{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,6]],"date-time":"2026-06-06T19:26:51Z","timestamp":1780774011340,"version":"3.54.1"},"reference-count":31,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2021,12,30]],"date-time":"2021-12-30T00:00:00Z","timestamp":1640822400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the National Natural Science Foundation of China (NSFC)","award":["Grant Nos. 41576159, 41776125"],"award-info":[{"award-number":["Grant Nos. 41576159, 41776125"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>The mixotrophic dinoflagellate Akashiwo sanguinea frequently forms harmful algal blooms around the world and has caused massive deaths of shellfish, finfish and birds, yet its toxic mechanism is still unclear. In this study, toxic effects of A. sanguinea on co-culturing phytoplankton and zooplankton were investigated. The results showed that sonicated cultures of A. sanguinea JX13 and JX14, isolated from the Pearl River Estuary, had a significant lethal effect on the rotifer Brachionus plicatilis, with the highest mortality rate of 80%. The highest inhibition rates of A. sanguinea cultures JX13 (90%) and JX14 (80%) on R. salina were much higher than that of AS2 (20%). Toxicity varied with the growth stage, during which A. sanguinea cells in the exponential stage showed the highest toxicity (40%), while A. sanguinea filtrate had the highest toxicity (10%) in the decline stage. The action mode of A. sanguinea toxicity on plankton was explored through an osmotic membrane culture device. It was found that A. sanguinea JX13 displayed an inhibitory effect on coexisting phytoplankton, whether they had contact or not, but the inhibition rate increased by 25% with contact. A lethal effect of A. sanguinea JX13 on rotifer Brachionus plicatilis was observed only in contact treatment. This study suggests that direct contact is the key action mode to trigger the release of toxins and induce toxic effects of A. sanguinea on co-occurring plankton.<\/jats:p>","DOI":"10.3390\/ijerph19010404","type":"journal-article","created":{"date-parts":[[2021,12,30]],"date-time":"2021-12-30T21:41:21Z","timestamp":1640900481000},"page":"404","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Toxic Characteristics and Action Mode of the Mixotrophic Dinoflagellate Akashiwo sanguinea on Co-Occurring Phytoplankton and Zooplankton"],"prefix":"10.3390","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7677-8746","authenticated-orcid":false,"given":"Xiaoer","family":"Wu","sequence":"first","affiliation":[{"name":"Institute of Hydrobiology, Jinan University, Guangzhou 510632, China"},{"name":"Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China"},{"name":"Marine Resources Big Data Center of South China Sea, Southern Marine Science and Engineering Guangdong Laboratory, Zhanjiang 524013, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Yang","sequence":"additional","affiliation":[{"name":"Institute of Hydrobiology, Jinan University, Guangzhou 510632, China"},{"name":"Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yeyin","family":"Yang","sequence":"additional","affiliation":[{"name":"Institute of Hydrobiology, Jinan University, Guangzhou 510632, China"},{"name":"Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ping","family":"Zhong","sequence":"additional","affiliation":[{"name":"Institute of Hydrobiology, Jinan University, Guangzhou 510632, China"},{"name":"Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ning","family":"Xu","sequence":"additional","affiliation":[{"name":"Institute of Hydrobiology, Jinan University, Guangzhou 510632, China"},{"name":"Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,12,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.jembe.2006.09.013","article-title":"Effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea","volume":"342","author":"Matsubara","year":"2007","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.hal.2015.10.005","article-title":"Effects of nitrogenous nutrition on growth and nitrogen assimilation enzymes of dinoflagellate Akashiwo sanguinea","volume":"50","author":"Liu","year":"2015","journal-title":"Harmful Algae"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1111\/jpy.12274","article-title":"Sexual resting cyst production by the dinoflagellate Akashiwo sanguinea: A potential mechanism contributing to the ubiquitous distribution of a harmful alga","volume":"51","author":"Tang","year":"2015","journal-title":"J. Phycol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/0025-326X(92)90223-S","article-title":"Harmful algal blooms in the Australian region","volume":"25","author":"Hallegraeff","year":"1992","journal-title":"Mar. Poll. Bull."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1076","DOI":"10.4319\/lo.1997.42.5_part_2.1076","article-title":"Harmful algal blooms and red tide problems on the US west coast","volume":"42","author":"Horner","year":"1997","journal-title":"Limnol. Oceanogr."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1016\/j.crvi.2008.06.005","article-title":"The impact of the 2003 summer heat wave and the 2005 late cold wave on the phytoplankton in the north-eastern English Channel","volume":"331","author":"Souissi","year":"2008","journal-title":"Comptes Rendus Biologies"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1029\/2004EO450002","article-title":"MODIS detects a devastating algal bloom in Paracas Bay, Peru","volume":"85","author":"Kahru","year":"2004","journal-title":"Eos Trans. AGU"},{"key":"ref_8","first-page":"159","article-title":"Evolution and causes of formation of Gymnodinium sanguineum bloom in Yantai Sishili Bay","volume":"32","author":"Wu","year":"2000","journal-title":"Oceanol. Limnol. Sin."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1023\/B:HYDR.0000020331.75003.18","article-title":"Harmful algal bloom causative collected from Hong Kong waters","volume":"512","author":"Lu","year":"2004","journal-title":"Hydrobiologia"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Jessup, D.A., Miller, M.A., Ryan, J.P., Nevins, H.M., Kerkering, H.A., Mekebri, A., Crane, D.B., Johnson, T.A., and Kudela, R.M. (2009). Mass stranding of marine birds caused by a surfactant-producing red tide. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0004550"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.hal.2014.05.004","article-title":"Large-scale bloom of Akashiwo sanguinea in the Northern California current system in 2009","volume":"37","author":"White","year":"2014","journal-title":"Harmful Algae"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"110652","DOI":"10.1016\/j.marpolbul.2019.110652","article-title":"Akashiwo sanguinea blooms in Chinese waters in 1998\u20132017","volume":"149","author":"Chen","year":"2019","journal-title":"Mar. Poll. Bull."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"197","DOI":"10.4490\/algae.2014.29.3.197","article-title":"Akashiwo sanguinea (Dinophyceae) extruding mucous from pores on the cell surface","volume":"29","author":"Badylak","year":"2014","journal-title":"Algae"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1111\/j.1749-7345.1990.tb00529.x","article-title":"A review of the effects of algal blooms on shellfish and aquaculture","volume":"21","author":"Shumway","year":"1990","journal-title":"J. World Aquacult. Soc."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"209","DOI":"10.3354\/ame01846","article-title":"Acute toxicity of the cosmopolitan bloom-forming dinoflagellate Akashiwo sanguinea to finfish, shellfish, and zooplankton","volume":"80","author":"Xu","year":"2017","journal-title":"Aquat. Microb. Ecol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1007\/s00343-020-0132-4","article-title":"Allelopathic effects of mixotrophic dinoflagellate Akashiwo sanguinea on co-occurring phytoplankton: The significance of nutritional ecology","volume":"39","author":"Yang","year":"2021","journal-title":"J. Ocean. Limnol."},{"key":"ref_17","first-page":"66","article-title":"Hemolytic toxicity of three important harmful microalgae isolated from Pearl River Estuary","volume":"13","author":"Ding","year":"2018","journal-title":"Asian J. Ecotoxicol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"19","DOI":"10.3354\/meps08537","article-title":"Allelopathic effects of Cochlodinium polykrikoides isolates and blooms from the estuaries of Long Island, New York, on co-occurring phytoplankton","volume":"406","author":"Tang","year":"2010","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Smith, W.L., and Chanley, M.H. (1975). Culture of phytoplankton for feeding marine invertebrates. Culture of Marine Invertebrate Animals, Springer.","DOI":"10.1007\/978-1-4615-8714-9"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1080\/20026491051695","article-title":"The effects of harmful algal blooms on aquatic organisms","volume":"10","author":"Landsberg","year":"2002","journal-title":"Rev. Fish Sci."},{"key":"ref_21","first-page":"625","article-title":"Effects of Akashiwo sanguinea-dominated algal blooms on the plankton community as observed from the coastal waters of southern Zhejiang, China","volume":"37","author":"Shen","year":"2018","journal-title":"Mar. Environ. Sci."},{"key":"ref_22","first-page":"321","article-title":"Effects of temperature, light intensity and nutrient condition on the growth and hemolytic activity of six species of typical ichthyotoxic algae","volume":"34","author":"Cao","year":"2015","journal-title":"Mar. Environ. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"29","DOI":"10.3354\/ame01724","article-title":"Ability of the marine diatoms Pseudo-nitzschia multiseries and P. pungens to inhibit the growth of co-occurring phytoplankton via allelopathy","volume":"74","author":"Xu","year":"2015","journal-title":"Aquat. Microb. Ecol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1007\/BF00350065","article-title":"Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay","volume":"116","author":"Bockstahler","year":"1993","journal-title":"Mar. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.hal.2008.08.019","article-title":"The potential role of anthropogenically derived nitrogen in the growth of harmful algae in California, USA","volume":"8","author":"Kudela","year":"2008","journal-title":"Harmful Algae"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"133","DOI":"10.3354\/ame040133","article-title":"Feeding by phototrophic red-tide dinoflagellates: Five species newly revealed and six species previously known to be mixotrophic","volume":"40","author":"Jeong","year":"2005","journal-title":"Aquat. Microb. Ecol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1926","DOI":"10.1038\/ismej.2012.29","article-title":"Marine microalgae attack and feed on metazoans","volume":"6","author":"Berge","year":"2012","journal-title":"ISME J."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"101926","DOI":"10.1016\/j.hal.2020.101926","article-title":"Contact micropredation may play a more important role than exotoxicity does in the lethal effects of Karlodinium australe blooms: Evidence from laboratory bioassays","volume":"99","author":"Song","year":"2020","journal-title":"Harmful Algae"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2082","DOI":"10.1073\/pnas.0912254107","article-title":"A dinoflagellate exploits toxins to immobilize prey prior to ingestion","volume":"107","author":"Sheng","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1038\/nature01008","article-title":"Pfiesteria shumwayae kills fish by micropredation not exotoxin secretion","volume":"418","author":"Vogelbein","year":"2002","journal-title":"Nature"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2601","DOI":"10.1007\/s00227-009-1285-z","article-title":"Cochlodinium polykrikoides blooms and clonal isolates from the northwest Atlantic coast cause rapid mortality in larvae of multiple bivalve species","volume":"156","author":"Tang","year":"2009","journal-title":"Mar. Biol."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/1\/404\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:56:24Z","timestamp":1760169384000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/1\/404"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,30]]},"references-count":31,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,1]]}},"alternative-id":["ijerph19010404"],"URL":"https:\/\/doi.org\/10.3390\/ijerph19010404","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,12,30]]}}}