Abstract
Unprecedented large-scale algal blooms were observed during autumn 2021 around the Katsurakoi fishing port, Kushiro, eastern Hokkaido, Japan. Monitoring of shoreline water showed that chlorophyll a (Chl a) concentrations and the cell density of Karenia spp., dominated by Karenia selliformis, repeatedly increased synchronously between September and November 2021. These increases were associated with a southerly wind-driven current, which transported offshore water on the shelf towards the shoreline at the sea surface. The blooms were prolonged as a result of algal accumulation in the semi-closed fishing port. The maximum Chl a concentration and cell density exceeded 50 µg Chl a/L and 104 cells/mL, respectively. During the autumn bloom of Karenia spp., the nitrate + nitrite and phosphate concentrations in the water were lower than those in 2019 and 2020, and the silicate concentration was comparable. The ammonium concentration during the bloom was notably higher than before the bloom period, reaching 15 µM. Mass mortality of several fish species and echinoderms that were cultured using rearing water intake from the same shoreline occurred synchronously with the increase in Karenia spp.
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References
Brand LE, Campbell L, Bresnan E (2012) Karenia: the biology and ecology of a toxic genus. Harmful Algae 14:156–178
Carreto JJ, Benavides HR, Negri RM, Glorioso PD (1986) Toxic red-tide in the Argentine Sea phytoplankton distribution and survival of the toxic dinoflagellate Gonyaulax excavate in a frontal area. J Plankton Res 8(1):15–28. https://doi.org/10.1093/plankt/8.1.15
Davidson K, Gowen RJ, Harrison PJ, Fleming LE, Hoagland P, Moschonas G (2014) Anthropogenic nutrients and harmful algae in coastal waters. J Environ Manag 146:206–216
Geesey M, Tester PA (1993) Gymnodinium breve: ubiquitous in Gulf of Mexico waters? In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier Science Publishers B.V., Amsterdam, pp 251–255
Go J, Nagai K, Segawa S, Honjo T (2016) Mortality and impact on life activity of Akoya pearl oysters caused by red tides of dinoflagellate Karenia mikimotoi. Nippon Suisan Gakkai Shi 82(5):737–742 (in Japanese with English abstracts)
Grasshoff K, Ehrhardt M, Kremling K (1999) Methods of sea water analysis, 3rd edn. Verlag Chemie, Weinheim
Hetland RD, Campbell L (2007) Convergent blooms of Karenia brevis along the Texas coast. Geophys Res Lett 34:LI19604. https://doi.org/10.1029/2007GL030474
Howarth RW, Marino R (2006) Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limnol Oceanogr 51(1):364–376. https://doi.org/10.4319/lo.2006.51.1_part_2.0364
Huang KX, Xie YH (2009) Effects of nitrogen availability on growth of Karenia mikimotoi. Ecol Enviro Sci 18(2):453–457
Imai I, Yamaguchi M, Hori Y (2006) Eutrophication and occurrences of harmful algal blooms in the Seto Inland Sea, Japan. Plankton Benthos Res 1:71–84
Ishida N, Yamatogi T, Ura K, Hirae S, Aoki K, Koike K (2017) Mortality factors of cultured bluefin tuna Thunnus orientalis in the coastal area of Tsushima, Nagasaki Prefecture, Japan. Nippon Suisan Gakkai Shi 83(1):41–51 (in Japanese with English abstracts)
Iwataki M, Lum QM, Kuwata K, Takahashi K, Arima D, Kuribayashi T, Kosaka Y, Hasegawa N, Watanabe T, Shikata T, Isada T, Orlova TY, Sakamot S (2022) Morphological variation and phylogeny of Karenia selliformis (Gymnodiniales, Dinophyceae) in an intensive cold-water algal bloom in eastern Hokkaido, Japan. Harmful Algae 114:102204. https://doi.org/10.1016/j.hal.2022.102204
Kakumu A, Morita K, Shimada H, Yamaguchi A, Imai I (2018) First detection of the noxious red tide dinoflagellate Karenia mikimotoi and bloom dynamics in 2015 and 2016 in Hakodate Bay, Hokkaido, northern Japan. Bull Plankton Soc Japan 65:1–11 (in Japanese with English abstracts)
Kakuta T (1984) Tokachi engan no akashiwo ni tsuite (Red tides in Tokachi coast). Kushiro Suishi Dayori 52:17–20 (in Japanese)
Katano T, Yoshida M, Lee J, Han M-S, Hayami Y (2009) Fixation of Chattonella antiqua and C. marina (Raphidophyceae) using Hepes-buffered paraformaldehyde and glutaraldehyde for flow cytometry and light microscopy. Phycologia 48:473–479. https://doi.org/10.2216/08-633102.1
Kim D, Li W, Matsuyama Y, Matsuo A, Yagi M, Cho K, Yamasaki Y, Takeshita S, Yamaguchi K, Oda T (2020) Strain-dependent lethal effects on abalone and haemolytic activities of the dinoflagellate Karenia mikimotoi. Aquaculture 520:734953. https://doi.org/10.1016/j.aquaculture.2020.734953
Kimura B, Kamizono M, Etoh T, Koizumi Y, Murakami M, Honjo T (1999) Population development of the red tide dinoflagellate Gymnodinium mikimotoi in inshore waters of Japan. Plankton Biol Ecol 46(1):37–47
Kuroda H, Setou T (2021) Extensive marine heatwaves at the sea surface in the northwestern Pacific Ocean in summer 2021. Remote Sensing 13:3989. https://doi.org/10.3390/rs13193989
Kuroda H, Azumaya T, Setou T, Hasegawa N (2021) Unprecedented outbreak of harmful algae in Pacific coastal waters off southeast Hokkaido, Japan, during late summer 2021 after record-breaking marine heatwaves. J Mar Sci Eng 9:1335. https://doi.org/10.3390/jmse9121335
Kuroda H, Taniuchi Y, Watanabe T, Azumaya T, Hasegawa N (2022) Distribution of harmful algae (Karenia spp.) in October 2021 off Southeast Hokkaido, Japan. Front Mar Sci 9:841364. https://doi.org/10.3389/fmars.2022.841364
Kusaka A, Azumaya T, Kawasaki T (2013) Monthly variations of hydrographic structures and water mass distribution off the Doto area, Japan. J Ocean 69(3):295–312
Kusakari M. (1994) Tokachi engan no akashiwo ni tsuite (Red tides in Tokachi coast). Shiken kenkyu ha ima 17 (in Japanese)
Lecorre P, Lhelguen S, Wafar M (1993) Nitrogen source for uptake by Gyrodinium cf aureolum in a tidal front. Limnol Oceanogr 38:446–451
Li X, Yan T, Yu R, Zhou M (2019) A review of Karenia mikimotoi: Bloom events, physiology, toxicity and toxic mechanism. Harmful Algae 90:101702
Lundholm N, Churro C, Fraga S, Hoppenrath M, Iwataki M, Larsen J, Mertens K, Moestrup Ø, Zingone A. (Eds) (2009 onwards). IOC-UNESCO Taxonomic Reference List of Harmful Micro Algae. Accessed at https://www.marinespecies.org/hab on 2022-03-07. https://doi.org/10.14284/362
Matsuyama Y, Nagai K, Mizuguchi T, Fujiwara M, Ishimura M, Yamaguchi M, Uchida T, Honjo T (1995) Ecological features and mass mortality of pearl oysters during red tides of Heterocapsa sp. in Ago Bay in 1992. Nippon Suisan Gakkaishi 61(1):35–41 (in Japanese with English Abstract)
Oda T (2012) Physiological and biochemical studies on toxic factors produced by red tide phytoplankton. Nippon Suisan Gakkaishi 78(3):368–371 (in Japanese)
Pitcher GC, Boyd AJ, Horstman DA, Mitchell-Innes BA (1998) Subsurface dinoflagellate populations, frontal blooms and the formation of red tide in the southern Benguela upwelling system. Mar Ecol Prog Ser 172:253–264
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Robin RS, Kanuri VV, Muduli PR, Mishra RK, Jaikumar M, Karthikeyan P, Kumar CS, Kumar CS (2013) Dinoflagellate bloom of Karenia mikimotoi along the southeast Arabian Sea, bordering western India. J Ecosystems 2013:463720. https://doi.org/10.1155/2013/463720
Shi F, McNabb P, Rhodes L, Holland P, Webb S, Adamson J, Immers A, Gooneratne R, Holland J (2012) The toxic effects of three dinoflagellate species from the genus Karenia on invertebrate larvae and finfish. N Z J Mar Freshwater Res 46(2):149–165
Shikata T, Sakamoto S, Onitsuka G, Aoki K, Yamaguichi M (2014) Effects of salinity on diel vertical migration behavior in two red-tide algae Chattonella Antiqua Karenia Mikimotoi. Plankton Benthos Res 9(1):42–50
Shimada H, Kanamori M, Yoshida H, Imai I (2016) First record of red tide due to the harmful dinoflagellate Karenia mikimotoi in Hakodate Bay, southern Hokkaido, in autumn 2015. Nippon Suisan Gakkai Shi 82(6):934–938 (in Japanese with English abstracts)
Steidinger KA, Vargo GA, Tester PA (1998) Bloom dynamics and physiology of Gymnodinium breve with emphasis on the Gulf of Mexico. In: Anderson DM, Cembella AC, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms. Springer, Heidelberg, pp 133–153
Stumpf RP, Litaker RW, Lanerolle L, Tester PA (2008) Hydrodynamic accumulation of Karenia off the west coast of Florida. Cont Shelf Res 28:189–213
Takasugi S, Kakuta T (1986) Tokachi engan no akashiwo yosatsu ni tsuite (prediction of red tides in Tokachi coast). Kushiro Suishi Dayori 56:8–11 (in Japanese)
Tazawa N (1972) Akashio Ni Tsuite. Kushiro Suishi Dayori 30:3–5 (in Japanese)
Yamaguchi M, Itakura S (1999) Nutrition and growth kinetics in nitrogen- or phosphorus-limited cultures of the noxious red tide dinoflagellate Gymnodinium mikimotoi. Fish Sci 65:367–373
Yamaguchi A, Hamao Y, Matsuno K, Iida T (2022) Horizontal distribution of harmful red-tide Karenia selliformis and phytoplankton community along the Pacific coast of Hokkaido in autumn 2021. Bull Jpn Soc Fish Oceanogr 86:41–49 (in Japanese with English abstracts)
Yamatogi T, Ishida N, Hirae S, Sugihara Y, Kamada M, Nishiyama K, Aoki K (2016) Environmental features and mass mortality of cultured fish during Karenia mikimotoi bloom in the Imari Bay. Japan Jpn J Phycol 64:94–101 (in Japanese with English abstracts)
Yoshida Y, Numata K (1982) Effect of wind on the accumulation of Chattonella antiqua (HADA) ONO. Nippon Suisan Gakkai Shi 48:1277–1280. https://doi.org/10.2331/suisan.48 (in Japanese with English abstracts)
Zhao Y, Tang X, Zhao Y, Wang Y (2017) Effect of various nitrogen conditions on population growth, temporary cysts and cellular biochemical compositions of Karenia mikimotoi. PLoS One 12(2):e0171996. https://doi.org/10.1371/journal.pone.0171996
Acknowledgements
We are grateful to the assistant staff of Kushiro Field Station and Hatsukaichi Field Stations, FRA, for supporting analyses of the water samples. This study was conducted by the urgent project by the Japan Fisheries Research and Education Agency and the Hokkaido Harmful Algal Bloom Emergency Support Project by the Fisheries Agency of Japan. We thank Marianne Fish, PhD, from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.
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Hasegawa, N., Watanabe, T., Unuma, T. et al. Repeated reaching of the harmful algal bloom of Karenia spp. around the Pacific shoreline of Kushiro, eastern Hokkaido, Japan, during autumn 2021. Fish Sci 88, 787–803 (2022). https://doi.org/10.1007/s12562-022-01642-w
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DOI: https://doi.org/10.1007/s12562-022-01642-w