Microbial Ecology

, Volume 79, Issue 1, pp 64–72 | Cite as

Towards an Understanding of Diel Feeding Rhythms in Marine Protists: Consequences of Light Manipulation

  • Anna AriasEmail author
  • Enric Saiz
  • Albert Calbet
Environmental Microbiology


Temporal programs synchronised with the daily cycle are of adaptive importance for organisms exposed to periodic fluctuations. This study deepens into several aspects of the exogenous and endogenous nature of microbial grazers. We investigated the diel rhythms of cell division and feeding activity of four marine protists under different light regimes. In particular, we tested if the feeding cycle of protistan grazers could be mediated by a light-aided enhancement of prey digestion, and also explored the consequences of cell division on diel feeding rhythms. Cell division occurred at night for the heterotrophic dinoflagellates Gyrodinium dominans and Oxyrrhis marina. In contrast, the mixotrophic dinoflagellate Karlodinium armiger and the ciliate Strombidium sp. mostly divided during the day. Additionally, a significant diurnal feeding rhythm was observed in all species. When exposed to continuous darkness, nearly all species maintained the cell division rhythm, but lost the feeding cycle within several hours/days (with the exception of O. marina that kept the rhythm for 9.5 days). Additional feeding experiments under continuous light also showed the same pattern. We conclude that the feeding rhythms of protistan grazers are generally regulated not by cell division nor by the enhancement of digestion by light. Our study, moreover, indicates that the cell division cycle is under endogenous control, whereas an external trigger is required to maintain the feeding rhythm, at least for most of the species studied here.


Cell division Continuous darkness Diel rhythms Feeding rhythms Grazing Microzooplankton Marine protists 



The authors would like to thank Kaiene Griffell for technical support.

Funding Information

This work is supported by the FERMI project (CGL2014-59227-R; MINECO/AEI/FEDER, UE) and is a contribution of the Marine Zooplankton Ecology Group (2017 SGR 87). AA was funded with a FPI fellowship (BES-2015-074092) from the MINECO of Spain.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with animals performed by any of the authors.


  1. 1.
    Mittag M (2001) Circadian rhythms in microalgae. In International review of cytology 206:213-247 Academic Press.Google Scholar
  2. 2.
    Suzuki L, Johnson CH (2001) Algae know the time of day: circadian and photoperiodic programs. J Phycol 37:933–942CrossRefGoogle Scholar
  3. 3.
    Duval WS, Geen GH (1976) Diel feeding and respiration rhythms in zooplankton. Limnol Oceanogr 21:823–829CrossRefGoogle Scholar
  4. 4.
    Dagg MJ, Frost BW, Walser WE (1989) Copepod diel migration, feeding, and the vertical flux of pheopigments. Limnol Oceanogr 34:1062–1071CrossRefGoogle Scholar
  5. 5.
    Huntley M, Brooks ER (1982) Effects of age and food availability on diel vertical migration of Calanus pacificus. Mar Biol 71:23–31CrossRefGoogle Scholar
  6. 6.
    Visser A, Saito H, Saiz E, Kiørboe T (2001) Observations of copepod feeding and vertical distribution under natural turbulent conditions in the North Sea. Mar Biol 138:1011–1019CrossRefGoogle Scholar
  7. 7.
    Arias A, Saiz E, Calbet A (2017) Diel feeding rhythms in marine microzooplankton: effects of prey concentration, prey condition, and grazer nutritional history. Mar Biol 164:205CrossRefGoogle Scholar
  8. 8.
    Jakobsen HH, Strom SL (2004) Circadian cycles in growth and feeding rates of heterotrophic protist plankton. Limnol Oceanogr 49:1915–1922CrossRefGoogle Scholar
  9. 9.
    Strom SL (2001) Light-aided digestion, grazing and growth in herbivorous protists. Aquat Microb Ecol 23:253–261CrossRefGoogle Scholar
  10. 10.
    Tarangkoon W, Hansen PJ (2011) Prey selection, ingestion and growth responses of the common marine ciliate Mesodinium pulex in the light and in the dark. Aquat Microb Ecol 62:25–38. CrossRefGoogle Scholar
  11. 11.
    Berk SG, Parks LH, Ting RS (1991) Photoadaptation alters the ingestion rate of Paramecium bursaria, a mixotrophic ciliate. Appl Environ Microbiol 57:2312–2316CrossRefGoogle Scholar
  12. 12.
    Chen KM, Chang J (1999) Influence of light intensity on the ingestion rate of a marine ciliate, Lohmanniella sp. J Plankton Res 21:1791–1798CrossRefGoogle Scholar
  13. 13.
    Porter KG (1988) Phagotrophic phytoflagellates in microbial food webs. Hydrobiologia 159:89–97. CrossRefGoogle Scholar
  14. 14.
    Ng WHA, Liu H (2015) Diel variation of the cellular carbon to nitrogen ratio of Chlorella autotrophica (Chlorophyta) growing in phosphorus- and nitrogen-limited continuous cultures. J Phycol 51:82–92. CrossRefPubMedGoogle Scholar
  15. 15.
    Ng WHA, Liu H, Zhang S (2017) Diel variation of grazing of the dinoflagellate Lepidodinium sp. and ciliate Euplotes sp. on algal prey: the effect of prey cell properties. J Plankton Res 39:450–462CrossRefGoogle Scholar
  16. 16.
    Garcés E, Delgado M, Masó M, Camp J (1999) In situ growth rate and distribution of the ichthyotoxic dinoflagellate Gyrodinium corsicum Paulmier in an estuarine embayment (Alfacs Bay, NW Mediterranean Sea). J Plankton Res 21:1977–1991CrossRefGoogle Scholar
  17. 17.
    Homma K, Hastings JW (1989) The S phase is discrete and is controlled by the circadian clock in the marine dinoflagellate Gonyaulax polyedra. Exp Cell Res 182:635–644CrossRefGoogle Scholar
  18. 18.
    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 Benthos Res 6:92–100CrossRefGoogle Scholar
  19. 19.
    Sweeney BM, Hastings JW (1958) Rhythmic cell division in populations of Gonyaulax polyedra. J Protozool 5:217–224CrossRefGoogle Scholar
  20. 20.
    van Dolah FM, Leighfield TA, Sandel HD, Hsu CK (1995) Cell division in the dinoflagellate Gambierdiscus toxicus is phased to the diurnal cycle and accompanied by activation of the cell cycle regulatory protein, CDC2 kinase. J Phycol 31:395–400. CrossRefGoogle Scholar
  21. 21.
    Yamaguchi M (1992) DNA synthesis and the cell cycle in the noxious red-tide dinoflagellate Gymnodinium nagasakiense. Mar Biol 112:191–198. CrossRefGoogle Scholar
  22. 22.
    Kohata K, Watanabe M (1986) Synchronous division and the pattern of diel vertical migration of Heterosigma akashiwo (Hada) Hada (Raphidophyceae) in a laboratory culture tank. J Exp Mar Biol Ecol 100:209–224CrossRefGoogle Scholar
  23. 23.
    Baek SH, Shimode S, Shin K, Han M-S, Kikuchi T (2009) Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of vertical migration and cell division. Harmful Algae 8:843–856CrossRefGoogle Scholar
  24. 24.
    Guillard RR (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds.). Culture of marine invertebrate animals. Springer, pp. 29–60Google Scholar
  25. 25.
    Calbet A, Isari S, Martínez RA, Saiz E, Garrido S, Peters J, Borrat RM, 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 483:67–84CrossRefGoogle Scholar
  26. 26.
    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. CrossRefGoogle Scholar
  27. 27.
    Li AS, Stoecker DK, Adolf JE (1999) Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat Microb Ecol 19:163–176. CrossRefGoogle Scholar
  28. 28.
    Sunju Kim YGK, Kim HS, Yih W, Wayne Coats D, Park MG (2008) Growth and grazing responses of the mixotrophic dinoflagellate Dinophysis acuminata as functions of light intensity and prey concentration. Aquat Microb Ecol 51:301–310CrossRefGoogle Scholar
  29. 29.
    Terje Berge PJH (2016) Role of the chloroplasts in the predatory dinoflagellate Karlodinium armiger. Mar Ecol Prog Ser 549:41–54CrossRefGoogle Scholar
  30. 30.
    Montagnes DJS, Lowe CD, Roberts EC, Breckels MN, Boakes DE, Davidson K, Keeling PJ, Slamovits CH, Steinke M, Yang Z, Watts PC (2011) An introduction to the special issue: Oxyrrhis marina, a model organism? J Plankton Res 33:549–554. CrossRefGoogle Scholar
  31. 31.
    Begun AA, Orlova TY, Selina MS (2004) A “bloom” in the water of Amursky Bay (Sea of Japan) caused by the dinoflagellate Oxyrrhis marina Dujardin, 1841. Russ J Mar Biol 30:51–55. CrossRefGoogle Scholar
  32. 32.
    Droop M (1953) Phagotrophy in Oxyrrhis marina Dujardin. Nature 172:250–251CrossRefGoogle Scholar
  33. 33.
    Johnson M (2000) Physical control of plankton population abundance and dynamics in intertidal rock pools. Hydrobiologia 440:145–152CrossRefGoogle Scholar
  34. 34.
    Jonsson PR (1994) Tidal rhythm of cyst formation in the rock pool ciliate Strombidium oculatum Gruber (Ciliophora, Oligotrichida): a description of the functional biology and an analysis of the tidal synchronization of encystment. J Exp Mar Biol Ecol 175:77–103CrossRefGoogle Scholar
  35. 35.
    Slaveykova V, Sonntag B, Gutiérrez JC (2016) Stress and protists: no life without stress. Eur J Protistol 55:39–49CrossRefGoogle Scholar
  36. 36.
    Agusti S, González-Gordillo JI, Vaqué D, Estrada M, Cerezo MI, Salazar G, Gasol JM, Duarte CM (2015) Ubiquitous healthy diatoms in the deep sea confirm deep carbon injection by the biological pump. Nat Commun 6:7608CrossRefGoogle Scholar
  37. 37.
    Bhaud Y, Guillebault D, Lennon J, Defacque H, Soyer-Gobillard MO, Moreau H (2000) Morphology and behaviour of dinoflagellate chromosomes during the cell cycle and mitosis. J Cell Sci 113:1231–1239PubMedGoogle Scholar
  38. 38.
    Cross FR, Umen JG (2015) The Chlamydomonas cell cycle. Plant J 82:370–392CrossRefGoogle Scholar
  39. 39.
    Jong LW, Fujiwara T, Nozaki H, Miyagishima SY (2017) Cell size for commitment to cell division and number of successive cell divisions in multicellular volvocine green algae Tetrabaena socialis and Gonium pectorale. Proc Jpn Acad Ser B Phys Biol Sci 93:832–840. CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Prison A, Lorenzen H (1966) Synchronized dividing algae. Annu Rev Plant Physiol 17:439–458CrossRefGoogle Scholar
  41. 41.
    Heller M (1977) The phased division of the freshwater dinoflagellate Ceratium hirundinella and its use as a method of assessing growth in natural populations. Freshw Biol 7:527–533CrossRefGoogle Scholar
  42. 42.
    Weiler CS. 1978. Phased cell division in the dinoflagellate genus Ceratium: temporal pattern, use in determining growth rates, and ecological implications. 126 pp. PhD. Diss., Univ. of Calif., San DiegoGoogle Scholar
  43. 43.
    Eppley RW, Coatsworth JL (1966) Culture of the marine phytoplankter, Dunaliella tertiolecta, with light-dark cycles. Arch Mikrobiol 55:66–80. CrossRefGoogle Scholar
  44. 44.
    Leighfield TA, Van Dolah FM (2001) Cell cycle regulation in a dinoflagellate, Amphidinium operculatum: identification of the diel entraining cue and a possible role for cyclic AMP. J Exp Mar Biol Ecol 262:177–197CrossRefGoogle Scholar
  45. 45.
    Van Dolah FM, Lidie KB, Morey JS, Brunelle SA, Ryan JC, Monroe EA, Haynes BL (2007) Microarray analysis of diurnal- and circadian-regulated genes in the Florida red-tide dinoflagellate Karenia brevis (Dinophyceae). J Phycol 43:741–752. CrossRefGoogle Scholar
  46. 46.
    Chisholm SW, Azam F, Eppley RW (1978) Silicic acid incorporation in marine diatoms on light:dark cycles: use as an assay for phased cell division. Limnol Oceanogr 23:518–529. CrossRefGoogle Scholar
  47. 47.
    Eppley RW, Holmes RW, Paasche E (1967) Periodicity in cell division and physiological behavior of Ditylum brightwellii, a marine planktonic diatom, during growth in light-dark cycles. Arch Mikrobiol 56:305–323. CrossRefGoogle Scholar
  48. 48.
    Paasche E (1968) Marine plankton algae grown with light-dark cycles. II. Ditylum brightwellii and Nitzschia turgidula. Physiol Plant 21:66–77. CrossRefGoogle Scholar
  49. 49.
    Richman S, Rogers JN (1969) The feeding of Calanus helgolandicus on synchronously growing populations of the marine diatom Ditylum brightwellii. Limnol Oceanogr 14:701–709CrossRefGoogle Scholar
  50. 50.
    Cook JR (1966) Photosynthetic activity during the division cycle in synchronized Euglena gracilis. Plant Physiol 41:821–825. CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Cohen D, Parnas H (1976) An optimal policy for the metabolism of storage materials in unicellular algae. J Theor Biol 56:1–18CrossRefGoogle Scholar
  52. 52.
    Johnson CH (2010) Circadian clocks and cell division: what’s the pacemaker? Cell Cycle 9:3864–3873CrossRefGoogle Scholar
  53. 53.
    Johan W, Rassoulzadegan F, Hagström Å (1990) Periodic bacterivore activity balances bacterial growth in the marine environment. Limnol Oceanogr 35:313–324. CrossRefGoogle Scholar
  54. 54.
    Rychert K (2016) Growth rates of common pelagic ciliates in a highly eutrophic lake measured with a modified dilution method. Oceanol Hydrobiol Stud 45:216–229Google Scholar
  55. 55.
    Sharma VK (2003) Adaptive significance of circadian clocks. Chronobiol Int 20(6):901–919CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institut de Ciències del Mar (ICM-CSIC)BarcelonaSpain

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