Allelopathic effects of mixotrophic dinoflagellate Akashiwo sanguinea on co-occurring phytoplankton: the significance of nutritional ecology

Abstract

Blooms of Akashiwo sanguinea frequently break out around the world, causing huge economic losses to the aquaculture industry and seriously damaging coastal ecosystems. However, the formation mechanisms of A. sanguinea blooms remain unclear. We investigated the allelopathic effects of A. sanguinea on multiple phytoplankton species, explored the mode of allelochemicals action and the way of nutrient factors regulation of the allelopathic activity. Results show that strains of A. sanguinea could inhibit the growth of co-occurring phytoplankton including Scrippsiella trochoidea, Phaeocystis globosa, and Rhodomonas salina, but inhibition of Prorocentrum micans was not obvious. The inhibition rates on phytoplankton were positively correlated with the cell densities of A. sanguinea. The highest inhibition rate of 94% on R. salina was for A. sanguinea CCMA256 culture of 2 000 cells/mL at 72 h. We observed that cells of S. trochoidea, Ph. globosa, and R. salina were lysed when co-cultured with A. sanguinea, with the shortest time for S. trochoidea. Additionally, the growth rates of A. sanguinea were promoted by co-culturing with S. trochoidea, Ph. globosa, and R. salina. Four components of A. sanguinea culture were all able to inhibit growth of R. salina: the strongest inhibitory effect was found in the sonicated culture, followed by whole-cell culture, filtrates of sonicated culture, and filtrate culture. The crude extract of A. sanguinea culture also lysed cells of R. salina, and the inhibition rates on R. salina increased with the increasing dose of crude extract. It was shown that both nutrient enrichment and nitrogen:phosphorus ratio imbalance enhanced remarkably the allelopathic activity of A. sanguinea. The highest inhibition rate on R. salina of 70% occurred in A. sanguinea JX13 treatment at 2 000 cells/mL under high nutrient condition in 48 h. In JX14 treatment at 2 000 cells/mL for N:P of 10:1, the inhibition rate increased by 1.7 times of that for N:P of 20:1. In addition, the allelopathy of A. sanguinea could not only be a competitive strategy but also a nutrition strategy, playing an important role in formation and/or maintenance of blooms of the mixotrophic dinoflagellate A. sanguinea.

This is a preview of subscription content, access via your institution.

References

  1. Accoroni S, Glibert P M, Pichierri S, Romagnoli T, Marini M, Totti C. 2015. A conceptual model of annual Ostreopsis cf. ovata blooms in the northern Adriatic Sea based on the synergic effects of hydrodynamics, temperature, and the N:P ratio of water column nutrients. Harmful Algae, 45: 14–25, https://doi.org/10.1016/j.hal.2015.04.002.

    Article  Google Scholar 

  2. Adolf J E, Bachvaroff T R, Krupatkina D N, Nonogaki H, Brown P J P, Lewitus A J, Harvey H R, Place A R. 2006. Species specificity and potential roles of Karlodinium micrum toxin. African Journal of Marine Science, 28(2): 415–419, https://doi.org/10.2989/18142320609504189.

    Article  Google Scholar 

  3. Adolf J E, Krupatkina D, Bachvaroff T, Place A R. 2007. Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae, 6(3): 400–412, https://doi.org/10.1016/j.hal.2006.12.003.

    Article  Google Scholar 

  4. Anderson D M, Burkholder J M, Cochlan W P, Glibert P M, Gobler C J, Heil C A, Kudela R M, Parsons M L, Rensel J E J, Townsend D W, Trainer V L, Vargo G A. 2008. Harmful algal blooms and eutrophication: examining linkages from selected coastal regions of the United States. Harmful Algae, 8(1): 39–53, https://doi.org/10.1016/j.hal.2008.08.017.

    Article  Google Scholar 

  5. Badylak S, Phlips E J, Mathews A L. 2014. Akashiwo sanguinea (Dinophyceae) blooms in a sub-tropical estuary: an alga for all seasons. Plankton and Benthos Research, 9(3): 147–155, https://doi.org/10.3800/pbr9.147.

    Article  Google Scholar 

  6. Berge T, Poulsen L K, Moldrup M, Daugbjerg N, Juel H P. 2012. Marine microalgae attack and feed on metazoans. The ISME Journal, 6(10): 1 926–1 936, https://doi.org/10.1038/ismej.2012.29.

    Article  Google Scholar 

  7. Bockstahler K R, Coats D W. 1993. Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. Marine Biology, 116(3): 477–487, https://doi.org/10.1007/BF00350065.

    Article  Google Scholar 

  8. Botes L, Smit A J, Cook P A. 2003. The potential threat of algal blooms to the abalone (Haliotis midae) mariculture industry situated around the South African coast. Harmful Algae, 2(4): 247–259, https://doi.org/10.1016/s1568-9883(03)00044-1.

    Article  Google Scholar 

  9. Burkholder J M, Glibert P M, Skelton H M. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae, 8(1): 77–93, https://doi.org/10.1016/j.hal.2008.08.010.

    Article  Google Scholar 

  10. Castro N O, Domingos P, Moser G A O. 2016. National and international public policies for the management of harmful algal bloom events. A case study on the Brazilian coastal zone. Ocean & Coastal Management, 128: 40–51, https://doi.org/10.1016/j.ocecoaman.2016.04.016.

    Article  Google Scholar 

  11. Chakraborty S, Feudel U. 2014. Harmful algal blooms: combining excitability and competition. Theoretical Ecology, 7(3): 221–237, https://doi.org/10.1007/s12080-014-0212-1.

    Article  Google Scholar 

  12. Chen T T, Liu Y, Song S Q, Li C W, Tang Y Z, Yu Z M. 2015. The effects of major environmental factors and nutrient limitation on growth and encystment of planktonic dinoflagellate Akashiwo sanguinea. Harmful Algae, 46: 62–70, https://doi.org/10.1016/j.hal.2015.05.006.

    Article  Google Scholar 

  13. Driscoll W W, Espinosa N J, Eldakar O T, Hackett J D. 2013. Allelopathy as an emergent, exploitable public good in the bloom-forming microalga Prymnesium parvum. Evolution, 67(6): 1 582–1 590, https://doi.org/10.1111/evo.12030.

    Article  Google Scholar 

  14. Du X N, Peterson W, McCulloch A, Liu G X. 2011. An unusual bloom of the dinoflagellate Akashiwo sanguinea off the central Oregon, USA, coast in autumn 2009. Harmful Algae, 10(6): 784–793, https://doi.org/10.1016/j.hal.2011.06.011.

    Article  Google Scholar 

  15. Fistarol G O, Legrand C, Selander E, Hummert C, Stolte W, Graneli E. 2004. Allelopathy in Alexandrium spp.: effect on a natural plankton community and on algal monocultures. Aquatic Microbial Ecology, 35(1): 45–56, https://doi.org/10.3354/ame035045.

    Article  Google Scholar 

  16. Fleming L E, Broad K, Clement A, Dewailly E, Elmir S, Knap A, Pomponi S A, Smith S, Solo Gabriele H, Walsh P. 2006. Oceans and human health: emerging public health risks in the marine environment. Marine Pollution Bulletin, 53(10–12): 545–560, https://doi.org/10.1016/j.marpolbul.2006.08.012.

    Article  Google Scholar 

  17. Flynn K J, Stoecker D K, Mitra A, Raven J A, Glibert P M, Hansen P J, Granéli E, Burkholder J M. 2013. Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. Journal of Plankton Research, 35(1): 3–11, https://doi.org/10.1093/plankt/fbs062.

    Article  Google Scholar 

  18. Galloway J N, Cowling E B, Seitzinger S P, Socolow R H. 2002. Reactive nitrogen: too much of a good thing? Ambio A Journal of the Human Environment, 31(2): 60–63, https://doi.org/10.1579/0044-7447-31.2.60.

    Article  Google Scholar 

  19. Glibert P M, Allen J I, Bouwman A F, Brown C W, Flynn K J, Lewitus A J, Madden C J. 2010. Modeling of HABs and eutrophication: status, advances, challenges. Journal of Marine Systems, 83(3–4): 262–275, https://doi.org/10.1016/j.jmarsys.2010.05.004.

    Article  Google Scholar 

  20. Glibert P M, Beusen A H W, Harrison J A, Dürr H H, Bouwman A F, Laruelle G G. 2018. Changing land-, sea-, and airscapes: sources of nutrient pollution affecting habitat suitability for harmful algae. In: Glibert P M, Berdalet E, Burford M A, Pitcher G C, Zhou M J eds. Global Ecology and Oceanography of Harmful Algal Blooms. Cham: Springer. p.53–76.

    Google Scholar 

  21. Glibert P M, Burkholder J A M, Kana T M, Alexander J, Skelton H, Shilling C. 2009. Grazing by Karenia brevis on Synechococcus enhances its growth rate and may help to sustain blooms. Aquatic Microbial Ecology, 55(1): 17–30, https://doi.org/10.3354/ame01279.

    Article  Google Scholar 

  22. Glibert P M, Maranger R, Sobota D J, Bouwman L. 2014. The Haber Bosch-harmful algal bloom (HB-HAB) link. Environmental Research Letters, 9(10): 105001, https://doi.org/10.1088/1748-9326/9/10/105001.

    Article  Google Scholar 

  23. Gobler C J, Sunda W G. 2012. Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis. Harmful Algae, 14: 36–45, https://doi.org/10.1016/j.hal.2011.10.013.

    Article  Google Scholar 

  24. Gómez F, Boicenco L. 2004. An annotated checklist of dinoflagellates in the Black Sea. Hydrobiologia, 517(1–3): 43–59, https://doi.org/10.1023/b:hydr.0000027336.05452.07.

    Article  Google Scholar 

  25. Granéli E, Hansen P J. 2006. Allelopathy in harmful algae: a mechanism to compete for resources? In: Granéli E, Turner J T eds. Ecology of Harmful Algae. Berlin, Heidelberg: Springer-Verlag. p.189–201.

    Google Scholar 

  26. Granéli E, Johansson N. 2003. Increase in the production of allelopathic substances by Prymnesium parvum cells grown under N- or P-deficient conditions. Harmful Algae, 2(2): 135–145, https://doi.org/10.1016/s1568-9883(03)00006-4.

    Article  Google Scholar 

  27. Granéli E, Salomon P S. 2010. Factors influencing allelopathy and toxicity in Prymnesium parvum. JAWRA Journal of the American Water Resources Association, 46(1): 108–120, https://doi.org/10.1111/j.1752-1688.2009.00395.x.

    Article  Google Scholar 

  28. Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith W L, Chanley M H eds. Culture of Marine Invertebrate Animals. Boston: Springer. p.29–60.

    Google Scholar 

  29. Hakanen P, Suikkanen S, Kremp A. 2014. Allelopathic activity of the toxic dinoflagellate Alexandrium ostenfeldii: intrapopulation variability and response of co-occurring dinoflagellates. Harmful Algae, 39: 287–294, https://doi.org/10.1016/j.hal.2014.08.005.

    Article  Google Scholar 

  30. Hallegraeff G M. 1992. Harmful algal blooms in the Australian region. Marine Pollution Bulletin, 25(5–8): 186–190, https://doi.org/10.1016/0025-326X(92)90223-S.

    Article  Google Scholar 

  31. Hallegraeff G M. 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. Journal of Phycology, 46(2): 220–235, https://doi.org/10.1111/j.1529-8817.2010.00815.x.

    Article  Google Scholar 

  32. Hansen P J, Hjorth M. 2002. Growth and grazing responses of Chrysochromulina ericina (Prymnesiophyceae): the role of irradiance, prey concentration and pH. Marine Biology, 141(5): 975–983, https://doi.org/10.1007/s00227-002-0879-5.

    Article  Google Scholar 

  33. Harper Jr D E, Guillen G. 1989. Occurrence of a dinoflagellate bloom associated with an influx of low salinity water at Galveston, Texas, and coincident mortalities of demersal fish and benthic invertebrates. Contributions in Marine Science, 31: 147–161.

    Google Scholar 

  34. Hattenrath-Lehmann T K, Gobler C J. 2011. Allelopathic inhibition of competing phytoplankton by North American strains of the toxic dinoflagellate, Alexandrium fundyense: evidence from field experiments, laboratory experiments, and bloom events. Harmful Algae, 11: 106–116. https://doi.org/10.1016/j.hal.2011.08.005.

    Article  Google Scholar 

  35. Heisler J, Glibert P M, Burkholder J M, Anderson D M, Cochlan W, Dennison W C, Dortch Q, Gobler C J, Heil C A, Humphries E, Lewitus A, Magnien R, Marshall H G, Sellner K, Stockwell D A, Stoecker D K, Suddleson M. 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae, 8(1): 3–13, https://doi.org/10.1016/j.hal.2008.08.006.

    Article  Google Scholar 

  36. 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(3): 256–262, https://doi.org/10.2216/i0031-8884-40-3-256.1.

    Article  Google Scholar 

  37. Hodgkiss I J, Lu S H. 2004. The effects of nutrients and their ratios on phytoplankton abundance in Junk Bay, Hong Kong. Hydrobiologia, 512(1–3): 215–229, https://doi.org/10.1023/B:HYDR.0000020330.37366.e5.

    Article  Google Scholar 

  38. Horner R A, Garrison D L, Plumley F G. 1997. Harmful algal blooms and red tide problems on the U.S. west coast. Limnology and Oceanography, 42(5part2): 1 076–1 088, https://doi.org/10.4319/lo.1997.42.5_part_2.1076.

    Article  Google Scholar 

  39. Jang S H, Jeong H J, Kwon J E, Lee K H. 2017. Mixotrophy in the newly described dinoflagellate Yihiella yeosuensis: a small, fast dinoflagellate predator that grows mixotrophically, but not autotrophically. Harmful Algae, 62: 94–103, https://doi.org/10.1016/j.hal.2016.12.007.

    Article  Google Scholar 

  40. Jeong H J, Du Yoo Y, Kim J S, Kim T H, Kim J H, Kang N S, Yih W. 2004. Mixotrophy in the phototrophic Harmful Alga Cochlodinium polykrikoides (Dinophycean): prey species, the effects of prey concentration, and grazing impact. Journal of Eukaryotic Microbiology, 51(5): 563–569, https://doi.org/10.1111/j.1550-7408.2004.tb00292.x.

    Article  Google Scholar 

  41. Jeong H J, Du Yoo Y, Seong K A, Kim J H, Park J Y, Kim S, Lee S H, Ha J H. 2005a. Feeding by the mixotrophic red-tide dinoflagellate Gonyaulax polygramma: mechanisms, prey species, effects of prey concentration, and grazing impact. Aquatic Microbial Ecology, 38(3): 249–257, https://doi.org/10.3354/ame038249.

    Article  Google Scholar 

  42. Jeong H J, Ok J H, Lim A S, Kwon J E, Kim S J, Lee S Y. 2016. Mixotrophy in the phototrophic dinoflagellate Takayama helix (family Kareniaceae): predator of diverse toxic and harmful dinoflagellates. Harmful Algae, 60: 92–106, https://doi.org/10.1016/j.hal.2016.10.008.

    Article  Google Scholar 

  43. 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. 2005b. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquatic Microbial Ecology, 41(2): 131–143, https://doi.org/10.3354/ame041131.

    Article  Google Scholar 

  44. Jessup D A, Miller M A, Ryan J P, Nevins H M, Kerkering H A, Mekebri A, Crane D B, Johnson T A, Kudela R M. 2009. Mass stranding of marine birds caused by a surfactant-producing red tide. PLoS One, 4(2): e4550, https://doi.org/10.1371/journal.pone.0004550.

    Article  Google Scholar 

  45. Kahru M, Michell B G, Diaz A, Miura M. 2004. MODIS detects a devastating algal bloom in Paracas Bay, Peru. Eos, 85(45): 465–472, https://doi.org/10.1029/2004EO450002.

    Article  Google Scholar 

  46. Katano T, Yoshida M, Yamaguchi S, Hamada T, Yoshino K, Hayami Y. 2011. Diel vertical migration and cell division of bloom-forming dinoflagellate Akashiwo sanguinea in the Ariake Sea, Japan. Plankton and Benthos Research, 6(2): 92–100, https://doi.org/10.3800/pbr6.92.

    Article  Google Scholar 

  47. Kim J H, Jeong H J, Lim A S, Rho J R, Lee S B. 2016. Killing potential protist predators as a survival strategy of the newly described dinoflagellate Alexandrium pohangense. Harmful Algae, 55: 41–55, https://doi.org/10.1016/j.hal.2016.01.009.

    Article  Google Scholar 

  48. Kubanek J, Hicks M K, Naar J, Villareal T A. 2005. Does the red tide dinoflagellate Karenia brevis use allelopathy to outcompete other phytoplankton? Limnology and Oceanography, 50(3): 883–895, https://doi.org/10.4319/lo.2005.50.3.0883.

    Article  Google Scholar 

  49. Legrand C, Rengefors K, Fistarol G O, Granéli E. 2003. Allelopathy in phytoplankton-biochemical, ecological and evolutionary aspects. Phycologia, 42(4): 406–419, https://doi.org/10.2216/i0031-8884-42-4-406.1.

    Article  Google Scholar 

  50. Leong S C Y, Murata A, Nagashima Y, Taguchi S. 2004. Variability in toxicity of the dinoflagellate Alexandrium tamarense in response to different nitrogen sources and concentrations. Toxicon, 43(4): 407–415, https://doi.org/10.1016/j.toxicon.2004.01.015.

    Article  Google Scholar 

  51. 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, https://doi.org/10.1016/j.hal.2018.03.009.

    Article  Google Scholar 

  52. 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. Journal of Experimental Marine Biology and Ecology, 342(2): 226–230, https://doi.org/10.1016/j.jembe.2006.09.013.

    Article  Google Scholar 

  53. 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(1): 82–86, https://doi.org/10.2216/i0031-8884-39-1-82.1.

    Article  Google Scholar 

  54. 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.

    Article  Google Scholar 

  55. Ou G Y, Wang H, Si R R, Guan W C. 2017. The dinoflagellate Akashiwo sanguinea will benefit from future climate change: the interactive effects of ocean acidification, warming and high irradiance on photophysiology and hemolytic activity. Harmful Algae, 68: 118–127, https://doi.org/10.1016/j.hal.2017.08.003.

    Article  Google Scholar 

  56. Park J, Jeong H J, Du Yoo Y et al. 2013. Mixotrophic dinoflagellate red tides in Korean waters: distribution and ecophysiology. Harmful Algae, 30(S1): S28–S40, https://doi.org/10.1016/j.hal.2013.10.004.

    Article  Google Scholar 

  57. Phlips E J, Badylak S, Christman M, Wolny J, Brame J, Garland J, Hall L, Hart J, Landsberg J, Lasi M, Lockwood J, Paperno R, Scheidt D, Staples A, Steidinger K. 2011. Scales of temporal and spatial variability in the distribution of harmful algae species in the Indian River Lagoon, Florida, USA. Harmful Algae, 10(3): 277–290, https://doi.org/10.1016/j.hal.2010.11.001.

    Article  Google Scholar 

  58. Poulin R X, Hogan S, Poulson-Ellestad K L, Brown E, Fernández F M, Kubanek J. 2018. Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors. Scientific Reports, 8(1): 9 572, https://doi.org/10.1038/s41598-018-27845-9.

    Article  Google Scholar 

  59. Prince E K, Myers T L, Kubanek J. 2008. Effects of harmful algal blooms on competitors: allelopathic mechanisms of the red tide dinoflagellate Karenia brevis. Limnology and Oceanography, 53(2): 531–541, https://doi.org/10.4319/lo.2008.53.2.0531.

    Article  Google Scholar 

  60. Remmel E J, Hambright K D. 2012. Toxin-assisted micropredation: experimental evidence shows that contact micropredation rather than exotoxicity is the role of Prymnesium toxins. Ecology Letters, 15(2): 126–132, https://doi.org/10.1111/j.1461-0248.2011.01718.x.

    Article  Google Scholar 

  61. Skovgaard A, Hansen P J. 2003. Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins. Limnology and Oceanography, 48(3): 1 161–1 166, https://doi.org/10.4319/lo.2003.48.3.1161.

    Article  Google Scholar 

  62. Tang Y Z, Gobler C J. 2010. Allelopathic effects of Cochlodinium polykrikoides isolates and blooms from the estuaries of Long Island, New York, on co-occurring phytoplankton. Marine Ecology Progress, 406: 19–31, https://doi.org/10.3354/meps08537.

    Article  Google Scholar 

  63. Tang Y Z, Gobler C J. 2015. Sexual resting cyst production by the dinoflagellate Akashiwo sanguinea: a potential mechanism contributing to the ubiquitous distribution of a harmful alga. Journal of Phycology, 51(2): 298–309, https://doi.org/10.1111/jpy.12274.

    Article  Google Scholar 

  64. Williamson G B, Richardson D. 1988. Bioassays for allelopathy: measuring treatment responses with independent controls. Journal of Chemical Ecology, 14(1): 181–187, https://doi.org/10.1007/BF01022540.

    Article  Google Scholar 

  65. Xu N, Tang Y Z, Qin J L, Duan S S, Gobler C J. 2015. Ability of the marine diatoms Pseudo-nitzschia multiseries and P. pungens to inhibit the growth of co-occurring phytoplankton via allelopathy. Aquatic Microbial Ecology, 74(1): 29–41, https://doi.org/10.3354/ame01724.

    Article  Google Scholar 

  66. Xu N, Wang M, Tang Y Z, Zhang Q, Duan S S, Gobler C J. 2017. Acute toxicity of the cosmopolitan bloom-forming dinoflagellate Akashiwo sanguinea to finfish, shellfish, and zooplankton. Aquatic Microbial Ecology, 80(3): 209–222, https://doi.org/10.3354/ame01846.

    Article  Google Scholar 

  67. Yang C Y, Li Y, Zhou Y Y, Zheng W, Tian Y, Zheng T L. 2012. Bacterial community dynamics during a bloom caused by Akashiwo sanguinea in the Xiamen sea area, China. Harmful Algae, 20: 132–141, https://doi.org/10.1016/j.hal.2012.09.002.

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ning Xu.

Additional information

Supported by the National Natural Science Foundation of China (NSFC) (Nos. 41576159, 41676099)

Data Availability Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Huang, B., Tang, Y. et al. Allelopathic effects of mixotrophic dinoflagellate Akashiwo sanguinea on co-occurring phytoplankton: the significance of nutritional ecology. J. Ocean. Limnol. (2020). https://doi.org/10.1007/s00343-020-0132-4

Download citation

Keywords

  • Akashiwo sanguinea
  • harmful algal blooms
  • mixotrophy
  • allelopathy
  • nutrients