Skip to main content
Log in

Repeated reaching of the harmful algal bloom of Karenia spp. around the Pacific shoreline of Kushiro, eastern Hokkaido, Japan, during autumn 2021

  • Original Article
  • Environment
  • Published:
Fisheries Science Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Brand LE, Campbell L, Bresnan E (2012) Karenia: the biology and ecology of a toxic genus. Harmful Algae 14:156–178

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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)

    Article  Google Scholar 

  • Grasshoff K, Ehrhardt M, Kremling K (1999) Methods of sea water analysis, 3rd edn. Verlag Chemie, Weinheim

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Huang KX, Xie YH (2009) Effects of nitrogen availability on growth of Karenia mikimotoi. Ecol Enviro Sci 18(2):453–457

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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)

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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)

    Google Scholar 

  • Kakuta T (1984) Tokachi engan no akashiwo ni tsuite (Red tides in Tokachi coast). Kushiro Suishi Dayori 52:17–20 (in Japanese)

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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)

    Article  Google Scholar 

  • Oda T (2012) Physiological and biochemical studies on toxic factors produced by red tide phytoplankton. Nippon Suisan Gakkaishi 78(3):368–371 (in Japanese)

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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)

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • Tazawa N (1972) Akashio Ni Tsuite. Kushiro Suishi Dayori 30:3–5 (in Japanese)

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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)

    Google Scholar 

  • 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)

    Google Scholar 

  • 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)

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Natsuki Hasegawa.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-022-01642-w

Keywords

Navigation