ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Amphidinium stirisquamtum sp. nov. (Dinophyceae), a new marine sand-dwelling dinoflagellate with a novel type of body scale

  • Luo, Zhaohe (Third Institute of Oceanography, Ministry of Natural Resources) ;
  • Wang, Na (Third Institute of Oceanography, Ministry of Natural Resources) ;
  • Mohamed, Hala F. (Third Institute of Oceanography, Ministry of Natural Resources) ;
  • Liang, Ye (School of Marine Sciences, Nanjing University of Information Science and Technology) ;
  • Pei, Lulu (Third Institute of Oceanography, Ministry of Natural Resources) ;
  • Huang, Shuhong (Third Institute of Oceanography, Ministry of Natural Resources) ;
  • Gu, Haifeng (Third Institute of Oceanography, Ministry of Natural Resources)
  • Received : 2021.04.14
  • Accepted : 2021.08.27
  • Published : 2021.12.15
Download PDF
⟨ Previous Next ⟩

Abstract

Amphidinium species are amongst the most abundant benthic dinoflagellates in marine intertidal sandy ecosystems. Some of them produce a variety of bioactive compounds that have both harmful effects and pharmaceutical potential. In this study, Amphidinium cells were isolated from intertidal sand collected from the East China Sea. The two strains established were subjected to detailed examination by light, and scanning and transmission electron microscopy. The vegetative cells had a minute, irregular, and triangular-shaped epicone deflected to the left, thus fitting the description of Amphidinium sensu stricto. These strains are distinguished from other Amphidinium species by combination characteristics: (1) longitudinal flagellum inserted in the lower third of the cell; (2) icicle-shaped scales, 276 ± 17 nm in length, on the cell body surface; (3) asymmetrical hypocone with the left side longer than the right; and (4) presence of immotile cells. Therefore, they are described here as Amphidinium stirisquamtum sp. nov. The molecular tree inferred from small subunit rRNA, large subunit rRNA, and internal transcribed spacer-5.8S sequences revealed that A. stirisquamtum is grouped together with the type species of Amphidinium, A. operculatum, in a fully supported clade, but is distantly related to other Amphidinium species bearing body scale. Live A.stirisquamtum cells greatly affected the survival of rotifers and brine shrimp, their primary grazers, making them more susceptible to predation by the higher tropic level consumers in the food web. This will increase the risk of introducing toxicity, and consequently, the bioaccumulation of toxins through marine food webs.

Keywords

Acknowledgement

This work was supported by the National Natural Science Foundation of China (41806154), the Scientific Research Foundation of Third Institute of Oceanography, MNR (2017023), the National Key Research and Development Program of China (2019YFE0124700) and the Youth Innovation Project of Xiamen 3502Z20206095. The authors would like to thank two anonymous reviewers whose comments and suggestions greatly improved the early version of the manuscript.

References

  1. Adachi, M., Sake, Y. & Ishida, Y. 1996. Analysis of Alexandrium (Dinophyceae) species using sequences of the 5.8S ribosomal DNA and internal transcribed spacer regions. J. Phycol. 32:424-432. https://doi.org/10.1111/j.0022-3646.1996.00424.x
  2. Baig, H. S., Saifullah, S. M. & Dar, A. 2006. Occurrence and toxicity of Amphidinium carterae Hulburt in the North Arabian Sea. Harmful Algae 5:133-140. https://doi.org/10.1016/j.hal.2005.06.010
  3. Berdalet, E., Tester, P. A., Chinain, M., Fraga, S., Lemee, R., Litaker, W., Penna, A., Usup, G., Vila, M. & Zingone, A. 2017. Harmful algal blooms in benthic systems. Oceanography 30:36-45.
  4. Boc, A., Diallo, A. B. & Makarenkov, V. 2012. T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res. 40:W573-W579. https://doi.org/10.1093/nar/gks485
  5. Calado, A. J. & Moestrup, O. 2005. On the freshwater dinoflagellates presently included in the genus Amphidinium, with a description of Prosoaulax gen. nov. Phycologia 44:112-119. https://doi.org/10.2216/0031-8884(2005)44[112:OTFDPI]2.0.CO;2
  6. Carroll, H., Beckstead, W., O'Connor, T., Ebbert, M., Clement, M., Snell, Q. & Mcclellan, D. 2007. DNA reference alignment benchmarks based on tertiary structure of encoded proteins. Bioinformatics 23:2648-2649. https://doi.org/10.1093/bioinformatics/btm389
  7. Claparede, E. & Lachmann, J. 1859. Etudes sur les infusoires et les rhizopodes. Mem. Inst. Natl. Genevois 6:261-482.
  8. Dang, L. -X., Li, Y., Liu, F., Zhang, Y., Yang, W. -D., Li, H. -Y. & Liu, J. -S. 2015. Chemical response of the toxic Dinoflagellate Karenia mikimotoi against grazing by three species of zooplankton. J. Eukaryot. Microbiol. 62:470-480. https://doi.org/10.1111/jeu.12201
  9. Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772.
  10. Daugbjerg, N., Hansen, G., Larsen, J. & Moestrup, O. 2000. Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39:302-317. https://doi.org/10.2216/i0031-8884-39-4-302.1
  11. De Jonge, V. N. & Van Beuselom, J. E. E. 1992. Contribution of resuspended microphytobenthos to total phytoplankton in the EMS estuary and its possible role for grazers. Neth. J. Sea Res. 30:91-105. https://doi.org/10.1016/0077-7579(92)90049-K
  12. Dodge, J. D. & Hart-Jones, B. 1982. Marine dinoflagellates of the British Isles. Her Majesty's Stationary Office, London, 303 pp.
  13. Dolapsakis, N. P. & Economou-Amilli, A. 2009. A new marine species of Amphidinium (Dinophyceae) from Thermaikos Gulf, Greece. Acta Protozool. 48:153-170.
  14. Echigoya, R., Rhodes, L., Oshima, Y. & Satake, M. 2005. The structures of five new antifungal and hemolytic amphidinol analogs from Amphidinium carterae collected in New Zealand. Harmful Algae 4:383-389. https://doi.org/10.1016/j.hal.2004.07.004
  15. Facca, C., Sfriso, A. & Socal, G. 2002. Changes in abundance and composition of phytoplankton and microphytobenthos due to increased sediment fluxes in the Venice lagoon, Italy. Estuar. Coast. Shelf Sci. 54:773-792. https://doi.org/10.1006/ecss.2001.0848
  16. Faimali, M., Giussani, V., Piazza, V., Garaventa, F., Corra, C., Asnaghi, V., Privitera, D., Gallus, L., Cattaneo-Vietti, R., Mangialajo, L. & Chiantore, M. 2012. Toxic effects of harmful benthic dinoflagellate Ostreopsis ovata on invertebrate and vertebrate marine organisms. Mar. Environ. Res. 76:97-107. https://doi.org/10.1016/j.marenvres.2011.09.010
  17. Farmer, M. A. & Roberts, K. R. 1989. Comparative analyses of the dinoflagellate flagellar apparatus. III. Freeze substitution of Amphidinium rhynchocephalum. J. Phycol. 25:280-292. https://doi.org/10.1111/j.1529-8817.1989.tb00124.x
  18. Forster, D., Dunthorn, M., Mahe, F., Dolan, J. R., Audic, S., Bass, D., Bittner, L., Boutte, C., Christen, R., Claverie, J. -M., Decelle, J., Edvardsen, B., Egge, E., Eikrem, W., Gobet, A., Kooistra, W. H. C. F., Logares, R., Massana, R., Montresor, M., Not, F., Ogata, H., Pawlowski, J., Pernice, M. C., Romac, S., Shalchian-Tabrizi, K., Simon, N., Richards, T. A., Santini, S., Sarno, D., Siano, R., Vaulot, D., Wincker, P., Zingone, A., De Vargas, C. & Stoeck, T. 2016. Benthic protists: the under-charted majority. FEMS Microbiol. Ecol. 92:fiw120. https://doi.org/10.1093/femsec/fiw120
  19. Garate-Lizarraga, I., Gonzalez-Armas, R., Verdugo-Diaz, G., Okolodkov, Y. B., Perez-Cruz, B. & Diaz-Ortiz, J. A. 2019. Seasonality of the dinoflagellate Amphidinium cf. carterae (Dinophyceae: Amphidiniales) in Bahia de la Paz, Gulf of California. Mar. Pollut. Bull. 146:532-541. https://doi.org/10.1016/j.marpolbul.2019.06.073
  20. Gemin, M. -P., Reveillon, D., Herve, F., Pavaux, A. -S., Tharaud, M., Sechet, V., Bertrand, S., Lemee, R. & Amzil, Z. 2019. Toxin content of Ostreopsis cf. ovata depends on bloom phases, depth and macroalgal substrate in the NW Mediterranean Sea. Harmful Algae 92:101727.
  21. Gomez, F., Qiu, D., Otero-Morales, E., Lopes, R. M. & Lin, S. 2016. Circumtropical distribution of the epiphytic dinoflagellate Coolia malayensis (Dinophyceae): morphology and molecular phylogeny from Puerto Rico and Brazil. Phycol. Res. 64:194-199. https://doi.org/10.1111/pre.12134
  22. Grell, K. G. & Wohlfarth-Bottermann, K. E. 1957. Licht- und elektronenmikroskopische untersuchungen an dem Dinoflagellaten Amphidinium elegans n. sp. Z. Zellforsch. Mikrosk. Anat. 47:7-17. https://doi.org/10.1007/BF00340000
  23. Guillard, R. R. L. & Ryther, J. H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8:229-239. https://doi.org/10.1139/m62-029
  24. Guiry, M. D. & Guiry, G. M. 2021. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org. Accessed Oct 1, 2021.
  25. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
  26. Hernroth, L. 1983. Marine pelagic rotifers and tintinnids: important trophic links in the spring plankton community of the Gullmar Fjord, Sweden. J. Plankton Res. 5:835-846. https://doi.org/10.1093/plankt/5.6.835
  27. Hillis, D. M. & Dixon, M. T. 1991. Ribosomal DNA: molecular evolution and phylogenetic inference. Q. Rev. Biol. 66:411-453. https://doi.org/10.1086/417338
  28. Hoppenrath, M., Murray, S., Sparmann, S. F. & Leander, B. S. 2012. Morphology and molecular phylogeny of Ankistrodinium gen. nov. (Dinophyceae), a new genus of marine sand-dwelling dinoflagellates formerly classified within Amphidinium. J. Phycol. 48:1143-1152. https://doi.org/10.1111/j.1529-8817.2012.01198.x
  29. Hoppenrath, M., Murray, S. A., Chomerat, N. & Horiguchi, T. 2014. Marine benthic Dinoflagellates: unveiling their worldwide biodiversity. Schweizerbart, Stuttgart, 276 pp.
  30. Horiguchi, T., Tamura, M., Katsumata, K. & Yamaguchi, A. 2012. Testudodinium gen. nov. (Dinophyceae), a new genus of sand-dwelling dinoflagellates formerly classified in the genus Amphidinium. Phycol. Res. 60:137-149. https://doi.org/10.1111/j.1440-1835.2012.00645.x
  31. Huang, S.- J., Kuo, C. -M., Lin, Y. -C., Chen, Y. -M. & Lu, C. -K. 2009. Carteraol E, a potent polyhydroxyl ichthyotoxin from the dinoflagellate Amphidinium carterae. Tetrahedron Lett. 50:2512-2515. https://doi.org/10.1016/j.tetlet.2009.03.065
  32. Huang, X. -C., Zhao, D., Guo, Y. -W., Wu, H. -M., Lin, L. -P., Wang, Z. -H., Ding, J. & Lin, Y. -S. 2004a. Lingshuiol, a novel polyhydroxyl compound with strongly cytotoxic activity from the marine dinoflagellate Amphidinium sp. Bioorg. Med. Chem. Lett. 14:3117-3120. https://doi.org/10.1016/j.bmcl.2004.04.029
  33. Huang, X. -C., Zhao, D., Guo, Y. -W., Wu, H. -M., Trivellone, E. & Cimino, G. 2004b. Lingshuiols A and B, two new polyhydroxy compounds from the Chinese marine dinoflagellate Amphidinium sp. Tetrahedron Lett. 45:5501-5504. https://doi.org/10.1016/j.tetlet.2004.05.067
  34. Hunter, R. L., Lajeunesse, T. C. & Santos, S. R. 2007. Structure and evolution of the rDNA internal transcribed spacer (ITS) region 2 in the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J. Phycol. 43:120-128. https://doi.org/10.1111/j.1529-8817.2006.00309.x
  35. Inuzuka, T., Yamada, K. & Uemura, D. 2014. Amdigenols E and G, long carbon-chain polyol compounds, isolated from the marine dinoflagellate Amphidinium sp. Tetrahedron Lett. 55:6319-6323. https://doi.org/10.1016/j.tetlet.2014.09.094
  36. Jorgensen, M. F., Murray, S. & Daugbjerg, N. 2004a. A new genus of athecate interstitial dinoflagellates, Togula gen. nov., previously encompassed within Amphidinium sensu lato: inferred from light and electron microscopy and phylogenetic analyses of partial large subunit ribosomal DNA sequences. Phycol. Res. 52:284-299. https://doi.org/10.1111/j.1440-183.2004.00352.x
  37. Jorgensen, M. F., Murray, S. & Daugbjerg, N. 2004b. Amphidinium revisited. I. Redefinition of Amphidinium (Dinophyceae) based on cladistic and molecular phylogenetic analyses. J. Phycol. 40:351-365. https://doi.org/10.1111/j.1529-8817.2004.03131.x
  38. Karafas, S., Teng, S. T., Leaw, C. P. & Alves-De-Souza, C. 2017. An evaluation of the genus Amphidinium (Dinophyceae) combining evidence from morphology, phylogenetics, and toxin production, with the introduction of six novel species. Harmful Algae 68:128-151. https://doi.org/10.1016/j.hal.2017.08.001
  39. Katoh, K. & Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30:772-780. https://doi.org/10.1093/molbev/mst010
  40. Kim, H. S., Yih, W., Kim, J. H., Myung, G. & Jeong, H. J. 2011. Abundance of epiphytic dinoflagellates from coastal waters off Jeju Island, Korea During Autumn 2009. Ocean Sci. J. 46:205. https://doi.org/10.1007/s12601-011-0016-9
  41. Kobayashi, J., Shigemori, H., Ishibashi, M., Yamasu, T., Hirota, H. & Sasaki, T. 1991. Amphidinolides G and H: new potent cytotoxic macrolides from the cultured symbiotic dinoflagellate Amphidinium sp. J. Org. Chem. 56:5221-5224. https://doi.org/10.1021/jo00017a044
  42. Lee, K. H., Jeong, H. J., Park, K., Kang, N. S., Yoo, Y. D., Lee, M. J., Lee, J. -W., Lee, S., Kim, T., Kim, H. S. & Noh, J. H. 2013. Morphology and molecular characterization of the epiphytic dinoflagellate Amphidinium massartii, isolated from the temperate waters off Jeju Island, Korea. Algae 28:213-231. https://doi.org/10.4490/algae.2013.28.3.213
  43. Li, X. -D., Wang, X. -Y., Xu, M. -E., Jiang, Y., Yan, T. & Wang, X. -C. 2020. Progress on the usage of the rotifer Brachionus plicatilis in marine ecotoxicology: a review. Aquat. Toxicol. 229:105678. https://doi.org/10.1016/j.aquatox.2020.105678
  44. Lin, J., Yan, T., Zhang, Q. & Zhou, M. 2016. Impact of several harmful algal bloom (HAB) causing species, on life history characteristics of rotifer Brachionus plicatilis Muller. Chin. J. Oceanol. Limnol. 34:642-653. https://doi.org/10.1007/s00343-016-5065-6
  45. Lucas, C. H., Widdows, J., Brinsley, M. D., Salkeld, P. N. & Herman, P. M. J. 2000. Benthic-pelagic exchange of microalgae at a tidal flat. 1. Pigment analysis. Mar. Ecol. Prog. Ser. 196:59-73. https://doi.org/10.3354/meps196059
  46. Maranda, L. & Shimizu, Y. 1996. Amphidinium operculatum var. nov. gibbosum (Dinophyceae), a free-swimming marine species producing cytotoxic metabolites. J. Phycol. 32:873-879. https://doi.org/10.1111/j.0022-3646.1996.00873.x
  47. Martinez, K. A., Lauritano, C., Druka, D., Romano, G., Grohmann, T., Jaspars, M., Martin, J., Diaz, C., Cautain, B., de La Cruz, M., Ianora, A. & Reyes, F. 2019. Amphidinol 22, a new cytotoxic and antifungal amphidinol from the Dinoflagellate Amphidinium carterae. Mar. Drugs 17:385. https://doi.org/10.3390/md17070385
  48. Medlin, L., Elwood, H. J., Stickel, S. & Sogin, M. L. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491-499. https://doi.org/10.1016/0378-1119(88)90066-2
  49. Murray, S., Flo Jorgensen, M., Daugbjerg, N. & Rhodes, L. 2004. Amphidinium revisited. II. Resolving species boundaries in the Amphidinium operculatum species complex (Dinophyceae), including the descriptions of Amphidinium trulla sp. nov. and Amphidinium gibbosum. comb. nov. J. Phycol. 40:366-382.
  50. Murray, S., Flo Jorgensen, M., Ho, S. Y. W., Patterson, D. J. & Jermiin, L. S. 2005. Improving the analysis of Dinoflagellate phylogeny based on rDNA. Protist 156:269-286. https://doi.org/10.1016/j.protis.2005.05.003
  51. Murray, S. & Patterson, D. 2002. The benthic dinoflagellate genus Amphidinium in south-eastern Australian waters, including three new species. Eur. J. Phycol. 37:279-298. https://doi.org/10.1017/S0967026202003591
  52. Murray, S. A., Garby, T., Hoppenrath, M. & Neilan, B. A. 2012. Genetic diversity, morphological uniformity and polyketide production in dinoflagellates (Amphidinium, Dinoflagellata). PLoS ONE 7:e38253. https://doi.org/10.1371/journal.pone.0038253
  53. Murray, S. A., Kohli, G. S., Farrell, H., Spiers, Z. B., Place, A. R., Dorantes-Aranda, J. J. & Ruszczyk, J. 2015. A fish kill associated with a bloom of Amphidinium carterae in a coastal lagoon in Sydney, Australia. Harmful Algae 49:19-28. https://doi.org/10.1016/j.hal.2015.08.003
  54. Neves, R. A. F., Fernandes, T., dos Santos, L. N. & Nascimento, S. M. 2017. Toxicity of benthic dinoflagellates on grazing, behavior and survival of the brine shrimp Artemia salina. PLoS ONE 12:e0175168. https://doi.org/10.1371/journal.pone.0175168
  55. Nishimura, T., Uchida, H., Noguchi, R., Oikawa, H., Suzuki, T., Funaki, H., Ihara, C., Hagino, K., Arimitsu, S., Tanii, Y., Abe, S., Hashimoto, K., Mimura, K., Tanaka, K., Yanagida, I. & Adachi, M. 2019. Abundance of the benthic dinoflagellate Prorocentrum and the diversity, distribution, and diarrhetic shellfish toxin production of Prorocentrum lima complex and P. caipirignum in Japan. Harmful Algae 96:101687. https://doi.org/10.1016/j.hal.2019.101687
  56. Nunes, B. S., Carvalho, F. D., Guilhermino, L. M. & Van Stappen, G. 2006. Use of the genus Artemia in ecotoxicity testing. Environ. Pollut. 144:453-462. https://doi.org/10.1016/j.envpol.2005.12.037
  57. Nuzzo, G., Cutignano, A., Sardo, A. & Fontana, A. 2014. Antifungal amphidinol 18 and its 7-sulfate derivative from the marine dinoflagellate Amphidinium carterae. J. Nat. Prod. 77:1524-1527. https://doi.org/10.1021/np500275x
  58. Parrish, C. C., Bodennec, G. & Gentien, P. 1998. Haemolytic glycoglycerolipids from Gymnodinium species. Phytochemistry 47:783-787. https://doi.org/10.1016/S0031-9422(97)00661-4
  59. Prince, E. K., Lettieri, L., McCurdy, K. J. & Kubanek, J. 2006. Fitness consequences for copepods feeding on a red tide dinoflagellate: deciphering the effects of nutritional value, toxicity, and feeding behavior. Oecologia 147:479-488. https://doi.org/10.1007/s00442-005-0274-2
  60. Quy, O. M., Fotedar, R. & Thy, H. T. T. 2018. Extension of rotifer (Brachionus plicatilis) inclusions in the larval diets of mud crab, Scylla paramamosain (Estampodor, 1949): effects on survival, growth, metamorphosis and development time. Mod. Appl. Sci. 12:65-74.
  61. Ronquist, F., Teslenko, M., van Der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. https://doi.org/10.1093/sysbio/sys029
  62. Rossini, G. P. 2014. Toxins and biologically active compounds from microalgae. CRC Press, Boca Raton, FL, 542 pp.
  63. Sakakura, Y. 2017. Application of rotifers for larval rearing of marine fishes cultivated under various conditions. In Hagiwara, A. & Yoshinaga, T. (Eds.) Rotifers: Aquaculture, Ecology, Gerontology, and Ecotoxicology. Springer Singapore, Singapore, pp. 63-73.
  64. Saldarriaga, J. F., Taylor, F. J. R., Keeling, P. J. & Cavalier-Smith, T. 2001. Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J. Mol. Evol. 53:204-213. https://doi.org/10.1007/s002390010210
  65. Scholin, C. A., Herzog, M., Sogin, M. & Anderson, D. M. 1994. Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30:999-1011. https://doi.org/10.1111/j.0022-3646.1994.00999.x
  66. Sekida, S., Okuda, K., Katsumata, K. & Horiguchi, T. 2003. A novel type of body scale found in two strains of Amphidinium species (Dinopbyceae). Phycologia 42:661-666. https://doi.org/10.2216/i0031-8884-42-6-661.1
  67. Sorgeloos, P., Dhert, P. & Candreva, P. 2001. Use of the brine shrimp, Artemia spp., in marine fish larviculture. Aquaculture 200:147-159. https://doi.org/10.1016/S0044-8486(01)00698-6
  68. Sparmann, S. F., Leander, B. S. & Hoppenrath, M. 2008. Comparative morphology and molecular phylogeny of Apicoporus n. gen.: a new genus of marine benthic dinoflagellates formerly classified within Amphidinium. Protist 159:383-399. https://doi.org/10.1016/j.protis.2007.12.002
  69. Spurr, A. R. 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43. https://doi.org/10.1016/S0022-5320(69)90033-1
  70. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. https://doi.org/10.1093/bioinformatics/btl446
  71. Stern, R. F., Andersen, R. A., Jameson, I., Kupper, F. C., Coffroth, M. -A., Vaulot, D., Le Gall, F., Veron, B., Brand, J. J., Skelton, H., Kasai, F., Lilly, E. L. & Keeling, P. J. 2012. Evaluating the ribosomal internal transcribed spacer (ITS) as a candidate dinoflagellate barcode marker. PLoS ONE 7:e42780. https://doi.org/10.1371/journal.pone.0042780
  72. Sterzelecki, F. C., dos Santos Cipriano, F., Vasconcelos, V. R., Sugai, J. K., Mattos, J. J., Derner, R. B., Magnotti, C. F., Lopes, R. G. & Cerqueira, V. R. 2021. Minimum rotifer density for best growth, survival and nutritional status of Brazilian sardine larvae, Sardinella brasiliensis. Aquaculture 534:736264. https://doi.org/10.1016/j.aquaculture.2020.736264
  73. Sun, Y., Hou, X., Xue, X., Zhang, L., Zhu, X., Huang, Y., Chen, Y. & Yang, Z. 2017. Trade-off between reproduction and lifespan of the rotifer Brachionus plicatilis under different food conditions. Sci. Rep. 7:15370. https://doi.org/10.1038/s41598-017-15863-y
  74. Takano, Y. & Horiguchi, T. 2004. Surface ultrastructure and molecular phylogenetics of four unarmored heterotrophic dinoflagellates, including the type species of the genus Gyrodinium (Dinophyceae). Phycol. Res. 52:107-116. https://doi.org/10.1111/j.1440-183.2004.00332.x
  75. Tamura, M., Takano, Y. & Horiguchi, T. 2009. Discovery of a novel type of body scale in the marine dinoflagellate, Amphidinium cupulatisquama sp. nov. (Dinophyceae). Phycol. Res. 57:304-312. https://doi.org/10.1111/j.1440-1835.2009.00550.x
  76. Tester, P. A., Litaker, R. W. & Berdalet, E. 2020. Climate change and harmful benthic microalgae. Harmful Algae 91:101655. https://doi.org/10.1016/j.hal.2019.101655
  77. Turner, J. T. & Tester, P. A. 1997. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol. Oceanogr. 42:1203-1213. https://doi.org/10.4319/lo.1997.42.5_part_2.1203
  78. Wellkamp, M., Garcia-Camacho, F., Duran-Riveroll, L. M., Tebben, J., Tillmann, U. & Krock, B. 2020. LC-MS/MS method development for the discovery and identification of amphidinols produced by Amphidinium. Mar. Drugs 18:497. https://doi.org/10.3390/md18100497
  79. Wu, J., Long, L., Song, Y., Zhang, S., Li, Q., Huang, J. & Xiao, Z. 2005. A mew unsaturated glycoglycerolipid from a cultured marine dinoflagellate Amphidinium carterae. Chem. Pharm. Bull. 53:330-332. https://doi.org/10.1248/cpb.53.330
  80. Yan, T., Wang, Y., Wang, L., Chen, Y., Han, G. & Zhou, M. 2009. Application of rotifer Brachionus plicatilis in detecting the toxicity of harmful algae. Chin. J. Oceanol. Limnol. 27:376-382. https://doi.org/10.1007/s00343-009-9104-4
  81. Yong, H. L., Mustapa, N. I., Lee, L. K., Lim, Z. F., Tan, T. H., Usup, G., Gu, H., Litaker, R. W., Tester, P. A., Lim, P. T. & Leaw, C. P. 2018. Habitat complexity affects benthic harmful dinoflagellate assemblages in the fringing reef of Rawa Island, Malaysia. Harmful Algae 78:56-68. https://doi.org/10.1016/j.hal.2018.07.009
  82. Yoshida, T., Nakai, R., Seto, H., Wang, M. -K., Iwataki, M. & Hiroishi, S. 2003. Sequence analysis of 5.8S rDNA and the internal transcribed spacer region in dinoflagellate Heterocapsa species (Dinophyceae) and development of selective PCR primers for the bivalve killer Heterocapsa circularisquama. Microbes Environ. 18:216-222. https://doi.org/10.1264/jsme2.18.216
  83. Zhang, H. 2015. Diversity, phylogeny and distribution of benthic dinoflagellates in Hainan Island, China. Ph.D. dissertation, Jinan University, Guangzhou.