DOI QR코드

DOI QR Code

Feeding by common heterotrophic protist predators on seven Prorocentrum species

  • You, Ji Hyun (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) ;
  • Kang, Hee Chang (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) ;
  • Park, Sang Ah (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Lim, An Suk (Division of Life Science, Gyeongsang National University)
  • Received : 2020.01.27
  • Accepted : 2020.02.28
  • Published : 2020.03.15

Abstract

Species belonging to the dinoflagellate genus Prorocentrum are known to cause red tides or harmful algal blooms. To understand the dynamics of a Prorocentrum sp., its growth and mortality due to predation need to be assessed. However, there are only a few Prorocentrum spp. for which heterotrophic protist predators have been reported. We explored feeding by the common heterotrophic dinoflagellates Gyrodinium dominans, Oxyrrhis marina, Pfiesteria piscicida, Oblea rotunda, and Polykrikos kofoidii and the naked ciliate Strombidinopsis sp. (approx. 90 ㎛ cell length) on the planktonic species Prorocentrum triestinum, P. cordatum, P. donghaiense, P. rhathymum, and P. micans as well as the benthic species P. lima and P. hoffmannianum. All heterotrophic protists tested were able to feed on the planktonic prey species. However, O. marina and O. rotunda did not feed on P. lima and P. hoffmannianum, while G. dominans, P. kofoidii, and Strombidinopsis sp. did. The growth and ingestion rates of G. dominans and P. kofoidii on one of the seven Prorocentrum spp. were significantly different from those on other prey species. G. dominans showed the top three highest growth rates when it fed on P. triestinum, P. cordatum, and P. donghaiense, however, P. kofoidii had negative growth rates when fed on these three prey species. In contrast, P. kofoidii had a positive growth rate only when fed on P. hoffmannianum. This differential feeding on Prorocentrum spp. between G. dominans and P. kofoidii may provide different ecological niches and reduce competition between these two common heterotrophic protist predators.

References

  1. An, X., Li, X. & Li, Z. 2016. Effects of concentrations of Prorocentrum donghaiense and Oxyrrhis marina on the feeding behaviour of Oithona brevicornis. Nat. Environ. Pollut. Technol. 15:1195-1198.
  2. Anderson, S. R. & Menden-Deuer, S. 2017. Growth, grazing, and starvation survival in three heterotrophic dinoflagellate species. J. Eukaryot. Microbiol. 64:213-225. https://doi.org/10.1111/jeu.12353
  3. Azanza, R. V., Fukuyo, Y., Yap, L. G. & Takayama, H. 2005. Prorocentrum minimum bloom and its possible link to a massive fish kill in Bolinao, Pangasinan, Northern Philippines. Harmful Algae 4:519-524. https://doi.org/10.1016/j.hal.2004.08.006
  4. Backer, L. C. & McGillicuddy, D. J. Jr. 2006. Harmful algal blooms: at the interface between coastal oceanography and human health. Oceanography 19:94-106.
  5. Barker, H. A. 1935. The culture and physiology of the marine dinoflagellates. Arch. Mikrobiol. 6:157-181. https://doi.org/10.1007/BF00407285
  6. Berdalet, E., Peters, F., Koumandou, V. L., Roldan, C., Guadayol, O. & Estrada, M. 2007. Species-specific physiological response of dinoflagellates to quantified smallscale turbulence. J. Phycol. 43:965-977. https://doi.org/10.1111/j.1529-8817.2007.00392.x
  7. Burkholder, J. M. & Glasgow, H. B. Jr. 1997. Pfiesteria piscicida and other Pfiesreria-like dinoflagellates: behavior, impacts, and environmental controls. Limnol. Oceanogr. 42:1052-1075. https://doi.org/10.4319/lo.1997.42.5_part_2.1052
  8. Buskey, E. J., Coulter, C. & Strom, S. 1993. Locomotory patterns of microzooplankton: potential effects on food selectivity of larval fish. Bull. Mar. Sci. 53:29-43.
  9. Calbet, A., Isari, S., Martinez, R. A., Saiz, E., Garrido, S., Peters, J., Borrat, R. M. & Alcaraz, M. 2013. Adaptations to feast and famine in different strains of the marine heterotrophic dinoflagellates Gyrodinium dominans and Oxyrrhis marina. Mar. Ecol. Prog. Ser. 483:67-84. https://doi.org/10.3354/meps10291
  10. Chen, H. L., Lu, S. H., Zhang, C. S. & Zhu, D. D. 2006. A survey on the red tide of Prorocentrum donghaiense in East China Sea, 2004. Ecol. Sci. 25:226-230.
  11. Claessens, M., Wickham, S. A., Post, A. F. & Reuter, M. 2008. Ciliate community in the oligotrophic Gulf of Aqaba, Red Sea. Aquat. Microb. Ecol. 53:181-190. https://doi.org/10.3354/ame01243
  12. Cosson, J., Cachon, M., Cachon, J. & Cosson, M. -P. 1988. Swimming behaviour of the unicellular biflagellate Oxyrrhis marina: in vivo and in vitro movement of the two flagella. Biol. Cell 63:117-126. https://doi.org/10.1016/0248-4900(88)90050-0
  13. Coyne, K. J., Hutchins, D. A., Hare, C. E. & Cary, S. C. 2001. Assessing temporal and spatial variability in Pfiesteria piscicida distributions using molecular probing techniques. Aquat. Microb. Ecol. 24:275-285. https://doi.org/10.3354/ame024275
  14. Dam, H. G. & Colin, S. P. 2005. Prorocentrum minimum (clone Exuv) is nutritionally insufficient, but not toxic to the copepod Acartia tonsa. Harmful Algae 4:575-584. https://doi.org/10.1016/j.hal.2004.08.007
  15. Faust, M. A. 1990. Morphologic details of six benthic species of Prorocentrum (Pyrrophyta) from a mangrove island, twin cays, belize, including two new species. J. Phycol. 26:548-558. https://doi.org/10.1111/j.0022-3646.1990.00548.x
  16. Faust, M. A. 2009. Ciguatera-causing dinoflagellates in a coral-reef mangrove ecosystem, Belize. Atoll Res. Bull. 569:1-30.
  17. Franklin, D. J., Brussaard, C. P. D. & Berges, J. A. 2006. What is the role and nature of programmed cell death in phytoplankton ecology? Eur. J. Phycol. 41:1-14. https://doi.org/10.1080/09670260500505433
  18. Frost, B. W. 1972. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17:805-815. https://doi.org/10.4319/lo.1972.17.6.0805
  19. Gaines, G. & Taylor, F. J. R. 1984. Extracellular digestion in marine dinoflagellates. J. Plankton Res. 6:1057-1061. https://doi.org/10.1093/plankt/6.6.1057
  20. Guillard, R. R. L. & Hargraves, P. E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234-236. https://doi.org/10.2216/i0031-8884-32-3-234.1
  21. 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
  22. Hajdu, S., Edler, L., Olenina, I. & Witek, B. 2000. Spreading and establishment of the potentially toxic dinoflagellate Prorocentrum minimum in the Baltic Sea. Int. Rev. Hydrobiol. 85:561-575. https://doi.org/10.1002/1522-2632(200011)85:5/6<561::AID-IROH561>3.0.CO;2-3
  23. Hallegraeff, G. M. 1992. Harmful algal blooms in the Australian region. Mar. Pollut. Bull. 25:186-190. https://doi.org/10.1016/0025-326X(92)90223-S
  24. Hansen, P. J. 1991. Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web. Mar. Ecol. Prog. Ser. 73:253-261. https://doi.org/10.3354/meps073253
  25. Hansen, P. J. 1992. Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar. Biol. 114:327-334. https://doi.org/10.1007/BF00349535
  26. Heil, C. A., Glibert, P. M. & Fan, C. 2005. Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4:449-470. https://doi.org/10.1016/j.hal.2004.08.003
  27. Heinbokel, J. F. 1978. Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar. Biol. 47:177-189. https://doi.org/10.1007/BF00395638
  28. Hernandez-Becerril, D. U., Altamirano, R. C. & Alonso, R. R. 2000. The dinoflagellate genus Prorocentrum along the coasts of the Mexican Pacific. Hydrobiologia 418:111-121. https://doi.org/10.1023/A:1003806719515
  29. Hoppenrath, M., Chomerat, N., Horiguchi, T., Schweikert, M., Nagahama, Y. & Murray, S. 2013. Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae): a proposal and review. Harmful Algae 27:1-28. https://doi.org/10.1016/j.hal.2013.03.006
  30. Hu, T., Curtis, J. M., Walter, J. A. & Wright, J. L. C. 1999. Hoffmanniolide: a novel macrolide from Prorocentrum hoffmannianum. Tetrahedron Lett. 40:3977-3980. https://doi.org/10.1016/S0040-4039(99)00513-4
  31. Hu, W., Xu, J., Sinkkonen, J. & Wu, J. 2010. Polyketides from marine dinoflagellates of the genus Prorocentrum, biosynthetic origin and bioactivity of their okadaic acid analogues. Mini-Rev. Med. Chem. 10:51-61. https://doi.org/10.2174/138955710791112541
  32. Ingarao, C., Lanciani, G., Verri, C. & Pagliani, T. 2009. First record of Prorocentrum lima (Dinophyceae) inside harbor areas and along the Abruzzo region coast, W Adriatic. Mar. Pollut. Bull. 58:596-600. https://doi.org/10.1016/j.marpolbul.2009.02.012
  33. Ismael, G. I. & Aida, M. L. 1997. First record of a Prorocentrum rhathymum (Prorocentraceae) red tide in the Gulf of California. Rev. Biol. Trop. 45:1263-1271.
  34. Jeong, H. J., Ha, J. H., Park, J. Y., Kim, J. H., Kang, N. S., Kim, S., Kim, J. S., Yoo, Y. D. & Yih, W. H. 2006. Distribution of the heterotrophic dinoflagellate Pfiesteria piscicida in Korean waters and its consumption of mixotrophic dinoflagellates, raphidophytes and fish blood cells. Aquat. Microb. Ecol. 44:263-278. https://doi.org/10.3354/ame044263
  35. Jeong, H. J., Kang, H., Shim, J. H., Park, J. K., Kim, J. S., Song, J. Y. & Choi, H. -J. 2001a. Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp. Mar. Ecol. Prog. Ser. 218:77-86. https://doi.org/10.3354/meps218077
  36. Jeong, H. J., Kang, H. C., You, J. H. & Jang, S. H. 2018. Interactions between the newly described small- and fast-swimming mixotrophic dinoflagellate Yihiella yeosuensis and common heterotrophic protists. J. Eukaryot. Microbiol. 65:612-626. https://doi.org/10.1111/jeu.12506
  37. Jeong, H. J., Kim, J. S., Song, J. Y., Kim, J. H., Kim, T. H., Kim, S. K. & Kang, N. S. 2007. Feeding by protists and copepods on the heterotrophic dinoflagellates Pfiesteria piscicida, Stoeckeria algicida, and Luciella masanensis. Mar. Ecol. Prog. Ser. 349:199-211. https://doi.org/10.3354/meps07094
  38. Jeong, H. J., Kim, S. K., Kim, J. S., Kim, S. T., Yoo, Y. D. & Yoon, J. Y. 2001b. Growth and grazing rates of the heterotrophic dinoflagellate Polykrikos kofoidii on red-tide and toxic dinoflagellates. J. Eukaryot. Microbiol. 48:298-308. https://doi.org/10.1111/j.1550-7408.2001.tb00318.x
  39. Jeong, H. J., Kim, T. H., Yoo, Y. D., Yoon, E. Y., Kim, J. S., Seong, K. A., Kim, K. Y. & Park, J. Y. 2011. Grazing impact of heterotrophic dinoflagellates and ciliates on common red-tide euglenophyte Eutreptiella gymnastica in Masan Bay, Korea. Harmful Algae 10:576-588. https://doi.org/10.1016/j.hal.2011.04.008
  40. 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. https://doi.org/10.1016/j.hal.2015.06.004
  41. 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., Yih, 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. https://doi.org/10.4490/algae.2017.32.5.30
  42. Jeong, H. J., Lim, A. S., Yoo, Y. D., Lee, M. J., Lee, K. H., Jang, T. Y. & Lee, K. 2014. Feeding by heterotrophic dinoflagellates and ciliates on the free-living dinoflagellate Symbiodinium sp. (Clade E). J. Eukaryot. Microbiol. 61:27-41. https://doi.org/10.1111/jeu.12083
  43. Jeong, H. J., Shim, J. H., Kim, J. S., Park, J. Y., Lee, C. W. & Lee, Y. 1999a. Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser. 176:263-277. https://doi.org/10.3354/meps176263
  44. Jeong, H. J., Shim, J. H., Lee, C. W., Kim, J. S. & Koh, S. M. 1999b. Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. J. Eukaryot. Microbiol. 46:69-76. https://doi.org/10.1111/j.1550-7408.1999.tb04586.x
  45. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S. & Kim, T. H. 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45:65-91. https://doi.org/10.1007/s12601-010-0007-2
  46. Jeong, H. J., Yoo, Y. D., Lee, K. H., Kim, T. H., Seong, K. A., Kang, N. S., Lee, S. Y., Kim, J. S., Kim, S. & Yih, W. H. 2013. Red tides in Masan Bay, Korea in 2004-2005: I. Daily variations in the abundance of red-tide organisms and environmental factors. Harmful Algae 30(Supp. 1):S75-S88. https://doi.org/10.1016/j.hal.2013.10.008
  47. Jeong, H. J., Yoon, J. Y., Kim, J. S., Yoo, Y. D. & Seong, K. A. 2002. Growth and grazing rates of the prostomatid ciliate Tiarina fusus on red-tide and toxic algae. Aquat. Microb. Ecol. 28:289-297.
  48. Kang, H. C., Jeong, H. J., Jang, S. H. & Lee, K. H. 2019. Feeding by common heterotrophic protists on the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) compared to that of other suessioid dinoflagellates. Algae 34:127-140. https://doi.org/10.4490/algae.2019.34.5.29
  49. 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. https://doi.org/10.1016/j.hal.2018.08.005
  50. Kang, N. S., Lee, K. H., Jeong, H. J., Yoo, Y. D., Seong, K. A., Potvin, E., Hwang, Y. J. & Yoon, E. Y. 2013. Red tides in Shiwha Bay, western Korea: a huge dike and tidal power plant established in a semi-enclosed embayment system. Harmful Algae 30(Suppl. 1):S114-S130. https://doi.org/10.1016/j.hal.2013.10.011
  51. Khan, S., Arakawa, O. & Onoue, Y. 1997. Neurotoxins in a toxic red tide of Heterosigma akashiwo (Raphidophyceae) in Kagoshima Bay, Japan. Aquac. Res. 28:9-14. https://doi.org/10.1111/j.1365-2109.1997.tb01309.x
  52. Kim, J. S. & Jeong, H. J. 2004. Feeding by the heterotrophic dinoflagellates Gyrodinium dominans and G. spirale on the red-tide dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser. 280:85-94. https://doi.org/10.3354/meps280085
  53. Kim, S. J., Jeong, H. J., Jang, S. H., Lee, S. Y. & Park, T. G. 2017. Interactions between the voracious heterotrophic nanoflagellate Katablepharis japonica and common heterotrophic protists. Algae 32:309-324. https://doi.org/10.4490/algae.2017.32.11.27
  54. Kim, S. J., Jeong, H. J., Kang, H. C., You, J. H. & Ok, J. H. 2019. Differential feeding by common heterotrophic protists on four Scrippsiella species of similar size. J. Phycol. 55:868-881. https://doi.org/10.1111/jpy.12864
  55. Kudela, R. M. & Gobler, C. J. 2012. Harmful dinoflagellate blooms caused by Cochlodinium sp.: global expansion and ecological strategies facilitating bloom formation. Harmful Algae 14:71-86. https://doi.org/10.1016/j.hal.2011.10.015
  56. Labib, W. 1996. Water discoloration in Alexandria, Egypt, April 1993. I. Occurrence of Prorocentrum triestinum Schiffer (red tide) bloom and associated physical and chemical conditions. Chem. Ecol. 12:163-170. https://doi.org/10.1080/02757549608039079
  57. Lee, C. W. 1998. Growth and grazing rates of the heterotrophic dinoflagellate Oxyrrhis marina and the ciliate Stormbidinopsis sp. on Prorocentrum spp. M.S. thesis, Kunsan National University, Gunsan, 36 pp. (in Korean with English abstract).
  58. Lee, K. H., Jeong, H. J., Kang, H. C., Ok, J. H., You, J. H. & Park, S. A. 2019a. 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. https://doi.org/10.4490/algae.2019.34.8.28
  59. Lee, K. H., Jeong, H. J., Yoon, E. Y., Jang, S. H., Kim, H. S. & Yih, W. 2014. Feeding by common heterotrophic dinoflagellates and a ciliate on the red-tide ciliate Mesodinium rubrum. Algae 29:153-163. https://doi.org/10.4490/algae.2014.29.2.153
  60. Lee, S. Y., Jeong, H. J., Kwon, J. E., You, J. H., Kim, S. J., Ok, J. H., Kang, H. C. & Park, J. Y. 2019b. First report of the photosynthetic dinoflagellate Heterocapsa minima in the Pacific Ocean: morphological and genetic characterizations and the nationwide distribution in Korea. Algae 34:7-21. https://doi.org/10.4490/algae.2019.34.2.28
  61. Lee, S. Y., Jeong, H. J., You, J. H. & Kim, S. J. 2018. Morphological and genetic characterization and the nationwide distribution of the phototrophic dinoflagellate Scrippsiella lachrymosa in the Korean waters. Algae 33:21-35. https://doi.org/10.4490/algae.2018.33.3.4
  62. Leles, S. G., Mitra, A., Flynn, K. J., Tillmann, U., Stoecker, D., Jeong, H. J., Burkholder, J., Hansen, P. J., Caron, D., Glibert, P., Hallegraef, G., Raven, J. A., Sanders, R. W. & Zubkov, M. 2019. Sampling bias misrepresents the biogeographical significance of constitutive mixotrophs across global oceans. Glob. Ecol. Biogeogr. 28:418-428. https://doi.org/10.1111/geb.12853
  63. Lewis, J. 1990. The cyst-theca relationship of Oblea rotunda (Diplopsalidaceae, Dinophyceae). Br. Phycol. J. 25:339-351. https://doi.org/10.1080/00071619000650381
  64. Li, Y., Lu, S., Jiang, T., Xiao, Y. & You, S. 2011. Environmental factors and seasonal dynamics of Prorocentrum populations in Nanji Islands National Nature Reserve, East China Sea. Harmful Algae 10:426-432. https://doi.org/10.1016/j.hal.2010.08.002
  65. Lim, A. S., Jeong, H. J., Jang, T. Y., Kang, N. S., Lee, S. Y., Yoo, Y. D. & Kim, H. S. 2013. Morphology and molecular characterization of the epiphytic dinoflagellate Prorocentrum cf. rhathymum in temperate waters off Jeju Island, Korea. Ocean Sci. J. 48:1-17. https://doi.org/10.1007/s12601-013-0001-6
  66. Lim, A. S., Jeong, H. J., Seong, K. A., Lee, M. J., Kang, N. S., Jang, S. H., Lee, K. H., Park, J. Y., Jang, T. Y. & Yoo, Y. D. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: II. Heterotrophic protists and their grazing impacts on redtide organisms. Algae 32:199-222. https://doi.org/10.4490/algae.2017.32.8.25
  67. Lowe, C. D., Day, A., Kemp, S. J. & Montagnes, D. J. S. 2005. There are high levels of functional and genetic diversity in Oxyrrhis marina. J. Eukaryot. Microbiol. 52:250-257. https://doi.org/10.1111/j.1550-7408.2005.00034.x
  68. Lu, C. K., Chou, H. N., Lee, C. K. & Li, Z. -H. 2005. Prorocentin, a new polyketide from the marine dinoflagellate Prorocentrum lima. Org. Lett. 7:3893-3896. https://doi.org/10.1021/ol051300u
  69. Mallin, M. A., Paerl, H. W. & Rudek, J. 1991. Seasonal phytoplankton composition, productivity and biomass in the Neuse River estuary, North Carolina. Estuar. Coast. Shelf Sci. 32:609-623. https://doi.org/10.1016/0272-7714(91)90078-P
  70. Matsubara, T., Nagasoe, S., Yamasaki, Y., Shikata, T., Shimasaki, Y., Oshima, Y. & Honjo, T. 2007. Effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea. J. Exp. Mar. Biol. Ecol. 342:226-230. https://doi.org/10.1016/j.jembe.2006.09.013
  71. Matsuoka, K., Cho, H. -J. & Jacobson, D. M. 2000. Observations of the feeding behavior and growth rates of the heterotrophic dinoflagellate Polykrikos kofoidii (Polykrikaceae, Dinophyceae). Phycologia 39:82-86. https://doi.org/10.2216/i0031-8884-39-1-82.1
  72. Morton, S. L., Bomber, J. W. & Tindall, P. M. 1994. Environmental effects on the production of okadaic acid from Prorocentrum hoffmannianum Faust I. temperature, light, and salinity. J. Exp. Mar. Biol. Ecol. 178:67-77. https://doi.org/10.1016/0022-0981(94)90225-9
  73. Murakami, Y., Oshima, Y. & Yasumoto, T. 1982. Identification of okadaic acid as a toxic component of a marine dinoflagellate Prorocentrum lima. Bull. Jpn. Soc. Sci. Fish. 48:69-72. https://doi.org/10.2331/suisan.48.69
  74. Nagahama, Y., Murray, S., Tomaru, A. & Fukuyo, Y. 2011. Species boundaries in the toxic dinoflagellate Prorocentrum lima (Dinophyceae, Prorocentrales), based on morphological and phylogenetic characters. J. Phycol. 47:178-189. https://doi.org/10.1111/j.1529-8817.2010.00939.x
  75. Nakamura, Y., Suzuki, S. -Y. & Hiromi, J. 1995. Growth and grazing of a naked heterotrophic dinoflagellate, Gyrodinium dominans. Aquat. Microb. Ecol. 9:157-164. https://doi.org/10.3354/ame009157
  76. Ok, J. H., Jeong, H. J., Lim, A. S. & Lee, K. H. 2017. Interactions between the mixotrophic dinoflagellate Takayama helix and common heterotrophic protists. Harmful Algae 68:178-191. https://doi.org/10.1016/j.hal.2017.08.006
  77. Pearce, I., Handlinger, J. H. & Hallegraeff, G. M. 2005. Histopathology in Pacific oyster (Crassostrea gigas) spat caused by the dinoflagellate Prorocentrum rhathymum. Harmful Algae 4:61-74. https://doi.org/10.1016/j.hal.2003.11.002
  78. Psarra, S., Tselepides, A. & Ignatiades, L. 2000. Primary productivity in the oligotrophic Cretan Sea (NE Mediterranean): seasonal and interannual variability. Prog. Oceanogr. 46:187-204. https://doi.org/10.1016/S0079-6611(00)00018-5
  79. Roselli, L., Vadrucci, M. R., Fanelli, F., Ungaro, N. & Caroppo, C. 2019. First bloom event of the small dinoflagellate Prorocentrum shikokuense in the Mediterranean Sea: cryptogenic or introduced? Mar. Pollut. Bull. 139:197-204. https://doi.org/10.1016/j.marpolbul.2018.12.034
  80. Scheiner, S. M. 1993. MANOVA: multiple response variables and multispecies interactions. In Scheiner, S. M. & Gurevitch, J. (Eds.) Design and Analysis of Ecological Experiments. Chapman and Hall, New York, pp. 94-112.
  81. Sierra-Beltran, A. P., Cortes-Altamirano, R. & Cortes-Lara, M. C. 2005. Occurrences of Prorocentrum minimum (Pavillard) in Mexico. Harmful Algae 4:507-517. https://doi.org/10.1016/j.hal.2004.08.018
  82. Smayda, T. J. 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42:1137-1153. https://doi.org/10.4319/lo.1997.42.5_part_2.1137
  83. Strathmann, R. R. 1967. Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol. Oceanogr. 12:411-418. https://doi.org/10.4319/lo.1967.12.3.0411
  84. Strom, S. L. & Buskey, E. J. 1993. Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol. Oceanogr. 38:965-977. https://doi.org/10.4319/lo.1993.38.5.0965
  85. Sugahara, K., Kitamura, Y., Murata, M., Satake, M. & Tachibana, K. 2011. Prorocentrol, a polyoxy linear carbon chain compound isolated from the toxic dinoflagellate Prorocentrum hoffmannianum. J. Org. Chem. 76:3131-3138. https://doi.org/10.1021/jo102585k
  86. Tango, P. J., Magnien, R., Butler, W., Luckett, C., Luckenbach, M., Lacouture, R. & Poukish, C. 2005. Impacts and potential effects due to Prorocentrum minimum blooms in Chesapeake Bay. Harmful Algae 4:525-531. https://doi.org/10.1016/j.hal.2004.08.014
  87. Tillmann, U. & Hoppenrath, M. 2013. Life cycle of the pseudocolonial dinoflagellate Polykrikos kofoidii (Gymnodiniales, Dinoflagellata). J. Phycol. 49:298-317. https://doi.org/10.1111/jpy.12037
  88. Torigoe, K., Murata, M., Yasumoto, T. & Iwashita, T. 1988. Prorocentrolide, a toxic nitrogenous macrocycle from a marine dinoflagellate, Prorocentrum lima. J. Am. Chem. Soc. 110:7876-7877. https://doi.org/10.1021/ja00231a048
  89. Verni, F. & Gualtieri, P. 1997. Feeding behaviour in ciliated protists. Micron 28:487-504. https://doi.org/10.1016/S0968-4328(97)00028-0
  90. Vila, M. & Maso, M. 2005. Phytoplankton functional groups and harmful algae species in anthropogenically impacted waters of the NW Mediterranean Sea. Sci. Mar. 69:31-45. https://doi.org/10.3989/scimar.2005.69n131
  91. Watts, P. C., Martin, L. E., Kimmance, S. A., Montagnes, D. J. S. & Lowe, C. D. 2010. The distribution of Oxyrrhis marina: a global disperser or poorly characterized endemic? J. Plankton Res. 33:579-589.
  92. Westfall, J. A., Bradbury, P. C. & Townsend, J. W. 1983. Ultrastructure of the dinoflagellate Polykrikos. I. Development of the nematocyst-taeniocyst complex and morphology of the site for extrusion. J. Cell Sci. 63:245-261.
  93. Wyatt, T. & Zingone, A. 2014. Population dynamics of red tide dinoflagellates. Deep Sea Res. Part II: Top. Stud. Oceanogr. 101:231-236. https://doi.org/10.1016/j.dsr2.2013.09.021
  94. Yasumoto, T., Seino, N., Murakami, Y. & Murata, M. 1987. Toxins produced by benthic dinoflagellates. Biol. Bull. 172:128-131. https://doi.org/10.2307/1541612
  95. Yoo, Y. D., Jeong, H. J., Kang, N. S., Kim, J. S., Kim, T. H. & Yoon, E. Y. 2010. Ecology of Gymnodinium aureolum. II. Predation by common heterotrophic dinoflagellates and a ciliate. Aquat. Microb. Ecol. 59:257-272. https://doi.org/10.3354/ame01401
  96. Zingone, A., Siano, R., D'Alelio, D. & Sarno, D. 2006. Potentially toxic and harmful microalgae from coastal waters of the Campania region (Tyrrhenian Sea, Mediterranean Sea). Harmful Algae 5:321-337. https://doi.org/10.1016/j.hal.2005.09.002