10\u201312, 12\u201314, and 14\u201316 \u00b0C across three successive 20-day stages) with animals maintained at 15 \u00b0C. Growth indices, gonadosomatic index (GSI), gonadal histology, and energy-budget components were evaluated in females and males. The 60 d experiment used three replicate tanks for each treatment-by-sex combination. Compared with the constant 15 \u00b0C treatment, the stepwise-warming regime showed a higher female GSI at stage III; representative gonadal sections documented stage-related structural changes in both treatments. No significant treatment effects were detected for final wet weight, specific growth rate, daily growth rate, or feed conversion ratio. Excretory energy decreased during stages II and III, while the proportion allocated to gonadal growth increased. Stage-specific within-sex comparisons showed higher gonadal growth energy under stepwise warming in both sexes during stage II, while the clearest GSI difference occurred in females during stage III; treatment \u00d7 sex interactions were not significant. The clearest differences between the two temperature regimes were observed during stages II and III (12\u201316 \u00b0C). The findings provide an integrative physiological basis for temperature management during broodstock conditioning of A. japonicus.<\/jats:p>","DOI":"10.3390\/ani16182815","type":"journal-article","created":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T08:10:22Z","timestamp":1788855022000},"page":"2815","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Different Temperature Regimes Affect Gonadal Development and Energy Budget in Apostichopus japonicus"],"prefix":"10.3390","volume":"16","author":[{"given":"Jingzhao","family":"Zhang","sequence":"first","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"}]},{"given":"Kaiyou","family":"Deng","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-2696-769X","authenticated-orcid":false,"given":"Xueyu","family":"Zhu","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"formal-analysis","vocabulary":"credit"}]},{"given":"Weijun","family":"Wang","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-1448-2336","authenticated-orcid":false,"given":"Yanwei","family":"Feng","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"given":"Xiaohui","family":"Xu","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9478-6918","authenticated-orcid":false,"given":"Zan","family":"Li","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"formal-analysis","vocabulary":"credit"}]},{"given":"Cuiju","family":"Cui","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"formal-analysis","vocabulary":"credit"}]},{"given":"Jianmin","family":"Yang","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"given":"Guohua","family":"Sun","sequence":"additional","affiliation":[{"name":"School of Fisheries, Ludong University, Yantai 264025, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"conceptualization","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Chen, J., Lv, Z., and Guo, M. (2022). Research advancement of Apostichopus japonicus from 2000 to 2021. Front. Mar. Sci., 9.","DOI":"10.3389\/fmars.2022.931903"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1080\/23308249.2016.1193472","article-title":"A review of sea cucumber aquaculture, ranching, and stock enhancement in China","volume":"24","author":"Han","year":"2016","journal-title":"Rev. Fish. Sci. Aquac."},{"key":"ref_3","unstructured":"Bureau of Fisheries of the Ministry of Agriculture and Rural Affairs, National Fisheries Technology Extension Center, and China Society of Fisheries (2025). China Fishery Statistical Yearbook 2025."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1007\/s10499-025-01988-9","article-title":"Evolving challenges and innovations in sea cucumber aquaculture","volume":"33","author":"Omont","year":"2025","journal-title":"Aquac. Int."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.ydbio.2008.11.003","article-title":"Neuronal peptides induce oocyte maturation and gamete spawning of sea cucumber, Apostichopus japonicus","volume":"326","author":"Kato","year":"2009","journal-title":"Dev. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"107820","DOI":"10.1016\/j.anireprosci.2025.107820","article-title":"Relaxin-like gonad-stimulating peptide promotes gamete maturation and spawning in the sea cucumber Apostichopus japonicus","volume":"275","author":"Wang","year":"2025","journal-title":"Anim. Reprod. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"742377","DOI":"10.1016\/j.aquaculture.2025.742377","article-title":"A long photoperiod following a short one, and low temperature, stimulate gametogenesis in the sea cucumber Holothuria arguinensis","volume":"603","author":"Marquet","year":"2025","journal-title":"Aquaculture"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1080\/19768354.2016.1266386","article-title":"Reproductive cycle and releasing time for increase of resource of adult sea cucumber Apostichopus japonicus released to seed breeding grounds","volume":"21","author":"Kang","year":"2017","journal-title":"Anim. Cells Syst."},{"key":"ref_9","first-page":"101","article-title":"Broodstock conditioning and spawning","volume":"Volume 39","author":"Yang","year":"2015","journal-title":"The Sea Cucumber Apostichopus japonicus: History, Biology and Aquaculture"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1007\/s12562-013-0627-4","article-title":"Combined influence of water temperature, salinity and body size on energy budget in the sea cucumber Apostichopus japonicus Selenka","volume":"79","author":"Xie","year":"2013","journal-title":"Fish. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3354\/aei00210","article-title":"Parameterisation and application of dynamic energy budget model to sea cucumber Apostichopus japonicus","volume":"9","author":"Ren","year":"2017","journal-title":"Aquac. Environ. Interact."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1016\/j.aquaculture.2016.06.045","article-title":"Modelling growth performance and feeding behaviour of Atlantic salmon (Salmo salar L.) in commercial-size aquaculture net pens: Model details and validation through full-scale experiments","volume":"464","author":"Alver","year":"2016","journal-title":"Aquaculture"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1016\/j.seares.2006.03.007","article-title":"Application of a dynamic energy budget model to the Pacific oyster, Crassostrea gigas, reared under various environmental conditions","volume":"56","author":"Pouvreau","year":"2006","journal-title":"J. Sea Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/j.seares.2018.05.001","article-title":"Effects of hypoxia on metabolic functions in marine organisms: Observed patterns and modelling assumptions within the context of dynamic energy budget (DEB) theory","volume":"143","author":"Thomas","year":"2019","journal-title":"J. Sea Res."},{"key":"ref_15","first-page":"101706","article-title":"Unveiling the roles of oxidative stress defense and energy metabolism adjustment in low-temperature stress responses of Apostichopus japonicus: An integrated physiological, transcriptomic and metabolomic analysis","volume":"58","author":"He","year":"2026","journal-title":"Comp. Biochem. Physiol. D Genom. Proteom."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1016\/j.aquaculture.2007.08.038","article-title":"Temperature effects on growth-ration relationships of juvenile sea cucumber Apostichopus japonicus (Selenka)","volume":"272","author":"An","year":"2007","journal-title":"Aquaculture"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.aquaculture.2016.09.039","article-title":"Effects of feeding frequency and density on growth, energy budget and physiological performance of sea cucumber Apostichopus japonicus (Selenka)","volume":"466","author":"Xia","year":"2017","journal-title":"Aquaculture"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"6872","DOI":"10.1111\/gcb.16453","article-title":"Acute, diel, and annual temperature variability and the thermal biology of ectotherms","volume":"28","author":"Kefford","year":"2022","journal-title":"Glob. Change Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"106231","DOI":"10.1016\/j.marenvres.2023.106231","article-title":"Combined effects of temperature and emersion-immersion cycles on metabolism and bioenergetics of the Pacific oyster Crassostrea (Magallana) gigas","volume":"192","author":"Bruhns","year":"2023","journal-title":"Mar. Environ. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"111082","DOI":"10.1016\/j.cbpa.2021.111082","article-title":"Invited review: Thermal effects on oxidative stress in vertebrate ectotherms","volume":"263","author":"Ritchie","year":"2022","journal-title":"Comp. Biochem. Physiol. A Mol. Integr. Physiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"117928","DOI":"10.1016\/j.marpolbul.2025.117928","article-title":"Effects of temperature and salinity on CO2 fluxes dynamics and respiration metabolism in the sea cucumber Apostichopus japonicus (Selenka)","volume":"215","author":"Mei","year":"2025","journal-title":"Mar. Pollut. Bull."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"AQUAST1935","DOI":"10.4194\/AQUAST1935","article-title":"Effects of dietary phospholipids on growth, biochemical composition, fatty acid profiles, blood metrics, and sex steroid hormone of male Pangasius nasutus broodstock","volume":"25","author":"Torsabo","year":"2025","journal-title":"Aquac. Stud."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1007\/s10499-026-02558-3","article-title":"Determining the age and size at sexual maturity in the sea cucumber Apostichopus japonicus","volume":"34","author":"Yan","year":"2026","journal-title":"Aquac. Int."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"8195","DOI":"10.1007\/s10499-024-01562-9","article-title":"Reproduction induces variation of digestive function in the sea cucumber Apostichopus japonicus","volume":"32","author":"Ru","year":"2024","journal-title":"Aquac. Int."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1657","DOI":"10.1111\/are.13621","article-title":"Energy budget adjustment of sea cucumber Apostichopus japonicus during breeding period","volume":"49","author":"Ru","year":"2018","journal-title":"Aquac. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"9932743","DOI":"10.1155\/are\/9932743","article-title":"Effects of temperature on reproductive performance, embryonic quality, and embryonic development of Chinese mitten crab","volume":"2025","author":"Cui","year":"2025","journal-title":"Aquac. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/0044-8486(81)90129-0","article-title":"Effects of temperature and ration on gametogenesis and growth in the tropical mussel Perna perna (L.)","volume":"22","author":"Epifanio","year":"1981","journal-title":"Aquaculture"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"735487","DOI":"10.1016\/j.aquaculture.2020.735487","article-title":"The effect of temperature on somatic and gonadal development of the sea urchin Paracentrotus lividus (Lamarck, 1816)","volume":"528","author":"Santos","year":"2020","journal-title":"Aquaculture"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1071\/MF10269","article-title":"Effects of climate change on fish reproduction and early life history stages","volume":"62","author":"Pankhurst","year":"2011","journal-title":"Mar. Freshw. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1023\/B:FISH.0000030602.51939.50","article-title":"Cold and dark or warm and light: Variations on the theme of environmental control of reproduction","volume":"28","author":"Pankhurst","year":"2003","journal-title":"Fish Physiol. Biochem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"736646","DOI":"10.1016\/j.aquaculture.2021.736646","article-title":"Physiological traits of income breeding strategy in the sea cucumber Apostichopus japonicus","volume":"539","author":"Ru","year":"2021","journal-title":"Aquaculture"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.theriogenology.2016.09.028","article-title":"Water temperature influences growth and gonad differentiation in European sea bass (Dicentrarchus labrax, L. 1758)","volume":"88","author":"Arfuso","year":"2017","journal-title":"Theriogenology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/j.aquaculture.2007.12.006","article-title":"Effect of different thermal regimes on growth and physiological performance of the sea cucumber Apostichopus japonicus Selenka","volume":"275","author":"Dong","year":"2008","journal-title":"Aquaculture"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Peng, Y., Yan, L., Zhao, C., Zhang, B., and Qiu, L. (2025). Effects of temperature and salinity on ovarian development and differences in energy metabolism between reproduction and growth during ovarian development in the Lateolabrax maculatus. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms26178295"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.aquaculture.2018.11.006","article-title":"Energy budget of cultured Paracentrotus lividus under different temperatures","volume":"501","author":"Yeruham","year":"2019","journal-title":"Aquaculture"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/S0022-0981(01)00338-0","article-title":"Environmental parameters controlling gametogenesis in the echinoid Psammechinus miliaris","volume":"266","author":"Kelly","year":"2001","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"101970","DOI":"10.1016\/j.aqrep.2024.101970","article-title":"Gametogenesis and vasa expression are seasonally regulated in yellow drum (Nibea albiflora)","volume":"35","author":"Yu","year":"2024","journal-title":"Aquac. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1007\/s10126-025-10478-1","article-title":"Early temporal dynamics of gonadal development and sexually dimorphic gene expression during sex differentiation in mandarin fish (Siniperca chuatsi)","volume":"27","author":"Rong","year":"2025","journal-title":"Mar. Biotechnol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"107476","DOI":"10.1016\/j.fishres.2025.107476","article-title":"Seasonal and sex-based variations in energy use in wild plaice: Differences in energetic costs of spawning and feeding behaviours outweigh effects of temperature on field metabolism","volume":"289","author":"Jones","year":"2025","journal-title":"Fish. Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.seares.2013.11.010","article-title":"Energy allocation and reproductive investment in a temperate protogynous hermaphrodite, the ballan wrasse Labrus bergylta","volume":"86","year":"2014","journal-title":"J. Sea Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e12278","DOI":"10.1111\/ivb.12278","article-title":"Sex-specific differences in gonopore and gonadal growth trajectories in the brooding sea urchin Abatus cavernosus (Spatangoida)","volume":"139","author":"Gil","year":"2020","journal-title":"Invertebr. Biol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Ru, X., Zhang, L., and Yang, H. (2021). Plasticity of locomotor activity permits energy homeostasis during reproduction in a female sea cucumber. Front. Mar. Sci., 8.","DOI":"10.3389\/fmars.2021.748571"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"738787","DOI":"10.1016\/j.aquaculture.2022.738787","article-title":"Examination of sex-related differences in intestinal and gonadal lipid metabolism in the sea cucumber Apostichopus japonicus","volume":"562","author":"Zhang","year":"2023","journal-title":"Aquaculture"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1007\/s10152-009-0174-7","article-title":"Males and females gonad fatty acids of the sea urchins Paracentrotus lividus and Arbacia lixula (Echinodermata)","volume":"64","author":"Pita","year":"2010","journal-title":"Helgol. Mar. Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"100936","DOI":"10.1016\/j.aqrep.2021.100936","article-title":"The male and female gonad transcriptome of the edible sea urchin Paracentrotus lividus: Identification of sex-related and lipid biosynthesis genes","volume":"22","author":"Machado","year":"2022","journal-title":"Aquac. Rep."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1007\/s10499-025-01828-w","article-title":"Integration analysis of microRNAs and mRNA reveals a regulatory mechanism in gonadal differentiation of sea cucumber Apostichopus japonicus","volume":"33","author":"Liu","year":"2025","journal-title":"Aquac. Int."},{"key":"ref_47","first-page":"100790","article-title":"Transcriptome analysis of gender-biased CYP genes in gonads of the sea cucumber Apostichopus japonicus","volume":"38","author":"Zhang","year":"2021","journal-title":"Comp. Biochem. Physiol. D Genom. Proteom."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"AQUAST2936","DOI":"10.4194\/AQUAST2936","article-title":"Cloning and expression profiles of gonadotropin \u03b2-subunits (FSH\u03b2, LH\u03b2) in female giant gourami (Osphronemus goramy) during gonadal development","volume":"26","author":"Prasetiyo","year":"2026","journal-title":"Aquac. Stud."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/16\/18\/2815\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T04:21:46Z","timestamp":1789014106000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/16\/18\/2815"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,8]]},"references-count":48,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["ani16182815"],"URL":"https:\/\/doi.org\/10.3390\/ani16182815","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,8]]}}}