Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Relative importance of physical and biological factors regulating tintinnid populations: a field study with frequent samplings in Sendai Bay, Japan

Takehiro Kazama A C and Jotaro Urabe A B
+ Author Affiliations
- Author Affiliations

A Graduate School of Life Sciences, Tohoku University, Aoba 6-3, Aramaki, Aoba-ku, Sendai 980-8578, Japan.

B Research Center for Marine Biology, Tohoku University, Asamushi, Aomori 039-3501, Japan.

C Corresponding author. Email: kazama303@gmail.com

Marine and Freshwater Research 67(4) 492-504 https://doi.org/10.1071/MF14256
Submitted: 27 August 2014  Accepted: 19 February 2015   Published: 13 July 2015

Abstract

To examine factors regulating the summer population dynamics of tintinnid species, temporally high-frequency observations of tintinnid ciliates were performed in Hiroura Estuary in Sendai Bay. Sampling was conducted on alternate days from 5 July to 2 August, 2010 at three estuary sites to examine which environmental (water temperature, salinity and tidal level change) and biological (abundances of Chl-a, bacteria, protozoans and zooplankton) factors are important for determining temporal changes in abundance and apparent population change rates for tintinnid species. During the study period, 20 tintinnid species were found and showed drastic population changes within a few days, resulting in different tintinnid assemblages from the first to the second half of the study period. Multivariate analysis and generalised linear mixed models showed that several environmental and biological factors were related significantly with the abundance and apparent population change rate of each tintinnid species, but no effect of potential predators such as copepods was found for the abundance and change rate. These results suggest that physicochemical and food conditions play more important roles than predation pressure in short-term temporal changes of tintinnid populations during summer in estuary environments.

Additional keywords: estuaries, microbial food web, micro-zooplankton, population dynamics, selective feeding, species composition.


References

Admiraal, W., and Venekamp, L. H. (1986). Significance of tintinnid grazing during bloom of Phaeocystis–Pouchetii (Haptophyceae) in Dutch coastal waters. Netherlands Journal of Sea Research 20, 61–66.
Significance of tintinnid grazing during bloom of Phaeocystis–Pouchetii (Haptophyceae) in Dutch coastal waters.Crossref | GoogleScholarGoogle Scholar |

Bakker, C., and Phaff, W. J. (1976). Tintinnida from coastal waters of the S.W.–Netherlands I. The genus Tintinnopsis Stein. Hydrobiologia 50, 101–111.
Tintinnida from coastal waters of the S.W.–Netherlands I. The genus Tintinnopsis Stein.Crossref | GoogleScholarGoogle Scholar |

Balkis, N. (2004). Tintinnids (Protozoa: Ciliophora) of the Büyükçekmece Bay in the Sea of Marmara. Scientia Marina 68, 33–44.

Barría de Cao, M. S., Beigy, D., and Piccolo, C. (2005). Temporal variability of diversity and biomass of tintinnids (Ciliophora) in a southwestern Atlantic temperate estuary. Journal of Plankton Research 27, 1103–1111.

Barton, K. (2009). MuMIn: multi–model inference (R package version 0.12. 2). Available at http://cran.r-project.org/web/packages/MuMIn/index.html [Verified 1 May 2012].

Bates, D., and Maechler, M. (2009). Lme4: Linear mixed-effects models using sfour classes (R package version 0.999375–31). Available at http://CRAN.R-project.org/package=lme4 [Verified 1 May 2012].

Børsheim, K. Y., and Bratbak, G. (1987). Cell volume to carbon conversion factors for a bacterivorous Monas sp. enriched from seawater. Marine Ecology Progress Series 36, 171–175.
Cell volume to carbon conversion factors for a bacterivorous Monas sp. enriched from seawater.Crossref | GoogleScholarGoogle Scholar |

Burnham, K. P., and Anderson, D. R. (1998). ‘Model selection and inference: a practical information-theoretic approach.’ (Springer–Verlag: New York.)

Calbet, A., and Saiz, E. (2005). The ciliate–copepod link in marine ecosystems. Aquatic Microbial Ecology 38, 157–167.
The ciliate–copepod link in marine ecosystems.Crossref | GoogleScholarGoogle Scholar |

Cordeiro, T. A., and Sassi, R. (1997). Tintinnina (Ciliophora, Protista) of the North Sea during the spring of 1986. Helgolaender Meeresuntersuchungen 51, 155–172.
Tintinnina (Ciliophora, Protista) of the North Sea during the spring of 1986.Crossref | GoogleScholarGoogle Scholar |

Dolan, J. R. (1991). Microphagous ciliates in mesohaline Chesapeake Bay waters: estimates of growth rates and consumption by copepods. Marine Biology 111, 303–309.
Microphagous ciliates in mesohaline Chesapeake Bay waters: estimates of growth rates and consumption by copepods.Crossref | GoogleScholarGoogle Scholar |

Dolan, J. R., and Gallegos, C. L. (2001). Estuarine diversity of Tintinnids (Planktonic ciliates). Journal of Plankton Research 23, 1009–1027.
Estuarine diversity of Tintinnids (Planktonic ciliates).Crossref | GoogleScholarGoogle Scholar |

Dolan, J. R., Montagnes, D. J., Agatha, S., Coats, D. W., and Stoecker, D. K. (2012). ‘The Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton.’ (Wiley : Chichester, UK.)

Engström-Öst,, J.,, Viitasalo, M.,, Jónasdóttir, S.,, Repka, S., Sivonen, K., Köski, M., and Schmidt, K. (2002). Calanoid copepods feed and produce eggs in the presence of toxic cyanobacteria Nodularia spumigena. Limnology and Oceanography 47, 878–885.
Calanoid copepods feed and produce eggs in the presence of toxic cyanobacteria Nodularia spumigena.Crossref | GoogleScholarGoogle Scholar |

Fessenden, L., and Cowles, T. J. (1994). Copepod predation on phagotrophic ciliates in Oregon coastal waters. Marine Ecology Progress Series 107, 103–111.
Copepod predation on phagotrophic ciliates in Oregon coastal waters.Crossref | GoogleScholarGoogle Scholar |

Gifford, D. J., and Dagg, M. J. (1991). The microzooplankton–mesozooplankton link: consumption of planktonic protozoa by the calanoid copepods Acartia tonsa Dana and Neocalanus plumchrus Murukawa. Marine Microbial Food Webs 5, 161–177.

Gismervik, I., and Andersen, T. (1997). Prey switching by Acartia clausi: experimental evidence and implications of intraguild predation assessed using a model. Marine Ecology Progress Series 157, 247–259.
Prey switching by Acartia clausi: experimental evidence and implications of intraguild predation assessed using a model.Crossref | GoogleScholarGoogle Scholar |

Godhantaraman, N., and Uye, S. (2003). Geographical and seasonal variations in taxonomic composition, abundance and biomass of microzooplankton across a brackish-water lagoonal system of Japan. Journal of Plankton Research 25, 465–482.
Geographical and seasonal variations in taxonomic composition, abundance and biomass of microzooplankton across a brackish-water lagoonal system of Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktVCgur8%3D&md5=3632041a5a943f9cfb7e2335a1d03669CAS |

Gómez, F. (2007). Trends on the distribution of ciliates in the open Pacific Ocean. Acta Protozoologica 32, 188–202.

Hada, Y. (1937). The fauna of Akkeshi Bay: IV. Pelagic ciliata with 56 text figures. Journal of the Faculty of Science of Hokkaido Imperial University Series IV Zoology 5, 143–216.

Hada, Y. (1938). Studies of the Tintinnoinea front the western tropical Pacific with 3 tables and 100 text figures. Journal of the Faculty of Science of Hokkaido Imperial University Series IV Zoology 6, 87–190.

Hobbie, J. E., Daley, R. D., and Jasper, S. (1977). Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology 33, 1225–1228.
| 1:STN:280:DyaE2s3itVertw%3D%3D&md5=8bbe35d7969284f8c02ffe99041f84b0CAS | 327932PubMed |

Houser, D. S., and Allen, D. M. (1996). Zooplankton dynamics in an intertidal salt-marsh basin. Estuaries 19, 659–673.
Zooplankton dynamics in an intertidal salt-marsh basin.Crossref | GoogleScholarGoogle Scholar |

Irigoien, X., Head, R. N., Harris, R. P., Cummings, D., Harbour, D., and Meyer-Harms, B. (2000). Feeding selectivity and egg production of Calanus helgolandicus in the English Channel. Limnology and Oceanography 45, 44–54.
Feeding selectivity and egg production of Calanus helgolandicus in the English Channel.Crossref | GoogleScholarGoogle Scholar |

Iwasaki, N. (1997). Order Harpacticoida. In ‘An Illustrated Guide to Marine Plankton in Japan’. (Eds M. Chihara and M. Murano.) pp. 954–960. (Tokai University Press: Tokyo.)

Jang, M. S., Shin, K., Lee, T., and Noh, I. (2010). Feeding selectivity of calanoid copepods on phytoplankton in Jangmok Bay, south coast of Korea. Ocean Science Journal 45, 101–111.
Feeding selectivity of calanoid copepods on phytoplankton in Jangmok Bay, south coast of Korea.Crossref | GoogleScholarGoogle Scholar |

Kamiyama, T. (1997). Growth and grazing responses of tintinnid ciliates feeding on the toxic dinoflagellate Heterocapsa circularisquama. Marine Biology 128, 509–515.
Growth and grazing responses of tintinnid ciliates feeding on the toxic dinoflagellate Heterocapsa circularisquama.Crossref | GoogleScholarGoogle Scholar |

Kamiyama, T., and Tsujino, M. (1996). Seasonal variation in the species composition of tintinnid ciliates in Hiroshima Bay, the Seto Inland Sea of Japan. Journal of Plankton Research 18, 2313–2327.
Seasonal variation in the species composition of tintinnid ciliates in Hiroshima Bay, the Seto Inland Sea of Japan.Crossref | GoogleScholarGoogle Scholar |

Katayama, S., Tamaki, M., and Okata, A. (2011). Diel changes in vertical distributions of two mysid species, Neomysis, in estuarine brackish water. Bulletin of the Japanese Society of Fisheries Oceanography 75, 19–28.

Kazama, T., Ishida, S., Shimano, S., and Urabe, J. (2012). Discrepancy between conventional morphological systematics and nuclear phylogeny of tintinnids (Ciliophora: Choreotrichia). Plankton and Benthos Research 7, 111–125.
Discrepancy between conventional morphological systematics and nuclear phylogeny of tintinnids (Ciliophora: Choreotrichia).Crossref | GoogleScholarGoogle Scholar |

Kemp, W. M., and Boynton, W. R. (1984). Spatial and temporal coupling of nutrient inputs to estuarine primary production: the role of particulate transport and decomposition. Bulletin of Marine Science 35, 522–535.

Kleppel, G. S., Frazel, D., Pieper, R. E., and Holliday, D. V. (1988). Natural diets of zooplankton off southern California. Marine Ecology Progress Series 49, 231–241.
Natural diets of zooplankton off southern California.Crossref | GoogleScholarGoogle Scholar |

Landry, M. R. (1981). Switching between herbivory and carnivory by the planktonic marine copepod Calanus pacificus. Marine Biology 65, 77–82.
Switching between herbivory and carnivory by the planktonic marine copepod Calanus pacificus.Crossref | GoogleScholarGoogle Scholar |

Lonsdale, D. J., Caron, D. A., Dennett, M. R., and Schaffner, R. (2000). Predation by Oithona spp. on protozooplankton in the Ross Sea, Antarctica. Deep-sea Research. Part II, Topical Studies in Oceanography 47, 3273–3283.
Predation by Oithona spp. on protozooplankton in the Ross Sea, Antarctica.Crossref | GoogleScholarGoogle Scholar |

Nakamura, Y., and Turner, J. T. (1997). Predation and respiration by the small cyclopoid Oithona similis: how important is feeding on ciliates and heterotrophic flagellates? Journal of Plankton Research 19, 1275–1288.
Predation and respiration by the small cyclopoid Oithona similis: how important is feeding on ciliates and heterotrophic flagellates?Crossref | GoogleScholarGoogle Scholar |

Nielsen, T. G., and Kiørboe, T. (1994). Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 2. Ciliates. Limnology and Oceanography 39, 508–519.
Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 2. Ciliates.Crossref | GoogleScholarGoogle Scholar |

Nishida, S. (1997). Order Cyclopoida. In ‘An Illustrated Guide to Marine Plankton in Japan’. (Eds M. Chihara and M. Murano.) pp. 935–951. (Tokai University Press: Tokyo.)

Ohtsuka, S., and Ueda, H. (1997). Order Caranoida. In ‘An Illustrated Guide to Marine Plankton in Japan’. (Eds M. Chihara and M. Murano.) pp. 660–931. (Tokai University Press: Tokyo.)

Oksanen, J., Guillaume Blanchet, F., Kindt, R., Legendre, P., O’Hara, B., Simpson, G. L., Solymos, P., Stevens, M. H. H., and Wagner, H. (2010). Vegan: Community Ecology Package. Available at http://vegan.r-forge.r-project.org/ [Verified 1 May 2012].

Olenina, I., Hajdu, S., Edler, L., Andersson, A., Wasmund, N., Busch, S., Göbel, J., Gromisz, S., Huseby, S., Huttunen, M., Jaanus, A., Kokkonen, P., Ledaine, I., and Niemkiewicz, E. (2006). Biovolumes and size classes of phytoplankton in the Baltic Sea. In ‘HELCOM Baltic Sea Environment Proceedings No. 106’. 144 pp. (Baltic Marine Environment Protection Commission – Helsinki Commission: Helsinki.)

Pierce, R. W., and Turner, J. T. (1992). Ecology of planktonic ciliates in marine food webs. Reviews in Aquatic Sciences 6, 139–181.

Quinlan, E. L., Jett, C. H., and Phlips, E. J. (2009). Microzooplankton grazing and the control of phytoplankton biomass in the Suwannee River estuary, USA. Hydrobiologia 632, 127–137.
Microzooplankton grazing and the control of phytoplankton biomass in the Suwannee River estuary, USA.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2010). R: A Language and Environment for Statistical Computing. Available at http://www.R-project.org/ [Verified 1 May 2012].

Sakaguchi, Y., Takahashi, Y., and Omori, H. (1986). ‘Rivers in Japan.’ pp. 219–230. (Iwanami Shoten: Tokyo.) [In Japanese].

Shaheen, P. A., Manderson, J. P., and Fahay, M. P. (2004). Stage-specific spatial and temporal variability in the diets of larval winter flounder (Pseudopleuronectes americanus) in a northeastern US estuarine nursery. Estuaries 27, 958–965.
Stage-specific spatial and temporal variability in the diets of larval winter flounder (Pseudopleuronectes americanus) in a northeastern US estuarine nursery.Crossref | GoogleScholarGoogle Scholar |

Sherr, E. B., Caron, D. A., and Sherr, B. F. (1993). Staining of heterotrophic protists for visualization via epifluorescence microscopy. In ‘Handbook of Methods in Aquatic Microbial Ecology’. (Eds P. F. Kemp, B. F. Sherr, E. B. Sherr, and J. S. Cole.) pp. 213–227. (Lewis Publishers: Boca Raton, FL, USA.)

Stoecker, D. K., and Capuzzo, J. M. (1990). Predation on protozoa: its importance to zooplankton. Journal of Plankton Research 12, 891–908.
Predation on protozoa: its importance to zooplankton.Crossref | GoogleScholarGoogle Scholar |

Stoecker, D. K., and Evans, G. T. (1985). Effects of protozoan herbivory and carnivory in a microplankton food web. Marine Ecology Progress Series 25, 159–167.
Effects of protozoan herbivory and carnivory in a microplankton food web.Crossref | GoogleScholarGoogle Scholar |

Stoecker, D. K., and Sanders, N. K. (1985). Differential grazing by Acartia tonsa on a dinoflagellate and a tintinnid. Journal of Plankton Research 7, 85–100.
Differential grazing by Acartia tonsa on a dinoflagellate and a tintinnid.Crossref | GoogleScholarGoogle Scholar |

Stoecker, D. K., Guillard, R. R. L., and Kavee, R. M. (1981). Selective predation by Favella ehrenbergii (Tintinnia) on and among dinoflagellates. The Biological Bulletin 160, 136–145.
Selective predation by Favella ehrenbergii (Tintinnia) on and among dinoflagellates.Crossref | GoogleScholarGoogle Scholar |

Stoecker, D. K., Davis, L. H., and Provan, A. (1983). Growth of Favella sp. (Ciliata: Tintinnina) and other microzooplankton in cages incubated in situ and comparison to growth in vitro. Marine Biology 75, 293–302.
Growth of Favella sp. (Ciliata: Tintinnina) and other microzooplankton in cages incubated in situ and comparison to growth in vitro.Crossref | GoogleScholarGoogle Scholar |

Strickland, J. D., and Parsons, T. R. (1972). ‘A Practical Handbook of Seawater Analysis’, 2nd edn. (Fisheries Research Board of Canada Bulletin: Ottawa, ON, Canada.)

Tanaka, T., and Taniguchi, A. (1999). Predator–prey eddy in heterotrophic nanoflagellate–bacteria relationships in a bay on the northeastern Pacific coast of Japan. Marine Ecology Progress Series 179, 123–134.
Predator–prey eddy in heterotrophic nanoflagellate–bacteria relationships in a bay on the northeastern Pacific coast of Japan.Crossref | GoogleScholarGoogle Scholar |

Taniguchi, A. (1997). Suborder Tintinnina. In ‘An Illustrated Guide to Marine Plankton in Japan’. (Eds M. Chihara and M. Murano.) pp. 421–483. (Tokai University Press: Tokyo.)

Ter Braak, C. F. (1988). ‘CANOCO: a FORTRAN program for canonical community ordination by [partial][detrended][canonical] correspondence analysis, principal components analysis and redundancy analysis (version 2.1).’ (Agricultural Mathematics: Wageningen.)

Ter Braak, C. F. (1994). Canonical community ordination. Part I: Basic theory and linear methods. Ecoscience 1, 127–140.

Thompson, G. A. (2004). Tintinnid diversity trends in the southern Atlantic Ocean (29 to 60 degrees S). Aquatic Microbial Ecology 35, 93–103.
Tintinnid diversity trends in the southern Atlantic Ocean (29 to 60 degrees S).Crossref | GoogleScholarGoogle Scholar |

Tiselius, P. (1989). Contribution of aloricate ciliates to the diet of Acartia clausi and Centropages hamatus in coastal waters. Marine Ecology Progress Series 56, 49–56.
Contribution of aloricate ciliates to the diet of Acartia clausi and Centropages hamatus in coastal waters.Crossref | GoogleScholarGoogle Scholar |

Turner, J. T., and Anderson, D. M. (1983). Zooplankton grazing during dinoflagellate blooms in Cape Cod Embayment, with observations of predation upon tintinnids by copepods. P.S.Z.N.I. Marine Ecology (Berlin) 4, 359–374.
Zooplankton grazing during dinoflagellate blooms in Cape Cod Embayment, with observations of predation upon tintinnids by copepods. P.S.Z.N.I.Crossref | GoogleScholarGoogle Scholar |

Uchima, M., and Hirano, R. (1986). Food of Oithona davisae (Copepoda: Cyclopoida) and the effect of food concentration at first feeding on larval growth. Bulletin of the Plankton Society of Japan 33, 21–28.

Ueda, H. (1997). Family Acartidae. In ‘An Illustrated Guide to Marine Plankton in Japan’. (Eds M. Chihara and M. Murano.) pp. 669–680. (Tokai University Press: Tokyo.)

Underwood, G. J. C., and Kromkamp, J. (1999). Primary production by phytoplankton and microphytobenthos in estuaries. Advances in Ecological Research 29, 93–153.
Primary production by phytoplankton and microphytobenthos in estuaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltl2lug%3D%3D&md5=33cd45409082ff3ddfbf0c369448c29aCAS |

Uye, S., Aoto, I., and Onbé, T. (2002). Seasonal population dynamics and production of Microsetella norvegica, a widely distributed but little-studied marine planktonic harpacticoid copepod. Journal of Plankton Research 24, 143–153.
Seasonal population dynamics and production of Microsetella norvegica, a widely distributed but little-studied marine planktonic harpacticoid copepod.Crossref | GoogleScholarGoogle Scholar |

Verity, P. G., and Langdon, C. (1984). Relationships between lorica volume, carbon, nitrogen, and ATP content of tintinnids in Narragansett Bay. Journal of Plankton Research 6, 859–868.
Relationships between lorica volume, carbon, nitrogen, and ATP content of tintinnids in Narragansett Bay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmtVOhur0%3D&md5=ffe6d04839704a63bcc887818f0ba4a1CAS |

Watras, C. J., Garcon, V. C., Olson, R. J., Chisholm, S. W., and Anderson, E. M. (1985). The effect of zooplankton grazing on estuarine blooms of the toxic dinoflagellate Gonyaulax tamarensis. Journal of Plankton Research 7, 891–908.
The effect of zooplankton grazing on estuarine blooms of the toxic dinoflagellate Gonyaulax tamarensis.Crossref | GoogleScholarGoogle Scholar |

Wetsteyn, L. J., and Kromkamp, J. C. (1994). Turbidity, nutrients and phytoplankton primary production in the Oosterschelde (the Netherlands) before, during and after a large-scale coastal engineering project (1980–1990). Hydrobiologia 282–283, 61–78.
Turbidity, nutrients and phytoplankton primary production in the Oosterschelde (the Netherlands) before, during and after a large-scale coastal engineering project (1980–1990).Crossref | GoogleScholarGoogle Scholar |

Yang, E. J., Ju, S., and Choi, J. (2010). Feeding activity of the copepod Acartia hongi on phytoplankton and micro-zooplankton in Gyeonggi Bay, Yellow Sea. Estuarine, Coastal and Shelf Science 88, 292–301.
Feeding activity of the copepod Acartia hongi on phytoplankton and micro-zooplankton in Gyeonggi Bay, Yellow Sea.Crossref | GoogleScholarGoogle Scholar |

Zervoudaki, S., Christou, E. D., and Nielsen, T. (2007). The importance of small copepods in a frontal area of the Aegean Sea. Journal of Plankton Research 29, 317–338.
The importance of small copepods in a frontal area of the Aegean Sea.Crossref | GoogleScholarGoogle Scholar |