{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T04:20:07Z","timestamp":1772252407934,"version":"3.50.1"},"reference-count":67,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2021,3,14]],"date-time":"2021-03-14T00:00:00Z","timestamp":1615680000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>The seaweed Asparagopsis armata exhibits a strong invasive behavior, producing halogenated compounds with effective biological effects. This study addresses the biochemical responses to sublethal concentrations of A. armata exudate on the marine snail Gibbula umbilicalis whole body and the shrimp Palaemon elegans eyes and hepatopancreas. Antioxidant defenses superoxide dismutase (SOD) and glutathione-S-transferase (GST), oxidative damage endpoints lipid peroxidation (LPO) and DNA damage, the neuronal parameter acetylcholinesterase (AChE), and the fatty acid profile were evaluated. Results revealed different metabolic responses in both species. Despite previous studies indicating that the exudate affected G. umbilicalis\u2019 survival and behavior, this does not seem to result from oxidative stress or neurotoxicity. For P. elegans, the inhibition of AChE and the decrease of antioxidant capacity is concomitant with the increase of LPO, suggesting neurotoxicity and oxidative stress as contributor mechanisms of toxicity for this species. Fatty acid profile changes were more pronounced for P. elegans with a general increase in polyunsaturated fatty acids (PUFAs) with the exudate exposure, which commonly means a defense mechanism protecting from membrane disruption. Nonetheless, the omega-3 PUFAs arachidonic acid (ARA) and docosapentaenoic acid (DPA) increased in both invertebrates, indicating a common regulation mechanism of inflammation and immunity responses.<\/jats:p>","DOI":"10.3390\/biology10030223","type":"journal-article","created":{"date-parts":[[2021,3,14]],"date-time":"2021-03-14T22:13:10Z","timestamp":1615759990000},"page":"223","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Asparagopsis armata Exudate Cocktail: The Quest for the Mechanisms of Toxic Action of an Invasive Seaweed on Marine Invertebrates"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4613-1132","authenticated-orcid":false,"given":"Carla O.","family":"Silva","sequence":"first","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Instituto Polit\u00e9cnico de Leiria, 2520-641 Peniche, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6107-9790","authenticated-orcid":false,"given":"Tiago","family":"Sim\u00f5es","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Instituto Polit\u00e9cnico de Leiria, 2520-641 Peniche, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4766-3736","authenticated-orcid":false,"given":"Rafael","family":"F\u00e9lix","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Instituto Polit\u00e9cnico de Leiria, 2520-641 Peniche, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0879-9470","authenticated-orcid":false,"given":"Amadeu M.V.M.","family":"Soares","sequence":"additional","affiliation":[{"name":"Department of Biology and CESAM (Centre for Environmental and Marine Studies), University of Aveiro, 3810-193 Aveiro, Portugal"}]},{"given":"Carlos","family":"Barata","sequence":"additional","affiliation":[{"name":"Environmental Chemistry Department, Institute of Environmental Assessment and Water Research (IDAEA) Consejo Superior de Investigaciones Cient\u00edficas (CSIC), Jordi Girona 18-26, 08034 Barcelona, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1306-3396","authenticated-orcid":false,"given":"Sara C.","family":"Novais","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Instituto Polit\u00e9cnico de Leiria, 2520-641 Peniche, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9887-1864","authenticated-orcid":false,"given":"Marco F.L.","family":"Lemos","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Instituto Polit\u00e9cnico de Leiria, 2520-641 Peniche, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2021,3,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/S0045-6535(03)00207-8","article-title":"The diversity of naturally produced organohalogens","volume":"52","author":"Gribble","year":"2003","journal-title":"Chemosphere"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Amsler, C.D. (2008). Algal Chemical Ecology, Springer.","DOI":"10.1007\/978-3-540-74181-7"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/0031-9422(77)80067-8","article-title":"Halogen chemistry of the red alga Asparagopsis","volume":"16","author":"McConnell","year":"1977","journal-title":"Phytochemistry"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1111\/j.1529-8817.2006.00226.x","article-title":"Ultrastructure of the gland cells of the red alga Asparagopsis armata (Bonnemaisoniaceae","volume":"42","author":"Paul","year":"2006","journal-title":"J. Phycol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"87","DOI":"10.3354\/meps306087","article-title":"Chemical defence against bacteria in the red alga Asparagopsis armata: Linking structure with function","volume":"306","author":"Paul","year":"2006","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3354\/meps323001","article-title":"Seaweed\u2013herbivore interactions at a small scale: Direct tests of feeding deterrence by filamentous algae","volume":"323","author":"Paul","year":"2006","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"107463","DOI":"10.1016\/j.ecolind.2021.107463","article-title":"The effects of the invasive seaweed Asparagopsis armata on native rock pool communities: Evidences from experimental exclusion","volume":"125","author":"Silva","year":"2021","journal-title":"Ecol. Indic."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Silva, C.O., Novais, S.C., Soares, A.M.V.M., Barata, C., and Lemos, M.F.L. (2021). Impacts of the Invasive Seaweed Asparagopsis armata Exudate on Energetic Metabolism of Rock Pool Invertebrates. Toxins, 13.","DOI":"10.3390\/toxins13010015"},{"key":"ref_9","first-page":"237","article-title":"Allelochemistry in marine macroalgae","volume":"5","author":"Harlin","year":"1996","journal-title":"Crit. Rev. Toxicol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"874","DOI":"10.1046\/j.1529-8817.2003.02157.x","article-title":"Are \u201cgreen tides\u201d harmful algal blooms? Toxic properties of water-soluble extracts from two bloom-forming macroalgae, Ulva fenestrata and Ulvaria obscura (Ulvophyceae)","volume":"39","author":"Nelson","year":"2003","journal-title":"J. Phycol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Gaud\u00eancio, M.J., and Guerra, M.T. (1987). Preliminary observations on Gibbula umbilicalis (da Costa, 1778) on the Portuguese coast. Long-Term Changes in Coastal Benthic Communities, Springer.","DOI":"10.1007\/978-94-009-4049-9_3"},{"key":"ref_12","first-page":"427","article-title":"Oxidative stress in aquatic organisms in relation to pollution and aquaculture","volume":"154","author":"Livingstone","year":"2003","journal-title":"Rev. De Med. Vet."},{"key":"ref_13","unstructured":"Huggett, R.J., Kimerly, R.A., Mehrle, P.M., and Bergman, H.L. (1992). Molecular responses to environmental contamination: Enzyme and protein systems as indicators of chemical exposure and effect. Biomarkers: Biochemical, Physiological and Histological Markers of Anthropogenic Stress, Lewis Publishers."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.gene.2003.12.027","article-title":"Response of the Pacific oyster Crassostrea gigas to hydrocarbon contamination under experimental conditions","volume":"329","author":"Boutet","year":"2004","journal-title":"Gene"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.aquatox.2003.07.004","article-title":"Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna","volume":"66","author":"Barata","year":"2004","journal-title":"Aquat. Toxicol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/j.chemosphere.2019.01.018","article-title":"Amitraz toxicity to the midge Chironomus riparius: Life-history and biochemical responses","volume":"221","author":"Monteiro","year":"2019","journal-title":"Chemosphere"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"108570","DOI":"10.1016\/j.cbpc.2019.108570","article-title":"Linking cholinesterase inhibition with behavioural changes in the sea snail Gibbula umbilicalis: Effects of the organophosphate pesticide chlorpyrifos","volume":"225","author":"Silva","year":"2019","journal-title":"Comp. Biochem. Physiol. Part C Toxicol. Pharmacol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1016\/j.ecolind.2016.03.044","article-title":"Fatty acid profiling as bioindicator of chemical stress in marine organisms: A review","volume":"67","author":"Filimonova","year":"2016","journal-title":"Ecol. Indic."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1016\/j.scitotenv.2017.02.015","article-title":"Fatty acid profile of the sea snail Gibbula umbilicalis as a biomarker for coastal metal pollution","volume":"586","author":"Silva","year":"2017","journal-title":"Sci. Total Environ."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1016\/j.ecolind.2017.09.046","article-title":"Using biomarkers to address the impacts of pollution on limpets (Patella depressa) and their mechanisms to cope with stress","volume":"95","author":"Silva","year":"2018","journal-title":"Ecol. Indic."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.ecolind.2015.01.031","article-title":"Biochemical and populational responses of an aquatic bioindicator species, Daphnia longispina, to a commercial formulation of a herbicide (Primextra\u00ae Gold TZ) and its active ingredient (S-metolachlor)","volume":"53","author":"Neves","year":"2015","journal-title":"Ecol. Indic."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1002\/pmic.200900470","article-title":"Proteins in ecotoxicology\u2013how, why and why not?","volume":"10","author":"Lemos","year":"2010","journal-title":"Proteomics"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1016\/j.chemosphere.2014.07.016","article-title":"Sensitivity of the sea snail Gibbula umbilicalis to mercury exposure\u2013linking endpoints from different biological organization levels","volume":"119","author":"Cabecinhas","year":"2015","journal-title":"Chemosphere"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"936","DOI":"10.1016\/j.chemosphere.2012.06.036","article-title":"Swimming velocity, avoidance behavior and biomarkers in Palaemon serratus exposed to fenitrothion","volume":"90","author":"Oliveira","year":"2013","journal-title":"Chemosphere"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.aquatox.2006.01.011","article-title":"Cholinesterase from the common prawn (Palaemon serratus) eyes: Catalytic properties and sensitivity to organophosphate and carbamate compounds","volume":"77","author":"Frasco","year":"2006","journal-title":"Aquat. Toxicol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"7130","DOI":"10.1016\/S0021-9258(19)42083-8","article-title":"Glutathione S-transferases the first enzymatic step in mercapturic acid formation","volume":"249","author":"Habig","year":"1974","journal-title":"J. Biol. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1023\/A:1025457831923","article-title":"Effects of dimethoate and beta-naphtho flavone on selected biomarkers of Poecilia reticulata","volume":"26","author":"Frasco","year":"2002","journal-title":"Fish Physiol. Biochem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"6049","DOI":"10.1016\/S0021-9258(18)63504-5","article-title":"Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein)","volume":"244","author":"McCord","year":"1969","journal-title":"J. Biol. Chem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/0003-2697(79)90738-3","article-title":"Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction","volume":"95","author":"Ohkawa","year":"1979","journal-title":"Anal. Biochem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/S0076-6879(84)05038-2","article-title":"Comparative studies on different methods of malonaldehyde determination","volume":"Volume 105","author":"Bird","year":"1984","journal-title":"Methods in Enzymology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1016\/S0025-326X(02)00142-X","article-title":"Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil","volume":"44","author":"Torres","year":"2002","journal-title":"Mar. Pollut. Bull."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1002\/em.2850110409","article-title":"DNA Precipitation Assay: A Rapid and Simple Method for Detecting DNA Damage in Mammalian Cells","volume":"11","author":"Olive","year":"1988","journal-title":"Environ. Mol. Mutagenesis"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/S0166-445X(99)00094-6","article-title":"Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada)","volume":"50","author":"Blaise","year":"2000","journal-title":"Aquat. Toxicol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/0006-2952(61)90145-9","article-title":"A new and rapid colorimetric determination of acetylcholinesterase activity","volume":"7","author":"Ellman","year":"1961","journal-title":"Biochem. Pharmacol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Guo, X. (2014). Advances in Gas Chromatography, BoD\u2013Books on Demand.","DOI":"10.5772\/57016"},{"key":"ref_37","unstructured":"(2020, November 01). R: A Language and Environment for Statistical Computing, Available online: https:\/\/www.R-project.org\/."},{"key":"ref_38","unstructured":"(2020, November 01). RStudio: Integrated Development for R, Available online: http:\/\/www.rstudio.com\/."},{"key":"ref_39","unstructured":"Pohlert, T. (2020, November 01). PMCMR: Calculate Pairwise Multiple Comparisons of Mean Rank Sums. Available online: http:\/\/CRAN.R-project.org\/package=PMCMR."},{"key":"ref_40","unstructured":"Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., and Stevens, M.H.H. (2020, November 01). Package \u2018Vegan\u2019. Available online: https:\/\/CRAN.R-project.org\/package=vegan."},{"key":"ref_41","unstructured":"Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., and Hornik, K. (2020, November 01). Cluster: Cluster Analysis Basics and Extensions, Available online: https:\/\/CRAN.R-project.org\/package=cluster."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0065-2296(05)43004-9","article-title":"Stress resistance and disease resistance in seaweeds: The role of reactive oxygen metabolism","volume":"43","author":"Dring","year":"2005","journal-title":"Adv. Bot. Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1016\/j.cbpc.2007.02.014","article-title":"Effects of copper and cadmium on cholinesterase and glutathione S-transferase activities of two marine gastropods (Monodonta lineata and Nucella lapillus)","volume":"145","author":"Cunha","year":"2007","journal-title":"Comp. Biochem. Physiol. Part C Toxicol. Pharmacol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/0020-1790(91)90001-U","article-title":"Glutathione S-transferase activities in phytophagous insects: Induction and inhibition by plant phototoxins and phenols","volume":"21","author":"Lee","year":"1991","journal-title":"Insect Biochem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1038\/s41514-017-0013-z","article-title":"How does hormesis impact biology, toxicology, and medicine?","volume":"3","author":"Calabrese","year":"2017","journal-title":"NPJ Aging Mech. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1093\/toxsci\/kfh007","article-title":"Nonmonotonic Dose-Response Relationships: Mechanistic Basis, Kinetic Modeling, and Implications for Risk Assessment","volume":"77","author":"Conolly","year":"2004","journal-title":"Toxicol. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.aquatox.2018.08.008","article-title":"Oxidative stress responses and cellular energy allocation changes in microalgae following exposure to widely used human antibiotics","volume":"203","author":"Aderemi","year":"2018","journal-title":"Aquat. Toxicol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.scitotenv.2016.04.091","article-title":"Effects of ocean acidification on the swimming ability, development and biochemical responses of sand smelt larvae","volume":"563","author":"Silva","year":"2016","journal-title":"Sci. Total Environ."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"760","DOI":"10.1007\/BF01700998","article-title":"Effect of fluoride on acetylcholinesterase activity and oxygen consumption in a freshwater field crab, Barytelphusa guerini","volume":"45","author":"Reddy","year":"1990","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1016\/j.ecoenv.2006.11.020","article-title":"Honeybee Apis mellifera acetylcholinesterase\u2014a biomarker to detect deltamethrin exposure","volume":"69","author":"Badiou","year":"2008","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1016\/j.neuro.2004.01.002","article-title":"The modulatory effect of pyrethroids on acetylcholine release in the hippocampus of freely moving rats","volume":"25","author":"Hossain","year":"2004","journal-title":"Neurotoxicology"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1111\/j.1432-1033.1991.tb15776.x","article-title":"Phosphatidylinositol-specific Phospholipase C induces biosynthesis of acetylcholinesterase via diacylglycerol in Schistosoma mansoni","volume":"195","author":"Espinoza","year":"1991","journal-title":"Eur. J. Biochem."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2019","DOI":"10.1016\/S1001-0742(11)61030-9","article-title":"Characterisation of acute toxicity, genotoxicity and oxidative stress posed by textile effluent on zebrafish","volume":"24","author":"Zhang","year":"2012","journal-title":"J. Environ. Sci."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Hampel, M., Blasco, J., and Mart\u00edn D\u00edaz, M.L. (2016). Biomarkers and Effects. Marine Ecotoxicology: Current Knowledge and Future Issues, Elsevier.","DOI":"10.1016\/B978-0-12-803371-5.00005-9"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1016\/j.cbpc.2008.10.107","article-title":"Antioxidant response of the bivalve Pinna nobilis colonised by invasive red macroalgae Lophocladia lallemandii","volume":"149","author":"Box","year":"2009","journal-title":"Comp. Biochem. Physiol. Part C Toxicol. Pharmacol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1080\/14786410802156036","article-title":"Cholinesterase inhibitors from Sargassum and Gracilaria gracilis: Seaweeds inhabiting South Indian coastal areas (Hare Island, Gulf of Mannar)","volume":"23","author":"Natarajan","year":"2009","journal-title":"Nat. Prod. Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1687","DOI":"10.3109\/13880209.2015.1123278","article-title":"Methanol extracts from Cystoseira tamariscifolia and Cystoseira nodicaulis are able to inhibit cholinesterases and protect a human dopaminergic cell line from hydrogen peroxide-induced cytotoxicity","volume":"54","author":"Silvestre","year":"2016","journal-title":"Pharm. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1007\/s12011-013-9727-3","article-title":"Changes of blue mussels Mytilus edulis L. lipid composition under cadmium and copper toxic effect","volume":"154","author":"Fokina","year":"2013","journal-title":"Biol. Trace Elem. Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"22197","DOI":"10.1007\/s11356-019-05492-5","article-title":"Redox status and fatty acid composition of Mactra corallina digestive gland following exposure to acrylamide","volume":"26","author":"Trabelsi","year":"2019","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.envpol.2007.12.010","article-title":"Chronic copper exposure and fatty acid composition of the amphipod Dikerogammarus villosus: Results from a field study","volume":"156","author":"Maazouzi","year":"2008","journal-title":"Environ. Pollut."},{"key":"ref_61","unstructured":"Vance, D.E., and Vance, J.E. (2002). Biochemistry of Lipids, Lipoproteins and Membranes, Elsevier. [4th ed.]."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.plipres.2010.07.004","article-title":"Docosapentaenoic acid (22:5n-3): A review of its biological effects","volume":"50","author":"Kaur","year":"2011","journal-title":"Prog. Lipid Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"233","DOI":"10.4010\/jln.19.233","article-title":"Marine omega-3 fatty acids and inflammation","volume":"19","author":"Calder","year":"2010","journal-title":"J. Lipid Nutr."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1007\/s11745-006-5006-9","article-title":"Impact of 20: 4n-6 supplementation on the fatty acid composition and hemocyte parameters of the pacific oyster Crassostrea gigas","volume":"41","author":"Delaporte","year":"2006","journal-title":"Lipids"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1080\/07315724.2002.10719248","article-title":"Omega-3 fatty acids in inflammation and autoimmune diseases","volume":"21","author":"Simopoulos","year":"2002","journal-title":"J. Am. Coll. Nutr."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1007\/s11745-997-0090-4","article-title":"Heneicosapentaenoate (21: 5n-3): Its incorporation into lipids and its effects on arachidonic acid and eicosanoid synthesis","volume":"32","author":"Larsen","year":"1997","journal-title":"Lipids"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1111\/j.1600-0897.2011.01089.x","article-title":"Short-chain fatty acids induce pro-inflammatory cytokine production alone and in combination with toll-like receptor ligands","volume":"67","author":"Mirmonsef","year":"2012","journal-title":"Am. J. Reprod. Immunol."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/10\/3\/223\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:35:36Z","timestamp":1760160936000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/10\/3\/223"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,14]]},"references-count":67,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2021,3]]}},"alternative-id":["biology10030223"],"URL":"https:\/\/doi.org\/10.3390\/biology10030223","relation":{"has-preprint":[{"id-type":"doi","id":"10.20944\/preprints202010.0133.v1","asserted-by":"object"}]},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,14]]}}}