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Effects of irradiance and temperature on the growth and feeding of the obligate mixotrophic dinoflagellate Gymnodinium smaydae

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Abstract

Gymnodinium smaydae is a fast-growing mixotrophic dinoflagellate. This study investigated whether light intensity (0–346 µmol photons m−2 s−1) and temperature (5–35 °C) affect the autotrophic or mixotrophic growth rate or ingestion rate of Gymnodinium smaydae GSSH1005. At all light intensities tested, G. smaydae GSSH1005 showed negative autotrophic growth rates, but positive mixotrophic growth rates when feeding on Heterocapsa rotundata. However, both autotrophic and mixotrophic growth rates were significantly affected by light intensity. The mixotrophic growth rates at 0–6 µmol photons m−2 s−1 were 0.67–0.72 day−1; they increased up to 1.28 day−1 at 58 µmol photons m−2 s−1, but became saturated at higher light intensities. The ingestion rates were also significantly affected by light intensity. The maximum ingestion rate of 2.3 ng C predator−1 day−1 was achieved at 58 µmol photons m−2 s−1. Although the autotrophic growth rates were negative at all temperatures tested, the mixotrophic growth rates were positive at 10–32 °C. Both autotrophic and mixotrophic growth rates were significantly affected by temperature. The maximum mixotrophic growth rate of 1.55 day−1 was noted at 25 °C. The ingestion rates were also significantly affected by temperature. The maximum ingestion rate of 4.2 ng C predator−1 day−1 was noted at 32 °C. Therefore, both light intensity and temperature can affect the population dynamics of G. smaydae GSSH1005.

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Data were obtained from this study, Skovgaard (1996, 2000), Li et al. (1999), Jakobsen et al. (2000), Kim et al. (2008), Jeong et al. (2018a), Lim et al. (2019b), and Ok et al. (2019)

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Data availability

Data collected and analyzed during this current study are available from the corresponding author on reasonable request.

References

  • Adolf JE, Stoecker DK, Harding LW Jr (2006) The balance of autotrophy and heterotrophy during mixotrophic growth of Karlodinium micrum (Dinophyceae). J Plankton Res 28:737–751

    CAS  Google Scholar 

  • Allen JR, Roberts TM, Loeblich AR III, Klotz LC (1975) Characterization of the DNA from the dinoflagellate Crypthecodinium cohnii and implications for nuclear organization. Cell 6:161–169

    CAS  PubMed  Google Scholar 

  • Baek SH, Shimode S, Kikuchi T (2008) Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of temperature, light intensity and photoperiod. Harmful Algae 7:163–173

    Google Scholar 

  • Band-Schmidt CJ, Morquecho L, Lechuga-Devéze CH, Anderson DM (2004) Effects of growth medium, temperature, salinity and seawater source on the growth of Gymnodinium catenatum (Dinophyceae) from Bahía Concepción, Gulf of California, Mexico. J Plankton Res 26:1459–1470

    Google Scholar 

  • Berge T, Hansen PJ (2016) Role of the chloroplasts in the predatory dinoflagellate Karlodinium armiger. Mar Ecol Prog Ser 549:41–54

    CAS  Google Scholar 

  • Berge T, Hansen PJ, Moestrup Ø (2008) Feeding mechanism, prey specificity and growth in light and dark of the plastidic dinoflagellate Karlodinium armiger. Aquat Microb Ecol 50:279–288

    Google Scholar 

  • Blasco D (1978) Observations on the diel migration of marine dinoflagellates off the Baja California coast. Mar Biol 46:41–47

    Google Scholar 

  • Bockstahler KR, Coats DW (1993) Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate population of Chesapeake Bay. Mar Biol 116:447–487

    Google Scholar 

  • Box GE (1949) A general distribution theory for a class of likelihood criteria. Biometrika 36:317–346

    CAS  PubMed  Google Scholar 

  • Burkholder JM, Glibert PM, Skelton HM (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77–93

    CAS  Google Scholar 

  • Ding Y, Ren G, Zhao Z, Xu Y, Luo Y, Li Q, Zhang J (2007) Detection, causes and projection of climate change over China: an overview of recent progress. Adv Atmos Sci 24:954–971

    Google Scholar 

  • Dunn OJ (1961) Multiple comparisons among means. J Am Stat Assoc 56:52–64

    Google Scholar 

  • Fagan T, Hastings JW, Morse D (1998) The phylogeny of glyceraldehyde–3–phosphate dehydrogenase indicates lateral gene transfer from cryptomonads to dinoflagellates. J Mol Evol 47:633–639

    CAS  PubMed  Google Scholar 

  • Franklin DJ, Cedrés CMM, Hoegh–Guldberg O (2006) Increased mortality and photoinhibition in the symbiotic dinoflagellates of the Indo–Pacific coral Stylophora pistillata (Esper) after summer bleaching. Mar Biol 149:633–642

    Google Scholar 

  • Frost BW (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

    Google Scholar 

  • Games PA, Howell JF (1976) Pairwise multiple comparison procedures with unequal n’s and/or variances: a Monte Carlo study. J Stat Educ 1:113–125

    Google Scholar 

  • Grzebyk D, Berland B (1996) Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. J Plankton Res 18:1837–1849

    Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Grun. Can J Microbiol 8:229–239

    CAS  PubMed  Google Scholar 

  • Hansen PJ (2011) The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J Euk Microbiol 58:203–214

    CAS  PubMed  Google Scholar 

  • Hansen PJ, Nielsen TG (1997) Mixotrophic feeding of Fragilidium subglobosum (Dinophyceae) on three species of Ceratium: effects of prey concentration, prey species and light intensity. Mar Ecol Prog Ser 147:187–196

    Google Scholar 

  • Harvey EL, Jeong HJ, Menden–Deuer S (2013) Avoidance and attraction: chemical cues influence predator-prey interactions of planktonic protists. Limnol Oceanogr 58:1176–1184

    Google Scholar 

  • Hasle GR (1950) Phototactic vertical migration in marine dinoflagellates. Oikos 2:162–175

    Google Scholar 

  • Heinbokel JF (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

    Google Scholar 

  • Holm-Hansen O (1969) Algae: amounts of DNA and organic carbon in single cells. Science 163:87–88

    CAS  PubMed  Google Scholar 

  • IPCC (2007) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC Secretariat, Geneva, Switzerland

  • IPCC (2013) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK

  • Jacobson DM, Anderson DM (1996) Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J Phycol 32:279–285

    Google Scholar 

  • Jakobsen HH, Hansen PJ, Larsen J (2000) Growth and grazing responses of two chloroplast-retaining dinoflagellates: effect of irradiance and prey species. Mar Ecol Prog Ser 201:121–128

    Google Scholar 

  • Jang SH, Jeong HJ, Kwon JE, Lee KH (2017a) Mixotrophy in the newly described dinoflagellate Yihiella yeosuensis: a small, fast dinoflagellate predator that grows mixotrophically, but not autotrophically. Harmful Algae 62:94–103

    PubMed  Google Scholar 

  • Jang SH, Jeong HJ, Moestrup Ø, Kang NS, Lee SY, Lee KH, Seong KA (2017b) Yihiella yeosuensis gen. et sp. nov. (Suessiaceae, Dinophyceae), a novel dinoflagellate isolated from the coastal waters of Korea. J Phycol 53:131–145

    CAS  PubMed  Google Scholar 

  • Jeong HJ, Shim JH, Kim JS, Park JY, Lee CW, Lee Y (1999) The feeding by the thecate mixotrophic dinoflagellate Fragilidium cf. mexicanum on redtide and toxic dinoflagellate. Mar Ecol Prog Ser 176:263–277

    Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS, Kim TH, Kim JH, Kang NS, Yih WH (2004) Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophycean): prey species, the effects of prey concentration and grazing impact. J Eukaryot Microbiol 51:563–569

    PubMed  Google Scholar 

  • Jeong HJ, Park JY, Nho JH, Park MO, Ha JH, Seong KA, Lee KY, Yih WH (2005a) Feeding by red–tide dinoflagellates on the cyanobacterium Synechococcus. Aquat Microb Ecol 41:131–143

    Google Scholar 

  • Jeong HJ, Yoo YD, Park JY, Song JY, Kim ST, Lee SH, Kim KY, Yih WH (2005b) Feeding by phototrophic red–tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic. Aquat Microb Ecol 40:133–150

    Google Scholar 

  • Jeong HJ, Yoo YD, Seong KA, Kim JH, Park JY, Kim SH, Lee SH, Ha JH, Yih WH (2005c) Feeding by the mixotrophic red–tide dinoflagellate Gonyaulax polygramma: mechanisms, prey species, effects of prey concentration, and grazing impact. Aquat Microb Ecol 38:249–257

    Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS, Seong KA, Kang NS, Kim TH (2010) Growth, feeding, and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci J 45:65–91

    CAS  Google Scholar 

  • Jeong HJ, Yoo YD, Kang NS, Lim AS, Seong KA, Lee SY, Lee MJ, Lee KH, Kim HS, Shin W, Nam SW, Yih W, Lee K (2012) Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc Nat Acad Sci USA 109:12604–12609

    CAS  PubMed  Google Scholar 

  • Jeong HJ, Lim AS, Franks PJ, Lee KH, Kim JH, Kang NS, Lee MJ, Jang SH, Lee SY, Yoon EY, Park JY, Yoo YD, Seong KA, Kwon JE, Jang TY (2015) A hierarchy of conceptual models of red–tide generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97–115

    Google Scholar 

  • Jeong HJ, Ok JH, Lim AS, Kwon JE, Kim SJ, Lee SY (2016) Mixotrophy in the phototrophic dinoflagellate Takayama helix (family Kareniaceae): predator of diverse toxic and harmful dinoflagellates. Harmful Algae 60:92–106

    PubMed  Google Scholar 

  • Jeong HJ, Lee KH, Yoo YD, Kang NS, Song JY, Kim TH, Seong KA, Kim JS, Potvin E (2018a) Effects of light intensity, temperature, and salinity on the growth and ingestion rates of the red–tide mixotrophic dinoflagellate Paragymnodinium shiwhaense. Harmful Algae 80:46–54

    PubMed  Google Scholar 

  • Jeong HJ, You JH, Lee KH, Kim SJ, Lee SY (2018b) Feeding by common heterotrophic protists on the mixotrophic alga Gymnodinium smaydae (Dinophyceae), one of the fastest growing dinoflagellates. J Phycol 54:734–743

    PubMed  Google Scholar 

  • Johnson MD (2011) The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynth Res 107:117–132

    CAS  PubMed  Google Scholar 

  • Johnson MD (2015) Inducible mixotrophy in the dinoflagellate Prorocentrum minimum. J Eukaryot Microbiol 62:431–443

    PubMed  Google Scholar 

  • Kamykowski D (1981) Laboratory experiments on the diurnal vertical migration of marine dinoflagellates through temperature gradients. Mar Biol 62:57–64

    Google Scholar 

  • Kamykowski D, Zentara SJ (1977) The diurnal vertical migration of motile phytoplankton through temperature gradients. Limnol Oceanogr 22:148–151

    Google Scholar 

  • Kang NS, Lee KH, Jeong HJ, Yoo YD, Seong KA, Potvin É, Hwang Y, Yoon EY (2013) Red tides in Shiwha Bay, western Korea: a huge dike and tidal power plant established in a semi-enclosed embayment system. Harmful Algae 30S:114–130

    Google Scholar 

  • Kang NS, Jeong HJ, Moestrup Ø, Lee SY, Lim AS, Jang TY, Lee KH, Lee MJ, Jang SH, Potvin E, Lee SK, Noh JH (2014) Gymnodinium smaydae n. sp., a new planktonic phototrophic dinoflagellate from the coastal waters of western Korea: morphology and molecular characterization. J Eukaryot Microbiol 61:182–203

    CAS  PubMed  Google Scholar 

  • Kang HC, Jeong HJ, Jang SH, Lee KH (2019) Feeding by common heterotrophic protists on the phototrophic dinoflagellate Biecheleriopsis adriatica (Suessiaceae) compared to that of other suessioid dinoflagellates. Algae 34:127–140

    Google Scholar 

  • Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618

    CAS  PubMed  Google Scholar 

  • Kibler SR, Litaker RW, Holland WC, Vandersea MW, Tester PA (2012) Growth of eight Gambierdiscus (Dinophyceae) species: effects of temperature, salinity and irradiance. Harmful Algae 19:1–14

    Google Scholar 

  • Kim DI, Matsuyama Y, Nagasoe S, Yamaguchi M, Yoon YH, Oshima Y, Imada N, Honjo T (2004) Effects of temperature, salinity and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae). J Plankton Res 26:61–66

    Google Scholar 

  • Kim S, Kang YG, Kim HS, Yih WH, Coats DW, Park MG (2008) Growth and grazing responses of the mixotrophic dinoflagellate Dinophysis acuminata as functions of light intensity and prey concentration. Aquat Microb Ecol 51:301–310

    Google Scholar 

  • Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583–621

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580

    CAS  PubMed  Google Scholar 

  • Lalli C, Parsons TR (1997) Biological oceanography: an introduction, 2nd edn. The Open University Elsevier Butterworth–Heinemann, Oxford

    Google Scholar 

  • Lee KH, Jeong HJ, Jang TY, Lim AS, Kang NS, Kim JH, Kim KY, Park KT, Lee K (2014) Feeding by the newly described mixotrophic dinoflagellate Gymnodinium smaydae: feeding mechanism, prey species, and effect of prey concentration. J Exp Mar Biol Ecol 459:114–125

    Google Scholar 

  • Lee KH, Jeong HJ, Kang HC, Ok JH, You JH, Park SA (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

    Google Scholar 

  • Lee KH, Jeong HJ, Lee KT, Franks PJS, Seong KA, Lee SY, Lee MJ, Jang SH, Potvin E, Lim AS, Yoon EY, Yoo YD, Kang NS, Kim KY (2019b) Effects of warming and eutrophication on coastal phytoplankton production. Harmful Algae 81:106–118

    PubMed  Google Scholar 

  • Levene H (1961) Robust tests for equality of variances. In: Olkins I (ed) Contributions to probability and statistics: essays in honor of Harold Hotelling. Stanford University Press, Redwood City, pp 279–292

    Google Scholar 

  • Levitus S, Antonov J, Boyer T (2005) Warming of the world ocean, 1955–2003. Geophys Res Lett 32:1–4

    Google Scholar 

  • Li A, Stoecker DK, Adolf JE (1999) Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat Microb Ecol 19:163–176

    Google Scholar 

  • Lim PT, Leaw CP, Usup G, Kobiyama A, Koike K, Ogata T (2006) Effects of light and temperature on growth, nitrate uptake, and toxin production of two tropical dinoflagellates: Alexandrium tamiyavanichii and Alexandrium minutum (dinophyceae). J Phycol 42:786–799

    CAS  Google Scholar 

  • Lim AS, Jeong HJ, Kim JH, Lee SY (2015a) Description of the new phototrophic dinoflagellate Alexandrium pohangense sp. nov. from Korean coastal waters. Harmful Algae 46:49–61

    CAS  Google Scholar 

  • Lim AS, Jeong HJ, Kim JH, Jang SH, Lee MJ, Lee K (2015b) 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

    Google Scholar 

  • Lim AS, Jeong HJ, Ok JH, Kim SJ (2018) Feeding by the harmful phototrophic dinoflagellate Takayama tasmanica (Family Kareniaceae). Harmful Algae 74:19–29

    PubMed  Google Scholar 

  • Lim AS, Jeong HJ, Ok JH (2019a) Five Alexandrium species lacking mixotrophic ability. Algae 34:289–301

    Google Scholar 

  • Lim AS, Jeong HJ, Ok JH, You JH, Kang HC, Kim SJ (2019b) Effects of light intensity and temperature on growth and ingestion rates of the mixotrophic dinoflagellate Alexandrium pohangense. Mar Biol 166:98

    Google Scholar 

  • López-Rosales L, Gallardo-Rodríguez J, Sánchez-Mirón A, Cerón-García M, Belarbi E, García-Camacho F, Molina-Grima E (2014) Simultaneous effect of temperature and irradiance on growth and okadaic acid production from the marine dinoflagellate Prorocentrum belizeanum. Toxins 6:229–253

    PubMed  PubMed Central  Google Scholar 

  • Magaña HA, Villareal TA (2006) The effect of environmental factors on the growth rate of Karenia brevis (Davis) G. Hansen and Moestrup. Harmful Algae 5:192–198

    Google Scholar 

  • Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 5:60

    Google Scholar 

  • Marine Environment Information System (MEIS). https://www.meis.go.kr. Accessed 05 Mar 2020

  • 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

    Google Scholar 

  • Matsuoka K, Iizuka S, Takayama H, Honjyo T, Fukuyo Y, Ishimaru T (1989) Geographic distribution of Gymnodinium nagasakiense Takayama et Adachi around west Japan. In: Okaichi T, Anderson DM, Nemoto T (eds) Red Tides: biology environmental science and toxicology. Elsevier, New York, pp 101–104

    Google Scholar 

  • Menden-Deuer S, Lessard EJ, Satterberg J, Grünbaum D (2005) Growth rates and starvation survival of three species of the pallium-feeding, thecate dinoflagellate genus Protoperidinium. Aquat Microb Ecol 41:145–152

    Google Scholar 

  • Morton SL, Norris DR, Bomber JW (1992) Effect of temperature, salinity and light intensity on the growth and seasonality of toxic dinoflagellates associated with ciguatera. J Exp Mar Biol Ecol 157:79–90

    Google Scholar 

  • Nagasoe S, Kim DI, Shimasaki Y, Oshima Y, Yamaguchi M, Honjo T (2006) Effects of temperature, salinity and irradiance on the growth of the red-tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee. Harmful Algae 5:20–25

    Google Scholar 

  • Nielsen MV (1996) Growth and chemical composition of the toxic dinoflagellate Gymnodinium galatheanum in relation to irradiance, temperature and salinity. Mar Ecol Prog Ser 136:205–211

    CAS  Google Scholar 

  • Ogata T, Ishimaru T, Kodama M (1987) Effect of water temperature and light intensity on growth rate and toxicity change in Protogonyaulax tamarensis. Mar Biol 95:217–220

    CAS  Google Scholar 

  • Ok JH, Jeong HJ, Lim AS, You JH, Kang HC, Kim SJ, Lee SY (2019) Effects of light and temperature on the growth of Takayama helix (Dinophyceae): mixotrophy as a survival strategy against photoinhibition. J Phycol 55:1181–1195

    CAS  PubMed  Google Scholar 

  • Ono K, Khan S, Onoue Y (2000) Effects of temperature and light intensity on the growth and toxicity of Heterosigma akashiwo (Raphidophyceae). Aquac Res 31:427–433

    Google Scholar 

  • Pillai KCS (1955) Some new test criteria in multivariate analysis. Ann Math Stat 26:117–121

    Google Scholar 

  • Poole HH, Atkins WRG (1929) Photo-electric measurements of submarine illumination throughout the year. J Mat Biol Assoc UK 16:297–324

    Google Scholar 

  • Richardson K, Beardall J, Raven JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191

    Google Scholar 

  • Seip KL, Reynolds CS (1995) Phytoplankton functional attributes along trophic gradient and season. Limnol Oceanogr 40:589–597

    Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Google Scholar 

  • Shumway SE, Burkholder JM, Springer J (2006) Effects of the estuarine dinoflagellate Pfiesteria shumwayae (Dinophyceae) on survival and grazing activity of several shellfish species. Harmful Algae 5:442–458

    Google Scholar 

  • Skovgaard A (1996) Mixotrophy in Fragilidium subglobosum (Dinophyceae): growth and grazing responses as functions of light intensity. Mar Ecol Prog Ser 143:247–253

    Google Scholar 

  • Skovgaard A (2000) A phagotrophically derivable growth factor in the plastidic dinoflagellate Gyrodinium resplendens (Dinophyceae). J Phycol 36:1069–1078

    Google Scholar 

  • Skovgaard A, Karpov SA, Guillou L (2012) The parasitic dinoflagellates Blastodinium spp. inhabiting the gut of marine, planktonic copepods: morphology, ecology, and unrecognized species diversity. Front Microbiol 3:305

    PubMed  PubMed Central  Google Scholar 

  • Staehr PA, Sand-Jensen KAJ (2006) Seasonal changes in temperature and nutrient control of photosynthesis, respiration and growth of natural phytoplankton communities. Freshw Biol 51:249–262

    CAS  Google Scholar 

  • Stoecker DK (1999) Mixotrophy among dinoflagellates. J Eukaryot Microbiol 46:397–401

    Google Scholar 

  • Stoecker DK, Li A, Coats DW, Gustafson DE, Nannen MK (1997) Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar Ecol Prog Ser 152:1–12

    Google Scholar 

  • Tukey JW (1953) The problem of multiple comparisons. In: Braun HI (ed) The collected works of John W. Tukey, volume VIII, multiple comparisons: 1948–1983. Chapman and Hall, London, pp 1–300

    Google Scholar 

  • Turner JT, Roncalli V, Ciminiello P, Dell’Aversano C, Fattorusso E, Tartaglione L, Carotenuto Y, Romano G, Esposito F, Miralto A, Ianora A (2012) Biogeographic effects of the Gulf of Mexico red-tide dinoflagellate Karenia brevis on Mediterranean copepods. Harmful Algae 16:63–73

    Google Scholar 

  • Welch BL (1947) The generalization of ‘student’s’ problem when several different population variances are involved. Biometrika 34:28–35

    CAS  PubMed  Google Scholar 

  • Whittington J, Sherman B, Green D, Oliver RL (2000) Growth of Ceratium hirundinella in a subtropical Australian reservoir: the role of vertical migration. J Plankton Res 22:1025–1045

    Google Scholar 

  • Xu N, Duan S, Li A, Zhang C, Cai Z, Hu Z (2010) Effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful Algae 9:13–17

    Google Scholar 

  • Yokouchi K, Onuma R, Horiguchi T (2018) Ultrastructure and phylogeny of a new species of mixotrophic dinoflagellate, Paragymnodinium stigmaticum sp. nov. (Gymnodiniales, Dinophyceae). Phycologia 57:539–554

    CAS  Google Scholar 

  • Yoo YD, Jeong HJ, Kim MS, Kang NS, Song JY, Shin WG, Kim KY, Lee KT (2009) Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J Eukaryot Microbiol 56:413–420

    PubMed  Google Scholar 

  • Yoo YD, Jeong HJ, Kang NS, Song JY, Kim KY, Lee KT, Kim JH (2010) Feeding by the newly described mixotrophic dinoflagellate Paragymnodinium shiwhaense: feeding mechanism, prey species, and effect of prey concentration. J Eukaryot Microbiol 57:145–158

    PubMed  Google Scholar 

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Acknowledgements

This research was supported by the useful dinoflagellate program of Korea Institute of Marine Science and Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (MOF) and the National Research Foundation (NRF) funded by the Ministry of Science and ICT (NRF-2015M1A5A1041806; NRF-2017R1E1A1A01074419) award to HJJ.

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You, J.H., Jeong, H.J., Lim, A.S. et al. Effects of irradiance and temperature on the growth and feeding of the obligate mixotrophic dinoflagellate Gymnodinium smaydae. Mar Biol 167, 64 (2020). https://doi.org/10.1007/s00227-020-3678-y

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