Aquatic Sciences

, 80:2 | Cite as

Effects of small-scale turbulence on growth and grazing of marine microzooplankton

  • Rodrigo A. Martínez
  • Albert Calbet
  • Enric Saiz
Research Article


We report the effects of small-scale turbulence at realistic intensity (ε = 1.1 × 10−2 cm2 s−3) on the growth and grazing rates of three marine heterotrophic dinoflagellates (Peridiniella danica, Gyrodinium dominans and Oxyrrhis marina) and one ciliate (Mesodinium pulex). All the dinoflagellates showed a reduction of volume-based growth rates, whereas M. pulex did not. P. danica was the most affected by small-scale turbulence, followed by G. dominans, and O. marina. Turbulence slightly increased O. marina ingestion rates, but this increase was not statistically significant. G. dominans and M. pulex ingestion rates were modestly lower under turbulence, and P. danica completely ceased feeding in turbulent treatments. Gross growth efficiencies of G. dominans and O. marina were negatively affected by turbulence, whereas they remained unaltered for M. pulex. P. danica feeding and growth rates in the presence of turbulence were close to zero. Overall, there was a negative relationship between the effects of turbulence on ingestion rates and the time needed to process a prey item. Neglecting the effects of turbulence in microzooplankton grazing estimates in the field could produce biased approximations of their impacts on primary producers.


Protozoan Microzooplankton Small-scale turbulence Dinoflagellate Ciliate Grazing Growth 



We thank K. Griffell for her technical assistance and Dr. F. Peters for his help in the use of the turbulence generator set-up. P. danica and M. pulex cultures were kindly provided by H.H. Jakobsen. Projects PROTOS (CTM2009-08783) and FERMI (CGL2014-59227-R) from the Spanish Ministry of Economy, Industry and Competitiveness (co-financed with FEDER funds from the EU). R.A.M. was funded by a PhD fellowship from the National Commission of Science (CONICYT), Ministry of Education, Chile. This study is a contribution of the Marine Zooplankton Ecology Group (2014SGR-498) at the Institut de Ciències del Mar-CSIC.


  1. Alcaraz M, Saiz E, Calbet A (1994) Small-scale turbulence and zooplankton metabolism: Effects of turbulence on heartbeat rates of planktonic crustaceans. Limnol Oceanogr 39:1465–1470CrossRefGoogle Scholar
  2. Almeda R, Augustin CB, Alcaraz M, Calbet A, Saiz E (2010) Feeding rates and gross growth efficiencies of larval developmental stages of Oithona davisae (Copepoda, Cyclopoida). J Exp Mar Biol Ecol 387:24–35CrossRefGoogle Scholar
  3. Arin L, Marrasé C, Maar M, Peters F, Sala MM, Alcaraz M (2002) Combined effects of nutrients and small-scale turbulence in a microcosm experiment. I. dynamics and size distribution of osmotrophic plankton. Aquat Microb Ecol 29:51–61CrossRefGoogle Scholar
  4. Berdalet E (1992) Effects of turbulence on the marine dinoflagellate Gymnodinium nelsonii. J Phycol 28:267–272CrossRefGoogle Scholar
  5. Berdalet E, Estrada M (1993) Effects of turbulence on several dinoflagellate species. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, New York, pp 737–740Google Scholar
  6. Berdalet E, Estrada M (2005) Effects of small-scale turbulence on the physiological functioning of marine algae. In: Subba Rao DV (ed) Algal cultures, analogues and applications. Science Publishers, Inc., Enfield, pp 459–500Google Scholar
  7. Berdalet E, Peters F, Koumandou VL, Roldán C, Guadayol Ò, Estrada M (2007) Species-specific physiological response of dinoflagellates to quantified small-scale turbulence. J Phycol 43:965–977CrossRefGoogle Scholar
  8. Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49:51–57CrossRefGoogle Scholar
  9. Calbet A, Saiz E (2005) The ciliate-copepod link in marine ecosystems. Aquat Microb Ecol 38:157–167CrossRefGoogle Scholar
  10. 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
  11. Caparroy P, Perez MT, Carlotti F (1998) Feeding behaviour of Centropages typicus in calm and turbulent conditions. Mar Ecol Prog Ser 168:109–118CrossRefGoogle Scholar
  12. Cosson J, Cachon M, Cachon J, Cosson MP (1988) Swimming behaviour of the unicellular biflagellate Oxyrrhis marina: in vivo and in vitro movement of the two flagella. Biol Cell 63:117–126CrossRefPubMedGoogle Scholar
  13. Cózar A, Echevarría F (2005) Size structure of the planktonic community in microcosms with different levels of turbulence. Sci Mar 69:187–197CrossRefGoogle Scholar
  14. Delaney MP (2003) Effes of temperature and turbulence on the predator–prey interactions between a heterotrophic flagellate and a marine bacterium. Microb Ecol 45:218–225CrossRefPubMedGoogle Scholar
  15. Dickey TD (1990) Physical-optical-biological scales relevant to recruitment in large marine ecosystems. In: Sherman K, Alexander LM, Gold BD (eds) Large marine ecosystems: Patterns, processes, and yields. American Association for Advancement in Science, pp 82–98Google Scholar
  16. Dolan JR, Sall N, Metcalfe A, Gasser B (2003) Effects of turbulence on the feeding and growth of a marine oligotrich ciliate. Aquat Microb Ecol 31:183–192CrossRefGoogle Scholar
  17. Frost BW (1972) Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17:805–815CrossRefGoogle Scholar
  18. Gifford DJ (1991) The protozoan-metazoan trophic link in pelagic ecosystems. J Protozool 38:81–86CrossRefGoogle Scholar
  19. Guadayol O, Peters F, Stiansen JE, Marrasé C, Lohrmann A (2009) Evaluation of oscillating grids and orbital shakers as means to generate isotropic and homogeneous small-scale turbulence in laboratory enclosures commonly used in plankton studies. Limnol Oceanogr Methods 7:287–303CrossRefGoogle Scholar
  20. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29–60CrossRefGoogle Scholar
  21. Guo Z, Zhang H, Liu S, Lin S (2013) Biology of the marine heterotrophic dinoflagellate Oxyrrhis marina: current status and future directions. Microorganisms 1:33–57CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hansen PJ, Calado AJ (1999) Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J Eukaryot Microbiol 46:382–389CrossRefGoogle Scholar
  23. Havskum H (2003) Effects of small-scale turbulence on interactions between the heterotrophic dinoflagellate Oxyrrhis marina and its prey, Isochrysis sp. Ophelia 57:125–135CrossRefGoogle Scholar
  24. 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 47:177–189CrossRefGoogle Scholar
  25. Hill PS, Nowell ARM, Jumars PA (1992) Encounter rate by turbulent shear of particles similar in diameter to the Kolmogorov scale. J Mar Res 50:643–668CrossRefGoogle Scholar
  26. Incze LS, Hebert D, Wolff N, Oakey N, Dye D (2001) Changes in copepod distributions associated with increased turbulence from wind stress. Mar Ecol Prog Ser 213:229–240CrossRefGoogle Scholar
  27. Jakobsen HH, Everett LM, Strom SL (2006) Hydromechanical signaling between the ciliate Mesodinium pulex and motile protist prey. Aquat Microb Ecol 44:197–206CrossRefGoogle Scholar
  28. Karentz D (1987) Dinoflagellate cell cycles. In: Kumar DH (ed) Phycotalk. Print House, India, pp 377–397Google Scholar
  29. Kiørboe T (1997) Small-scale turbulence, marine snow formation, and planktivorous feeding. Sci Mar 61:141–158Google Scholar
  30. Kiørboe T, MacKenzie BR (1995) Turbulence-enhanced prey encounter rates in larval fish: effects of spatial scale, larval behaviour and size. J Plank Res 17:2319–2331CrossRefGoogle Scholar
  31. Kiørboe T, Saiz E (1995) Planktivorous feeding in calm and turbulent environments, with emphasis on copepods. Mar Ecol Prog Ser 122:135–145CrossRefGoogle Scholar
  32. Landry MR, Hassett RP (1982) Estimating the grazing impact of marine micro-zooplankton. Mar Biol 67:283–288CrossRefGoogle Scholar
  33. Löder MGJ, Boersma M, Kraberg AC, Aberle N, Wiltshire KH (2014) Microbial predators promote their competitors: commensalism within an intra-guild predation system in microzooplankton. Ecosphere 5:1–23CrossRefGoogle Scholar
  34. Logan BE, Kirchman DL (1991) Uptake of dissolved organics by marine bacteria as a function of fluid motion. Mar Biol 111:175–181CrossRefGoogle Scholar
  35. MacKenzie BR, Kiørboe T (1995) Encounter rates and swimming behavior of pause-travel and cruise larval fish predators in calm and turbulent laboratory environments. Limnol Oceanogr 40:1278–1289CrossRefGoogle Scholar
  36. MacKenzie BR, Leggett WC (1991) Quantifying the contribution of small-scale turbulence to the encounter rates between larval fish and their zooplankton prey: effects of wind and tide. Mar Ecol Prog Ser 73:149–160CrossRefGoogle Scholar
  37. MacKenzie BR, Miller TJ, Cyr S, Leggett WC (1994) Evidence for a dome-shaped relationship between turbulence and larval fish ingestion rates. Limnol Oceanogr 39:1790–1799CrossRefGoogle Scholar
  38. Malits A, Peters F, Bayer-Giraldi M, Marrasé C, Zoppini A, Guadayol O, Alcaraz M (2004) Effects of small-scale turbulence on bacteria: a matter of size. Microb Ecol 48:287–299CrossRefPubMedGoogle Scholar
  39. Margalef R (1997) Turbulence and marine life. Sci Mar 61:109–123Google Scholar
  40. Menden-Deuer S, Grünbaum D (2006) Individual foraging behaviors and population distributions of a planktonic predator aggregating to phytoplankton thin layers. Limnol Oceanogr 51:109–116CrossRefGoogle Scholar
  41. Moeseneder M, Herndl G (1995) Influence of turbulence on bacterial production in the sea. Limnol Oceanogr 40:1466–1473CrossRefGoogle Scholar
  42. Neumann A (2008) Feeding mechanism of the dinoflagellate Peridiniella danica. Master Thesis, p 64Google Scholar
  43. Peters F, Marrasé C (2000) Effects of turbulence on plankton: an overview of experimental evidence and some theoretical considerations. Mar Ecol Prog Ser 205:291–306CrossRefGoogle Scholar
  44. Peters F, Redondo JM (1997) Turbulence generation and measurement: application to studies on plankton. Scien Mar 61(Supl. 1):205–228Google Scholar
  45. Peters F, Choi JW, Gross T (1996) Paraphysomonas imperforata (Protista, Chrysomonadida) under different turbulence levels: feeding, physiology and energetics. Mar Ecol Prog Ser 134:235–245CrossRefGoogle Scholar
  46. Peters F, Marrasé C, Gasol JM, Sala M, Arin L (1998) Effects of turbulence on bacterial growth mediated through food web interactions. Mar Ecol Prog Ser 172:293–303CrossRefGoogle Scholar
  47. Peters F, Marrasé C, Havskum H, Rassoulzadegan F, Dolan J, Alcaraz M, Gasol JM (2002) Turbulence and the microbial food web: effects on bacterial losses to predation and on community structure. J Plankton Res 24:321–331CrossRefGoogle Scholar
  48. Roberts EC, Wootton EC, Davidson K, Jeong HJ, Lowe CD, Montagnes DJS (2011) Feeding in the dinoflagellate Oxyrrhis marina: linking behaviour with mechanisms. J Plankton Res 33:603–614CrossRefGoogle Scholar
  49. Rothschild BJ, Osborn TR (1988) Small-scale turbulence and plankton contact rates. J Plankton Res 10:465–474CrossRefGoogle Scholar
  50. Saito H, Ota T, Suzuki K, Nishioka J, Tsuda A (2006) Role of heterotrophic dinoflagellate Gyrodinium sp. in the fate of an iron induced diatom bloom. Geophys Res Lett 33:1–4Google Scholar
  51. Saiz E, Alcaraz M (1992) Enhanced excretion rates induced by small-scale turbulence in Acartia (Copepoda: Calanoida). J Plankton Res 14:681–689CrossRefGoogle Scholar
  52. Saiz E, Kiørboe T (1995) Predatory and suspension feeding of the copepod Acartia tonsa in turbulent environments. Mar Ecol Prog Ser 122:147–158CrossRefGoogle Scholar
  53. Saiz E, Alcaraz M, Paffenhöfer G-A (1992) Effects of small-scale turbulence on feeding rate and gross-growth efficiency of three Acartia species (Copepoda: Calanoida). J Plankton Res 14:1085–1097CrossRefGoogle Scholar
  54. Saiz E, Calbet A, Broglio E (2003) Effects of small-scale turbulence on copepods: the case of Oithona davisae. Limnol Oceanogr 48:1304–1311CrossRefGoogle Scholar
  55. Samayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42:1137–1153CrossRefGoogle Scholar
  56. Schmoker C, Hernandez-Leon S, Calbet A (2013) Microzooplankton grazing in the oceans: impacts, data variability, knowledge gaps and future directions. J Plankton Res 35:691–706CrossRefGoogle Scholar
  57. Shimeta J, Jumars PA, Lessard EJ (1995) Influences of turbulence on suspension feeding by planktonic protozoa; experiments in laminar shear fields. Limnol Oceanogr 40:845–859CrossRefGoogle Scholar
  58. Sullivan JM, Swift E (2003) Effects of small-scale turbulence on net growth rate and size of ten species of marine dinofalgellates. J Phycol 39:83–94CrossRefGoogle Scholar
  59. Tamar H (1992) Four Marine Species of Mesodinium (Ciliophora: Mesodiniidae) II. Mesodinium pulex Clap. & Lachm., 1858. Archiv für Protistenkunde 141:284–303CrossRefGoogle Scholar
  60. Thomas WH, Gibson CH (1990) Effects of small-scale turbulence on microalgae. J Appl Phycol 2:71–77CrossRefGoogle Scholar
  61. Thomas WH, Tynan CT, Gibson CH (1997) Turbulence–phytoplankton interrelationships. In: Round FE, Chapman DJ (eds) Progress in phycological research. Biopress Ltd., Bristol, pp 283–324Google Scholar
  62. Visser AW, 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
  63. Waite A, Lindahl O (2006) Bloom and decline of the toxic flagellate Chattonella marina in a Swedish fjord. Mar Ecol Prog Ser 326:77–83CrossRefGoogle Scholar
  64. Watts PC, Martin LE, Kimmance SA, Montagnes DJS, Lowe CD (2011) The distribution of Oxyrrhis marina: a global disperser or poorly characterized endemic? J Plankton Res 33:579–589CrossRefGoogle Scholar
  65. Weisse T, Anderson R, Arndt H, Calbet A, Hansen PJ, Montagnes DJ (2016) Functional ecology of aquatic phagotrophic protists—concepts, limitations, and perspectives. Eur J Protistol 55:50–74CrossRefPubMedGoogle Scholar
  66. Yeung PKK, Wong JTY (2003) Inhibition of cell proliferation by mechanical agitation involves transient cell cycle arrest at G1 phase in dinoflagellates. Protoplasma 2000:173–178Google Scholar
  67. Zirbel M, Veron F, Latz M (2000) The reversible effect of flow on the morphology of Ceratocorys horrida (Peridiniales, Dinophyta). J Phycol 36:46–58CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Institut de Ciències del MarCSICBarcelonaSpain
  2. 2.Instituto de Fomento Pesquero (IFOP)Puerto MonttChile

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