{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T08:28:49Z","timestamp":1778574529255,"version":"3.51.4"},"reference-count":49,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2022,6,3]],"date-time":"2022-06-03T00:00:00Z","timestamp":1654214400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"\u201cInnovation in Fisheries\u201d EU-Greece Operational Program of Fisheries and Maritime, EPAL 2014\u20132020","award":["5029294"],"award-info":[{"award-number":["5029294"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JMSE"],"abstract":"<jats:p>Integrated multitrophic aquaculture (IMTA) is an innovative mariculture methodology that reduces the environmental footprint and increases the profitability of the farm. It combines the cultivation of species belonging to different trophic levels, simulating a natural food web. In this study, five Mediterranean species were co-cultured in three operating fish farms in the Aegean (E. Mediterranean) Sea with different trophic conditions. The co-cultivated species were sea bream (Sparus aurata), European sea bass (Dicentrarchus labrax), Mediterranean mussel (Mytilus galloprovincialis), rayed pearl oyster (Pinctada imbricata radiata), and sea cucumber (Holothuria polii). Bream, bass, and mussels were cultivated according to the traditional on-growing methods (fish cages and longlines), whereas the pearl oysters and sea cucumbers were cultivated in baskets designed specifically for oyster farms. To estimate the growth of the co-cultivated species, growth indicators were calculated using length and weight measurements. Furthermore, the growth measurements from co-cultivated species were compared to the respective ones from natural populations. All the species showed high survival rates in the integrated multitrophic aquaculture (IMTA) conditions. Pearl oysters and Mediterranean mussels had positive growth in fish farms with high concentrations of nutrients. Mussel condition index (CI) was 42% in Aquaculture 1 (Aq1) and 33% in Aquaculture 2 (Aq2), compared to 35% in a typical Mediterranean mussel farm. Pearl oysters CI in Aq1 was 53%, in Aq2 56%, in Aquaculture 3 (Aq3) 19%, and in natural populations ranging from 30% to 45%. In contrast, holothurians did not gain weight under the fish cage regime despite the high survival rate. Their final total weight was 17.3 g in Ag1, 8.3 g in Aq2, and 18.3 g in Aq3, but in the natural population, the mean weight was 80 g.<\/jats:p>","DOI":"10.3390\/jmse10060776","type":"journal-article","created":{"date-parts":[[2022,6,3]],"date-time":"2022-06-03T10:33:01Z","timestamp":1654252381000},"page":"776","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["An IMTA in Greece: Co-Culture of Fish, Bivalves, and Holothurians"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1251-0804","authenticated-orcid":false,"given":"Dimitra","family":"Chatzivasileiou","sequence":"first","affiliation":[{"name":"Marine Ecology Laboratory, Department of Biology, University of Crete, GR 70013 Heraklion, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Panagiotis D.","family":"Dimitriou","sequence":"additional","affiliation":[{"name":"Marine Ecology Laboratory, Department of Biology, University of Crete, GR 70013 Heraklion, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7127-5779","authenticated-orcid":false,"given":"John","family":"Theodorou","sequence":"additional","affiliation":[{"name":"Department of Animal Production, Fisheries & Aquaculture, University of Patras, GR 30200 Mesolonghi, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ioanna","family":"Kalantzi","sequence":"additional","affiliation":[{"name":"Hellenic Centre for Marine Research, Institute of Oceanography, GR 71500 Heraklion, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Iordanis","family":"Magiopoulos","sequence":"additional","affiliation":[{"name":"Hellenic Centre for Marine Research, Institute of Oceanography, GR 71500 Heraklion, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3039-7910","authenticated-orcid":false,"given":"Nafsika","family":"Papageorgiou","sequence":"additional","affiliation":[{"name":"Marine Ecology Laboratory, Department of Biology, University of Crete, GR 70013 Heraklion, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3557-0575","authenticated-orcid":false,"given":"Paraskevi","family":"Pitta","sequence":"additional","affiliation":[{"name":"Hellenic Centre for Marine Research, Institute of Oceanography, GR 71500 Heraklion, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manolis","family":"Tsapakis","sequence":"additional","affiliation":[{"name":"Hellenic Centre for Marine Research, Institute of Oceanography, GR 71500 Heraklion, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ioannis","family":"Karakassis","sequence":"additional","affiliation":[{"name":"Marine Ecology Laboratory, Department of Biology, University of Crete, GR 70013 Heraklion, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,6,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1016\/j.marenvres.2009.12.007","article-title":"Effects of fish farming on the biological and geochemical properties of muddy and sandy sediments in the Mediterranean Sea","volume":"69","author":"Papageorgiou","year":"2010","journal-title":"Mar. Environ. Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1016\/j.marpolbul.2005.09.034","article-title":"Benthic impacts of fish farming: Meta-analysis of community and geochemical data","volume":"52","author":"Kalantzi","year":"2006","journal-title":"Mar. Pollut. Bull."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3354\/meps07763","article-title":"Ghost nutrients\u2019 from fish farms are transferred up the food web by phytoplankton grazers","volume":"374","author":"Pitta","year":"2009","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Mansour, A.T., Ashour, M., Alprol, A.E., and Alsaqufi, A.S. (2022). Aquatic Plants and Aquatic Animals in the Context of Sustainability: Cultivation Techniques, Integration, and Blue Revolution. Sustainability, 14.","DOI":"10.3390\/su14063257"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/j.aquaculture.2018.07.051","article-title":"Application of open water integrated multi-trophic aquaculture to intensive monoculture: A review of the current status and challenges in Korea","volume":"497","author":"Park","year":"2018","journal-title":"Aquaculture"},{"key":"ref_6","first-page":"11","article-title":"The AquaNet Integrated Multi-Trophic Aquaculture Project: Rationale of the Project and Development of Kelp Cultivation as the Inorganic Extractive Component of the System","volume":"104","author":"Chopin","year":"2004","journal-title":"Bull. Aquac. Assoc. Can."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1111\/are.12234","article-title":"Suspended culture of the sea cucumber Apostichopus japonicus below a Pacific oyster raft-potential for integrated multi-trophic aquaculture","volume":"46","author":"Yokoyama","year":"2015","journal-title":"Aquac. Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1111\/raq.12147","article-title":"Role of deposit-feeding sea cucumbers in integrated multitrophic aquaculture: Progress, problems, potential and future challenges","volume":"10","author":"Zamora","year":"2018","journal-title":"Rev. Aquac."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.marpolbul.2015.04.019","article-title":"Trophic structure in a pilot system for the integrated multi-trophic aquaculture off the east coast of Korean peninsula as determined by stable isotopes","volume":"95","author":"Park","year":"2015","journal-title":"Mar. Pollut. Bull."},{"key":"ref_10","first-page":"133","article-title":"Integrated aquaculture (INTAQ) as a tool for an ecosystem approach to the marine farming sector in the Mediterranean Sea","volume":"Volume 529","author":"Angel","year":"2009","journal-title":"FAO Fisheries and Aquaculture"},{"key":"ref_11","unstructured":"Hughes, A.D., Corner, R.A., Cocchi, M., Alexander, K.A., Freeman, S., Angel, D., Chiantore, M., Gunning, D., Maguire, J., and Mendoza Beltran, A. (2016). Beyond Fish Monoculture\u2014Developing Integrated Multi-Trophic Aquaculture in Europe, AD Futura."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.aquaculture.2015.03.005","article-title":"The implications of aquaculture policy and regulation for the development of integrated multi-trophic aquaculture in Europe","volume":"443","author":"Alexander","year":"2015","journal-title":"Aquaculture"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.aquaculture.2018.10.071","article-title":"Contribution of sea cucumber Holothuria tubulosa on organic load reduction from fish farming operation","volume":"501","author":"Neofitou","year":"2019","journal-title":"Aquaculture"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"737881","DOI":"10.1016\/j.aquaculture.2021.737881","article-title":"Culturing the sea cucumber Holothuria poli in open-water integrated multi-trophic aquaculture at a coastal Mediterranean fish farm","volume":"550","author":"Cutajar","year":"2022","journal-title":"Aquaculture"},{"key":"ref_15","unstructured":"Theodorou, J.A., Makri, M., Douvi, X., Ramfos, A., and Spinos, E. (2021). Seasonal variation in the biochemical composition, condition index, and meat yield of the non-indigenous pearl oyster Pinctada imbricata radiata (Leach, 1814) from the West of the Aegean Sea, Greece. Aquac. Fish."},{"key":"ref_16","first-page":"4","article-title":"On the occurrence of rayed pearl oyster Pinctada imbricata radiata (Leach, 1814) in Western Greece (Ionian Sea) and its biofouling potential","volume":"13","author":"Theodorou","year":"2019","journal-title":"Biharean Biol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Moutopoulos, D.K., Minasidis, V., Katselis, G., Theodorou, J.A., Ziou, A., and Douligeri, A.S. (2022). Investigating the Acceptance of a New Bivalve Product in the Greek Shellfish Market: The Non-Indigenous Pearl Oyster Pinctada imbricata radiata. J. Mar. Sci. Eng., 10.","DOI":"10.3390\/jmse10020251"},{"key":"ref_18","first-page":"101821","article-title":"Biological aspects, population and fishery dynamics of the non-indigenous pearl oyster Pinctada imbricata radiata (Leach, 1814) in the Eastern Mediterranean","volume":"45","author":"Moutopoulos","year":"2021","journal-title":"Reg. Stud. Mar. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"163","DOI":"10.3354\/meps232163","article-title":"A physiological comparison between Pacific oysters Crassostrea gigas and Sydney Rock oysters Saccostrea glomerata: Food, feeding and growth in a shared estuarine habitat","volume":"232","author":"Bayne","year":"2002","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1016\/j.marpolbul.2015.09.035","article-title":"Mussel farming in Maliakos Gulf and quality indicators of the marine environment: Good benthic below poor pelagic ecological status","volume":"101","author":"Dimitriou","year":"2015","journal-title":"Mar. Pollut. Bull."},{"key":"ref_21","unstructured":"Gren, I.-M., Jonzon, Y., and Lindqvist, M. (2008). Costs of Nutrient Reductions to the Baltic Sea-Technical, Swedish University of Agricultural Sciences. Technical report."},{"key":"ref_22","unstructured":"Soto, D. (2009). Integrated Mariculture a Global Review. FAO Fisheries and Aquaculture, FAO. Technical Paper. No. 529."},{"key":"ref_23","first-page":"405","article-title":"A Practical Handbook","volume":"28","author":"Bogue","year":"1957","journal-title":"J. High. Educ."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1016\/0043-1354(84)90230-6","article-title":"An optimal manual procedure for ammonia analysis in natural waters by the indophenol blue method","volume":"18","author":"Degobbis","year":"1984","journal-title":"Water Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/0011-7471(63)90358-9","article-title":"A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence","volume":"10","author":"Yentsch","year":"1963","journal-title":"Deep. Res. Oceanogr. Abstr."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/j.ecolind.2009.04.007","article-title":"Principal component analysis: Development of a multivariate index for assessing eutrophication according to the European water framework directive","volume":"10","author":"Primpas","year":"2010","journal-title":"Ecol. Indic."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Dimitriou, P.D., Papageorgiou, N., Arvanitidis, C., Assimakopoulou, G., Pagou, K., Papadopoulou, K.N., Pavlidou, A., Pitta, P., Reizopoulou, S., and Simboura, N. (2015). One step forward: Benthic pelagic coupling and indicators for environmental status. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0141071"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.ecolind.2005.03.006","article-title":"A synthesis of the biological quality elements for the implementation of the European Water Framework Directive in the Mediterranean ecoregion: The case of Saronikos Gulf","volume":"5","author":"Simboura","year":"2005","journal-title":"Ecol. Indic."},{"key":"ref_29","first-page":"15","article-title":"Morphometry and condition index in Mediterranean mussels (Mytilus galloprovincialis Lamrck, 1819) from Boka Kotorska Bay (Montenegro, Southeast Adriatic Sea)","volume":"33","author":"Gvozdenovic","year":"2020","journal-title":"Stud. Mar."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"859","DOI":"10.2983\/035.030.0327","article-title":"Production and marketing trends of the cultured mediterranean mussel Mytilus galloprovincialis lamarck 1819, in Greece","volume":"30","author":"Theodorou","year":"2011","journal-title":"J. Shellfish Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1080\/13657305.2019.1708994","article-title":"Semi-quantitative risk assessment of Mediterranean mussel (Mytilus galloprovincialis L.) harvesting bans due to harmful algal bloom (HAB) incidents in Greece","volume":"24","author":"Theodorou","year":"2020","journal-title":"Aquac. Econ. Manag."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/S0044-8486(97)00206-8","article-title":"Seasonal variations in the meat weight, condition index and biochemical composition of mussels (Mytilus edulis L.) in suspended culture in two Scottish sea lochs","volume":"159","author":"Stirling","year":"1998","journal-title":"Aquaculture"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"441","DOI":"10.2478\/oandhs-2021-0038","article-title":"Effects of seasonal changes and depth on growth parameters of the Mediterranean mussel (Mytilus galloprovincialis) on a shipwreck in the Eastern Mediterranean Sea","volume":"50","author":"Karadal","year":"2021","journal-title":"Oceanol. Hydrobiol. Stud."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1111\/are.14870","article-title":"Effects of environmental factors and food availability in Northern Aegean sea on the cultivation of Mediterranean Mussels (Mytilus galloprovincialis)","volume":"52","author":"Keskin","year":"2021","journal-title":"Aquac. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"371","DOI":"10.3354\/aei00236","article-title":"Simulation of mussel Mytilus galloprovincialis growth with a dynamic energy budget model in Maliakos and Thermaikos Gulfs (Eastern mediterranean)","volume":"9","author":"Hatzonikolakis","year":"2017","journal-title":"Aquac. Environ. Interact."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1590\/1678-4162-12002","article-title":"Growth and survival of the native oyster Crassostrea gasar cultured under different stocking densities in two grow-out systems in tropical climate","volume":"73","author":"Macedo","year":"2021","journal-title":"Arq. Bras. De Med. Vet. E Zootec."},{"key":"ref_37","first-page":"265","article-title":"Seasonal Variation in the Length-Weight Relationships and Condition Factor of Four Commercially Important Sea Cucumbers Species from Karachi Coast\u2014Northern Arabian Sea","volume":"3","author":"Ahmed","year":"2018","journal-title":"Nat. Eng. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.aquaculture.2012.10.022","article-title":"Growth and food source of the sea cucumber Apostichopus japonicus cultured below fish cages\u2014Potential for integrated multi-trophic aquaculture","volume":"372\u2013375","author":"Yokoyama","year":"2013","journal-title":"Aquaculture"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"22150","DOI":"10.1038\/s41598-020-78876-0","article-title":"Epidemiology of a SKin Ulceration Disease (SKUD) in the sea cucumber Holothuria scabra with a review on the SKUDs in Holothuroidea (Echinodermata)","volume":"10","author":"Delroisse","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"339","DOI":"10.3354\/aei00361","article-title":"Site selection of mussel mitigation cultures in relation to efficient nutrient compensation of fish farming","volume":"12","author":"Maar","year":"2020","journal-title":"Aquac. Environ. Interact."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/S0044-8486(99)00102-7","article-title":"Filtration by the pearl oyster, Pinctada margaritifera, under conditions of low seston load and small particle size in a tropical lagoon habitat","volume":"176","author":"Pouvreau","year":"1999","journal-title":"Aquaculture"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2961","DOI":"10.1016\/j.dsr2.2005.08.012","article-title":"Biological response to P addition in the Eastern Mediterranean Sea. The microbial race against time","volume":"52","author":"Pitta","year":"2005","journal-title":"Deep. Res. Part II Top. Stud. Oceanogr."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1093\/plankt\/fbab053","article-title":"Relationships of pelagic ciliates with the microbial food web components at a coastal station in the oligotrophic Eastern Mediterranean Sea: Temporal and vertical variability","volume":"43","author":"Romano","year":"2021","journal-title":"J. Plankton Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"301","DOI":"10.3354\/meps152301","article-title":"Ingestion of a bacterivorous ciliate by the oyster Crassostrea gigas: Protozoa as a trophic link between picoplankton and benthic suspension-feeders","volume":"152","author":"Hassen","year":"1997","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"31","DOI":"10.3354\/meps10520","article-title":"Plankton response to nutrient enrichment is maximized at intermediate distances from fish farms","volume":"493","author":"Tsagaraki","year":"2013","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_46","first-page":"749","article-title":"Sea cucumber (Holothuria tubulosa Gmelin, 1790) culture under marine fish net cages for potential use in integrated multi-trophic aquaculture (IMTA)","volume":"46","author":"Tolon","year":"2017","journal-title":"Indian J. Geo-Mar. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"142843","DOI":"10.1016\/j.scitotenv.2020.142843","article-title":"Fish farming, metals and antibiotics in the eastern Mediterranean Sea: Is there a threat to sediment wildlife?","volume":"764","author":"Kalantzi","year":"2021","journal-title":"Sci. Total Environ."},{"key":"ref_48","first-page":"523","article-title":"Sexual Cycle of Three Commercially Important Holothurian Species (Echinodermata) from the Lagoon of New Caledonia","volume":"31","author":"Conand","year":"1981","journal-title":"Bull. Mar. Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.aquaculture.2018.09.024","article-title":"The effect of resource quality on the growth of Holothuria scabra during aquaculture waste bioremediation","volume":"499","author":"Robinson","year":"2019","journal-title":"Aquaculture"}],"container-title":["Journal of Marine Science and Engineering"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-1312\/10\/6\/776\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:24:19Z","timestamp":1760138659000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-1312\/10\/6\/776"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,3]]},"references-count":49,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2022,6]]}},"alternative-id":["jmse10060776"],"URL":"https:\/\/doi.org\/10.3390\/jmse10060776","relation":{},"ISSN":["2077-1312"],"issn-type":[{"value":"2077-1312","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,3]]}}}