Bioluminescence capability and intensity in the dinoflagellate Alexandrium species |
Park, Sang Ah
(School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Ok, Jin Hee (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Kang, Hee Chang (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) You, Ji Hyun (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Eom, Se Hee (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Yoo, Yeong Du (Department of Marine Biotechnology, College of Ocean Sciences, Kunsan National University) Lee, Moo Joon (Department of Marine Biotechnology, Anyang University) |
1 | Eckford-Soper, L. K., Bresnan, E., Lacaze, J. -P., Green, D. H. & Davidson, K. 2016. The competitive dynamics of toxic Alexandrium fundyense and non-toxic Alexandrium tamarense: the role of temperature. Harmful Algae 53:135-144. DOI |
2 | Huelsenbeck, J. P. & Ronquist, F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755. DOI |
3 | John, U., Litaker, R. W., Montresor, M., Murray, S., Brosnahan, M. L. & Anderson, D. M. 2014. Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165:779-804. DOI |
4 | Wilson, T. & Hastings, J. W. 2013. Bioluminescence: living lights, lights for living. Harvard University Press, Cambridge, MA, 185 pp. |
5 | Murray, S., John, U., Savela, H. & Kremp, A. 2020. Alexandrium spp.: genetic and ecological factors influencing saxitoxin production and proliferation. In Botana, L. M., Louzao, M. C. & Vilarino, N. (Eds.) Climate Change and Marine and Freshwater Toxins. Walter de Gruyter, Berlin, pp. 133-166. |
6 | Hastings, J. W. & Sweeney, B. M. 1957. The luminescent reaction in extracts of the marine dinoflagellate, Gonyaulax polyedra. J. Cell. Comp. Physiol. 49:209-225. DOI |
7 | Montresor, M., John, U., Beran, A. & Medlin, L. K. 2004. Alexandrium tamutum sp. nov. (Dinophyceae): a new nontoxic species in the genus Alexandrium. J. Phycol. 40:398-411. DOI |
8 | Swift, E., Biggley, W. H. & Seliger, H. H. 1973. Species of oceanic dinoflagellates in the genera Dissodinium and Pyrocystis: interclonal and interspecific comparisons of the color and photon yield of bioluminescence. J. Phycol. 9:420-426. DOI |
9 | Sweeney, B. M. 1963. Bioluminescent dinoflagellates. Biol. Bull. 125:177-181. DOI |
10 | Sweeney, B. M. 1986. The loss of the circadian rhythm in photosynthesis in an old strain of Gonyaulax polyedra. Plant Physiol. 80:978-981. DOI |
11 | Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599. DOI |
12 | Lee, K. H., Jeong, H. J., Kang, H. C., Ok, J. H., You, J. H. & Park, S. A. 2019. Growth rates and nitrate uptake of co-occurring red-tide dinoflagellates Alexandrium affine and A. fraterculus as a function of nitrate concentration under light-dark and continuous light conditions. Algae 34:237-251. DOI |
13 | Yoo, Y. D., Jeong, H. J., Kim, M. S., Kang, N. S., Song, J. Y., Shin, W., Kim, K. Y. & Lee, K. 2009. Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J. Eukaryot. Microbiol. 56:413-420. DOI |
14 | Cram, D. L. & Schulein, F. H. 1974. Observations on surface-shoaling Cape hake off South West Africa. ICES J. Mar. Sci. 35:272-275. DOI |
15 | Valiadi, M. & Iglesias-Rodriguez, D. 2013. Understanding bioluminescence in dinoflagellates: how far have we come? Microorganisms 1:3-25. DOI |
16 | Valiadi, M., Iglesias-Rodriguez, M. D. & Amorim, A. 2012. Distribution and genetic diversity of the luciferase gene within marine dinoflagellates. J. Phycol. 48:826-836. DOI |
17 | Murakami, M., Okita, Y., Matsuda, H., Okino, T. & Yamaguchi, K. 1998. From the dinoflagellate Alexandrium hiranoi. Phytochemistry 48:85-88. DOI |
18 | Bill, B. D., Moore, S. K., Hay, L. R., Anderson, D. M. & Trainer, V. L. 2016. Effects of temperature and salinity on the growth of Alexandrium (Dinophyceae) isolates from the Salish Sea. J. Phycol. 52:230-238. DOI |
19 | Blossom, H. E., Baedkel, T. D., Tillmann, U. & Hansen, P. J. 2017. A search for mixotrophy and mucus trap production in Alexandrium spp. and the dynamics of mucus trap formation in Alexandrium pseudogonyaulax. Harmful Algae 64:51-62. DOI |
20 | Ciminiello, P., Fattorusso, E., Forino, M. & Montresor, M. 2000. Saxitoxin and neosaxitoxin as toxic principles of Alexandrium andersoni (Dinophyceae) from the Gulf of Naples, Italy. Toxicon 38:1871-1877. DOI |
21 | Cusick, K. D. & Widder, E. A. 2014. Intensity differences in bioluminescent dinoflagellates impact foraging efficiency in a nocturnal predator. Bull. Mar. Sci. 90:797-811. DOI |
22 | Cussatlegras, A. -S. & Le Gal, P. 2007. Variability in the bioluminescence response of the dinoflagellate Pyrocystis lunula. J. Exp. Mar. Biol. Ecol. 343:74-81. DOI |
23 | Orr, R. J. S., Stuken, A., Murray, S. A. & Jakobsen, K. S. 2013. Evolutionary acquisition and loss of saxitoxin biosynthesis in dinoflagellates: the second "core" gene, sxtG. Appl. Environ. Microbiol. 79:2128-2136. DOI |
24 | Blossom, H. E., Markussen, B., Daugbjerg, N., Krock, B., Norlin, A. & Hansen, P. J. 2019. The cost of toxicity in microalgae: direct evidence from the dinoflagellate Alexandrium. Front. Microbiol. 10:1065. DOI |
25 | 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. DOI |
26 | Lee, K. H., Jeong, H. J., Kwon, J. E., Kang, H. C., Kim, J. H., Jang, S. H., Park, J.Y., Yoon, E. Y. & Kim, J. S. 2016. Mixotrophic ability of the phototrophic dinoflagellates Alexandrium andersonii, A. affine, and A. fraterculus. Harmful Algae 59:67-81. DOI |
27 | Kremp, A., Lindholm, T., Dressler, N., Erler, K., Gerdts, G., Eirtovaara, S. & Leskinen, E. 2009. Bloom forming Alexandrium ostenfeldii (Dinophyceae) in shallow waters of the Aland archipelago, Northern Baltic Sea. Harmful Algae 8:318-328. DOI |
28 | Nguyen-Ngoc, L. 2004. An autecological study of the potentially toxic dinoflagellate Alexandrium affine isolated from Vietnamese waters. Harmful Algae 3:117-129. DOI |
29 | Orr, R. J. S., Stuken, A., Rundberget, T., Eikrem, W. & Jakobsen, K. S. 2011. Improved phylogenetic resolution of toxic and non-toxic Alexandrium strains using a concatenated rDNA approach. Harmful Algae 10:676-688. DOI |
30 | Prakash, A. & Taylor, F. J. R. 1966. A "red water" bloom of Gonyaulax acatenella in the Strait of Georgia and its relation to paralytic shellfish toxicity. J. Fish. Res. Board Can. 23:1265-1270. DOI |
31 | Stamatakis, A. 2006. RaxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. DOI |
32 | McCapra, F. 1976. Chemical mechanisms in bioluminescence. Acc. Chem. Res. 9:201-208. DOI |
33 | Murakami, M., Makabe, K., Yamaguchi, K., Konosu, S. & Walchli, M. R. 1988. Goniodomin A, a novel polyether macrolide from the dinoflagellate Goniodoma pseudogoniaulax. Tetrahedron Lett. 29:1149-1152. DOI |
34 | Scholin, C. A., Herzog, M., Sogin, M. & Anderson, D. M. 1994. Identification of group- and strain-specific genetic makers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30:999-1011. DOI |
35 | Seliger, H. H., Biggley, W. H. & Swift, E. 1969. Absolute values of photon emission from the marine dinoflagellates Pyrodinium bahamense, Gonyaulax polyedra and Pyrocystis lunula. Photochem. Photobiol. 10:227-232. DOI |
36 | Shimomura, O. 2006. Bioluminescence: chemical principles and methods. World Scientific, Toh Tuck Link, 500 pp. |
37 | Laabir, M., Jauzein, C., Genovesi, B., Masseret, E., Grzebyk, D., Cecchi, P., Vaquer, A., Perrin, Y. & Collos, Y. 2011. Influence of temperature, salinity and irradiance on the growth and cell yield of the harmful red tide dinoflagellate Alexandrium catenella colonizing Mediterranean waters. J. Plankton Res. 33:1550-1563. DOI |
38 | Lapota, D., Geiger, M. L., Stiffey, A. V., Rosenberger, D. E. & Young, D. K. 1989. Correlations of planktonic bioluminescence with other oceanographic parameters from a Norwegian fjord. Mar. Ecol. Prog. Ser. 55:217-227. DOI |
39 | Latz, M. I. & Jeong, H. J. 1996. Effect of red tide dinoflagellate diet and cannibalism on the bioluminescence of the heterotrophic dinoflagellates Protoperidinium spp. Mar. Ecol. Prog. Ser. 132:275-285. DOI |
40 | Latz, M. I. & Lee, A. O. 1995. Spontaneous and stimulated bioluminescence of the dinoflagellate Ceratocorys horrzda (Peridiniales). J. Phycol. 31:120-132. DOI |
41 | Lewis, N. I., Xu, W., Jericho, S. K., Kreuzer, H. J., Jericho, M. H. & Cembella, A. D. 2006. Swimming speed of three species of Alexandrium (Dinophyceae) as determined by digital in-line holography. Phycologia 45:61-70. DOI |
42 | Martinez, A., Mendez, S. & Fabre, A. 2016. First record of bioluminescence of Alexandrium fraterculus (dinoflagellate), in the Uruguayan coast, South Western Atlantic Ocean. Pan-Am. J. Aquat. Sci. 11:356-360. |
43 | Rohr, J., Latz, M. I., Fallon, S., Nauen, J. C. & Hendricks, E. 1998. Experimental approaches towards interpreting dolphin-stimulated bioluminescence. J. Exp. Biol. 201:1447-1460. DOI |
44 | Swift, E., Sullivan, J. M., Batchelder, H. P., Van Keuren, J., Vaillancourt, R. D. & Bidigare, R. R. 1995. Bioluminescent organisms and bioluminescence measurements in the North Atlantic Ocean near latitude 59.5°N, longitude 21°W. J. Geophys. Res. Oceans 100:6527-6547. DOI |
45 | Le Tortorec, A. H., Tahvanainen, P., Kremp, A. & Simis, S. G. H. 2016. Diversity of luciferase sequences and bioluminescence production in Baltic Sea Alexandrium ostenfeldii. Eur. J. Phycol. 51:317-327. DOI |
46 | Lee, S. Y., Jeong, H. J., Ok, J. H., Kang, H. C. & You, J. H. 2020. Spatial-temporal distributions of the newly described mixotrophic dinoflagellate Gymnodinium smaydae in Korean coastal waters. Algae 35:225-236. DOI |
47 | Kruskal, W. H. & Wallis, W. A. 1952. Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47:583-621 DOI |
48 | Lim, A. S., Jeong, H. J., Kim, J. H., Jang, S. H., Lee, M. J. & Lee, K. 2015. Mixotrophy in the newly described dinoflagellate Alexandrium pohangense: a specialist for feeding on the fast-swimming ichthyotoxic dinoflagellate Cochlodinium polykrikoides. Harmful Algae 49:10-18. DOI |
49 | Lim, A. S., Jeong, H. J. & Ok, J. H. 2019. Five Alexandrium species lacking mixotrophic ability. Algae 34:289-301. DOI |
50 | Lindstrom, J., Grebner, W., Rigby, K. & Selander, E. 2017. Effects of predator lipids on dinoflagellate defense mechanisms-increased bioluminescence capacity. Sci. Rep. 7:13104. DOI |
51 | Miller, S. D., Haddock, S. H. D., Elvidge, C. D. & Lee, T. F. 2005. Detection of a bioluminescent milky sea from space. Proc. Natl. Acad. Sci. U. S. A. 102:14181-14184. DOI |
52 | Lim, A. S., Jeong, H. J., Ok, J. H. & Kim, S. J. 2018. Feeding by the harmful phototrophic dinoflagellate Takayama tasmanica (Family Kareniaceae). Harmful Algae 74:19-29. DOI |
53 | Liu, L., Wilson, T. & Hastings, J. W. 2004. Molecular evolution of dinoflagellate luciferases, enzymes with three catalytic domains in a single polypeptide. Proc. Natl. Acad. Sci. U. S. A. 101:16555-16560. DOI |
54 | Marcinko, C. L. J., Painter, S. C., Martin, A. P. & Allen, J. T. 2013. A review of the measurement and modelling of dinoflagellate bioluminescence. Prog. Oceanogr. 109:117-129. DOI |
55 | Dunn, O. J. 1961. Multiple comparisons among means. J. Am. Stat. Assoc. 56:52-64. DOI |
56 | Eckert, R. 2015. Excitation and luminescence in Noctiluca miliaris. In Johnson, F. H. & Haneda, Y. (Eds.) Bioluminescence in Progress. Princeton University Press, Princeton, NJ, pp. 269-300. |
57 | Esaias, W. E. & Curl, H. C. Jr. 1972. Effect of dinoflagellate bioluminescence on copepod ingestion rates. Limnol. Oceanogr. 17:901-906. DOI |
58 | Mann, H. B. & Whitney, D. R. 1947. On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18:50-60. DOI |
59 | Litaker, R. W., Vandersea, M. W., Kibler, S. R., Reece, K. S., Stokes, N. A., Steidinger, K. A., Millie, D. F., Bendis, B. J., Pigg, R. J. & Tester, P. A. 2003. Identification of Pfiesteria piscicida (Dinophyceae) and Pfiesteria-like organisms using internal transcribed spacer-specific PCR assays. J. Phycol. 39:754-761. DOI |
60 | MacKenzie, L., de Salas, M., Adamson, J. & Beuzenberg, V. 2004. The dinoflagellate genus Alexandrium (Halim) in New Zealand coastal waters: comparative morphology, toxicity and molecular genetics. Harmful Algae 3:71-92. DOI |
61 | Latz, M. I., Bovard, M., VanDelinder, V., Segre, E., Rohr, J. & Groisman, A. 2008. Bioluminescent response of individual dinoflagellate cells to hydrodynamic stress measured with millisecond resolution in a microfluidic device. J. Exp. Biol. 211:2865-2875. DOI |
62 | Esaias, W. E., Curl, H. C. Jr. & Seliger, H. H. 1973. Action spectrum for a low intensity, rapid photoinhibition of mechanically stimulable bioluminescence in the marine dinoflagellates Gonyaulax catenella, G. acatenella, and G. tamarensis. J. Cell. Physiol. 82:363-372. DOI |
63 | Games, P. A. & Howell, J. F. 1976. Pairwise multiple comparison procedures with unequal n's and/or variances: a Monte Carlo study. J. Educ. Stat. 1:113-125. DOI |
64 | Gu, H. 2011. Morphology, phylogenetic position, and ecophysiology of Alexandrium ostenfeldii (Dinophyceae) from the Bohai Sea, China. J. Syst. Evol. 49:606-616. DOI |
65 | Latz, M. I., Nauen, J. C. & Rohr, J. 2004. Bioluminescence response of four species of dinoflagellates to fully developed pipe flow. J. Plankton Res. 26:1529-1546. DOI |
66 | Lilly, E. L., Halanych, K. M. & Anderson, D. M. 2005. Phylogeny, biogeography, and species boundaries within the Alexandrium minutum group. Harmful Algae 4:1004-1020. DOI |
67 | Kang, H. C., Jeong, H. J., Kim, S. J., You, J. H. & Ok, J. H. 2018. Differential feeding by common heterotrophic protists on 12 different Alexandrium species. Harmful Algae 78:106-117. DOI |
68 | Jeong, H. J., Kang, H. C., Lim, A. S., Jang, S. H., Lee, K., Lee, S. Y., Ok, J. H., You, J. H., Kim, J. H., Lee, K. H., Park, S. A., Eom, S. H., Yoo, Y. D. & Kim, K. Y. 2021. Feeding diverse prey as an excellent strategy of mixotrophic dinoflagellates for global dominance. Sci. Adv. 7:eabe4214. DOI |
69 | Jeong, H. J., Lim, A. S., Franks, P. J. S., Lee, K. H., Kim, J. H., Kang, N. S., Lee, M. J., Jang, S. H., Lee, S. Y., Yoon, E. Y., Park, J. Y., Yoo, Y. D., Seong, K. A., Kwon, J. E. & Jang, T. Y. 2015. A hierarchy of conceptual models of red-tide generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97-115. DOI |
70 | Jeong, H. J., Lim, A. S., Lee, K., Lee, M. J., Seong, K. A., Kang, N. S., Jang, S. H., Lee, K. H., Lee, S. Y., Kim, M. O., Kim, J. H., Kwon, J. E., Kang, H. C., Kim, J. S., Yuh, W., Shin, K., Jang, P. K., Ryu, J. -H., Kim, S. Y., Park, J. Y. & Kim, K. Y. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: I. Temporal variations in three-dimensional distributions of red-tide organisms and environmental factors. Algae 32:101-130. DOI |
71 | Kang, H. C., Jeong, H. J., Ok, J. H., You, J. H., Jang, S. H., Lee, S. Y., Lee, K. H., Park, J. Y. & Rho, J. -R. 2019. Spatial and seasonal distributions of the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) in Korea: quantification using qPCR. Algae 34:111-126. DOI |
72 | Kelly, M. G. 1968. The occurrence of dinoflagellate luminescence at Woods Hole. Biol. Bull. 135:279-295. DOI |
73 | Krasnow, R., Dunlap, J. C., Taylor, W., Hastings, J. W., Vetterling, W. & Gooch, V. 1980. Circadian spontaneous bioluminescent glow and flashing of Gonyau1ax polyedra. J. Comp. Phvsiol. 138:19-26. DOI |
74 | Anderson, D. M., Alpermann, T. J., Cembella, A. D., Collos, Y., Masseret, E. & Montresor, M. 2012. The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10-35. DOI |
75 | Jeong, H. J., Park, J. Y., Nho, J. H., Park, M. O., Ha, J. H., Seong, K. A., Jeng, C., Seong, C. N., Lee, K. Y. & Yih, W. H. 2005. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol. 41:131-143. DOI |
76 | Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. DOI |
77 | Satake, M., MacKenzie, L. & Yasumoto, T. 1997. Identification of Protoceratium reticulatum as the biogenetic origin of yessotoxin. Nat. Toxins 5:164-167. DOI |
78 | Sullivan, J. M. & Swift, E. 1995. Photoenhancement of bioluminescence capacity in natural and laboratory populations of the autotrophic dinoflagellate Ceratium fusus (Ehrenb.) Dujardin. J. Geophys. Res. Oceans 100: 6565-6574. DOI |
79 | Subong, B. J. J., Benico, G. A., Sulit, A. K. L., Mendoza, C. O., Cruz, L. J., Azanza, R. V. & Jimenez, E. C. 2017. Toxicity and protein expression of Alexandrium species collected in the Philippine waters. Philipp. J. Sci. 146:425-436. |
80 | Von Dassow, P. & Latz, M. I. 2002. The role of Ca2+ in stimulated bioluminescence of the dinoflagellate Lingulodinium polyedrum. J. Exp. Biol. 205:2971-2986. DOI |
81 | Baker, A., Robbins, I., Moline, M. A. & Iglesias-Rodriguez, M. D. 2008. Oligonucleotide primers for the detection of bioluminescent dinoflagellates reveal novel luciferase sequences and information on the molecular evolution of this gene. J. Phycol. 44:419-428. DOI |
82 | Bergkvist, J., Selander, E. & Pavia, H. 2008. Induction of toxin production in dinoflagellates: the grazer makes a difference. Oecologia 156:147-154. DOI |
83 | Biggley, W. H., Swift, E., Buchanan, R. J. & Seliger, H. H. 1969. Stimulable and spontaneous bioluminescence in the marine dinoflagellates, Pyrodinium bahumense, Gonyaulax polyedra, and Pyrocystis lunula. J. Gen. Physiol. 54:96-122. DOI |
84 | Colin, S. P. & Dam, H. G. 2003. Effects of the toxic dinoflagellate Alexandrium fundyense on the copepod Acartia hudsonica: a test of the mechanisms that reduce ingestion rates. Mar. Ecol. Prog. Ser. 248:55-65. DOI |
85 | Haddock, S. H. D., Moline, M. A. & Case, J. F. 2010. Bioluminescence in the sea. Annu. Rev. Mar. Sci. 2:443-493. DOI |
86 | Guillard, R. R. L. & Hargraves, P. E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234-236. DOI |
87 | 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. DOI |
88 | Guiry, M. D. & Guiry, G. M. 2021. AlgaeBase. Available from: https://www.algaebase.org. Accessed Oct 10, 2021. |
89 | Higman, W. A., Stone, D. M. & Lewis, J. M. 2001. Sequence comparisons of toxic and non-toxic Alexandrium tamarense (Dinophyceae) isolates from UK waters. Phycologia 40:256-262. DOI |
90 | Welch, B. L. 1947. The generalization of 'student's' problem when several different population variances are involved. Biometrika 34:28-35. DOI |
91 | White, H. H. 1979. Effects of dinoflagellate bioluminescence on the ingestion rates of herbivorous zooplankton. J. Exp. Mar. Biol. Ecol. 36:217-224. DOI |
92 | Widder, E. A. 2010. Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science 328:704-708. DOI |
93 | Widder, E. A. & Case, J. F. 1981. Two flash forms in the bioluminescent dinoflagellate, Pyrocystis fusiformis. J. Comp. Physiol. 143:43-52. DOI |
94 | Fogel, M. & Hastings, J. W. 1972. Bioluminescence: mechanism and mode of control of scintillon activity. Proc. Natl. Acad. Sci. U. S. A. 69:690-693. DOI |
95 | Cusick, K. D. & Widder, E. A. 2020. Bioluminescence and toxicity as driving factors in harmful algal blooms: ecological functions and genetic variability. Harmful Algae 98:101850. DOI |
96 | Jacobson, D. M. & Anderson, D. M. 1996. Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J. Phycol. 32:279-285. DOI |
97 | Jang, S. H. & Jeong, H. J. 2020. Spatio-temporal distributions of the newly described mixotrophic dinoflagellate Yihiella yeosuensis (Suessiaceae) in Korean coastal waters and its grazing impact on prey populations. Algae 35:45-59. DOI |
98 | Wohlrab, S., Iversen, M. H. & John, U. 2010. A molecular and co-evolutionary context for grazer induced toxin production in Alexandrium tamarense. PLoS ONE 5:e15039. DOI |
99 | Blossom, H. E., Daugbjerg, N. & Hansen, P. J. 2012. Toxic mucus traps: a novel mechanism that mediates prey uptake in the mixotrophic dinoflagellate Alexandrium pseudogonyaulax. Harmful Algae 17:40-53. DOI |
100 | Draisci, R., Ferretti, E., Palleschi, L., Marchiafava, C., Poletti, R., Milandri, A., Ceredi, A. & Pompei, M. 1999. High levels of yessotoxin in mussels and presence of yessotoxin and homoyessotoxin in dinoflagellates of the Adriatic Sea. Toxicon 37:1187-1193. DOI |