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

The contribution of heterotrophic nanoflagellate grazing towards bacterial mortality in tropical waters: comparing estuaries and coastal ecosystems

Chui Wei Bong A and Choon Weng Lee A B
+ Author Affiliations
- Author Affiliations

A Laboratory of Microbial Ecology, Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia.

B Corresponding author. Email: lee@um.edu.my

Marine and Freshwater Research 62(4) 414-420 https://doi.org/10.1071/MF10213
Submitted: 9 August 2010  Accepted: 25 February 2011   Published: 28 April 2011

Abstract

Heterotrophic nanoflagellate (HNF) grazing depends on both temperature and trophic status of an ecosystem. As most microbes already function at their temperature optimum in tropical waters, we hypothesised that HNF grazing rates would be higher in more productive sites such as estuaries than in less productive areas such as coastal waters. We sampled two estuaries and three coastal sites along the Straits of Malacca and the South China Sea near the Malaysia Peninsula. Bacterial abundance ranged 0.9–6.3 × 106 cells mL–1, whereas HNF abundance ranged 1.8–10.1 ×103 cells mL–1. Bacterial production ranged 1.1–12.7 × 105 cells mL–1 h–1, whereas HNF grazing rates were an order of magnitude lower at 1.0–78.5 × 104 cells mL–1 h–1. Bacterial abundance, net bacterial production and HNF grazing rates were higher in estuaries than coastal waters but HNF abundance did not differ between the two areas. Across all stations, HNF grazing rates increased with bacterial production, and accounted for ~33% of bacterial production. Our results suggest that in the tropical waters studied, there was a bacterial production–grazing imbalance. Other loss factors such as viral lysis, sedimentation or the presence of benthic filter feeders could account for this imbalance.

Additional keywords: bacterial mortality, top-down control.


References

Adamczewski, T., Chrost, R. J., Kalinowska, K., and Skowronska, A. (2010). Relationship between bacteria and heterotrophic nanoflagellates in lake water examined by different techniques controlling grazing pressure. Aquatic Microbial Ecology 60, 203–213.
Relationship between bacteria and heterotrophic nanoflagellates in lake water examined by different techniques controlling grazing pressure.Crossref | GoogleScholarGoogle Scholar |

Agis, M., Granda, A., and Dolan, J. R. (2007). A cautionary note: examples of possible microbial community dynamics in dilution grazing experiments. Journal of Experimental Marine Biology and Ecology 341, 176–183.
A cautionary note: examples of possible microbial community dynamics in dilution grazing experiments.Crossref | GoogleScholarGoogle Scholar |

Alongi, D. M., Chong, V. C., Dixon, P., Sasekumar, A., and Tirendi, F. (2003). The influence of fish cage aquaculture on pelagic carbon flow and water chemistry in tidally dominated mangrove estuaries of Peninsular Malaysia. Marine Environmental Research 55, 313–333.
The influence of fish cage aquaculture on pelagic carbon flow and water chemistry in tidally dominated mangrove estuaries of Peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvFCh&md5=73dbefeff861662b2bad50ede38c8ddaCAS | 12517423PubMed |

Becquevort, S. (1997). Nanoprotozooplankton in the Atlantic sector of the Southern Ocean during early spring: biomass and feeding activities. Deep-Sea Research Part II: Topical Studies in Oceanography 44, 355–373.
Nanoprotozooplankton in the Atlantic sector of the Southern Ocean during early spring: biomass and feeding activities.Crossref | GoogleScholarGoogle Scholar |

Bloem, J., Bär-Gilissen, M. J. B., and Cappenberg, T. E. (1986). Fixation, counting, and manipulation of heterotrophic nanoflagellates. Applied and Environmental Microbiology 52, 1266–1272.
| 1:STN:280:DC%2BC3crotVOmsA%3D%3D&md5=e36e6664a2630e9fde281a33cc304debCAS | 16347232PubMed |

Bouvy, M., Pagano, M., M’Boup, M., Got, P., and Troussellier, M. (2006). Functional structure of microbial food web in the Senegal River Estuary (West Africa): impact of metazooplankton. Journal of Plankton Research 28, 195–207.
Functional structure of microbial food web in the Senegal River Estuary (West Africa): impact of metazooplankton.Crossref | GoogleScholarGoogle Scholar |

Ferrier-Pagès, C., and Gattuso, J. P. (1998). Biomass, production and grazing rates of pico- and nanoplankton in coral reef waters (Miyako Island, Japan). Microbial Ecology 35, 46–57.
Biomass, production and grazing rates of pico- and nanoplankton in coral reef waters (Miyako Island, Japan).Crossref | GoogleScholarGoogle Scholar | 9459658PubMed |

Fukami, K., Murata, N., Morio, Y., and Nishijima, T. (1996). Distribution of heterotrophic nanoflagellates and their importance as the bacterial consumer in a eutrophic coastal seawater. Journal of Oceanography 52, 399–407.
Distribution of heterotrophic nanoflagellates and their importance as the bacterial consumer in a eutrophic coastal seawater.Crossref | GoogleScholarGoogle Scholar |

González, J. M., Torréton, J. P., Dufour, P., and Charpy, L. (1998). Temporal and spatial dynamics of the pelagic microbial food web in an atoll lagoon. Aquatic Microbial Ecology 16, 53–64.
Temporal and spatial dynamics of the pelagic microbial food web in an atoll lagoon.Crossref | GoogleScholarGoogle Scholar |

Hammer, Ø., Harper, D. A. T., and Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4, 1–9.

Havens, K. E. (1993). An experimental analysis of macrozooplankton, microzooplankton and phytoplankton in a temperate eutrophic lake. Archiv fuer Hydrobiologie 127, 9–20.

Heinänen, A. P. (1991). Bacterial numbers, biomass and productivity in the Baltic Sea: a cruise study. Marine Ecology Progress Series 70, 283–290.
Bacterial numbers, biomass and productivity in the Baltic Sea: a cruise study.Crossref | GoogleScholarGoogle Scholar |

Iriarte, A., Sarobe, A., and Orive, E. (2008). Seasonal variability in bacterial abundance, production and protistan bacterivory in the lower Urdaibai estuary, Bay of Biscay. Aquatic Microbial Ecology 52, 273–282.
Seasonal variability in bacterial abundance, production and protistan bacterivory in the lower Urdaibai estuary, Bay of Biscay.Crossref | GoogleScholarGoogle Scholar |

Jürgens, K., and Matz, C. (2002). Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie van Leeuwenhoek 81, 413–434.
Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria.Crossref | GoogleScholarGoogle Scholar | 12448740PubMed |

Karl, D. M. (2007). Microbial oceanography: paradigms, processes and promise. Nature Reviews Microbiology 5, 759–769.
Microbial oceanography: paradigms, processes and promise.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeis7bO&md5=94d4b280570923740e836b7f8190af21CAS | 17853905PubMed |

Kennish, M. J. (1990). ‘Ecology of Estuaries. Volume II: Biological Aspects.’ (CRC Press: Boca Raton.)

Kepner, R. L., and Pratt, J. R. (1994). Use of fluorochromes for direct enumeration of total bacteria in environmental samples: past and present. Microbiological Reviews 58, 603–615.
| 1:CAS:528:DyaK2MXivFahtLo%3D&md5=f46fe0783dc42b1df363119c046b1671CAS | 7854248PubMed |

Krstulović, N., Šolić, M., and Marasovic, I. (1997). Relationship between bacteria, phytoplankton and heterotrophic nanoflagellates along the trophic gradient. Helgolaender Meeresuntersuchungen 51, 433–443.
Relationship between bacteria, phytoplankton and heterotrophic nanoflagellates along the trophic gradient.Crossref | GoogleScholarGoogle Scholar |

Lee, C. W., and Bong, C. W. (2007). Bacterial respiration, growth efficiency and protist grazing rates in mangrove waters in Cape Rachado, Malaysia. Asian Journal of Water, Environment and Pollution 4, 11–16.
| 1:CAS:528:DC%2BD2sXltFWmurs%3D&md5=320ceed5d8945b825e0f2471e7d005c0CAS |

Lee, C. W., and Bong, C. W. (2008). Bacterial abundance and production, and their relation to primary production in tropical coastal waters of Peninsular Malaysia. Marine and Freshwater Research 59, 10–21.
Bacterial abundance and production, and their relation to primary production in tropical coastal waters of Peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKnt7g%3D&md5=a4768dc68a5d4e37cbeb38f9eab377a7CAS |

Lee, C. W., Kudo, I., Yanada, M., and Maita, Y. (2001). Bacterial abundance and production and heterotrophic nanoflagellate abundance in subarctic coastal waters (Western North Pacific Ocean). Aquatic Microbial Ecology 23, 263–271.
Bacterial abundance and production and heterotrophic nanoflagellate abundance in subarctic coastal waters (Western North Pacific Ocean).Crossref | GoogleScholarGoogle Scholar |

Lee, C. W., Kudo, I., Yokokawa, T., Yanada, M., and Maita, Y. (2002). Dynamics of bacterial respiration and related growth efficiency, dissolved nutrients and dissolved oxygen concentration in a subarctic coastal embayment. Marine and Freshwater Research 53, 1–7.
Dynamics of bacterial respiration and related growth efficiency, dissolved nutrients and dissolved oxygen concentration in a subarctic coastal embayment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVSnsrc%3D&md5=28f873b1543a8ec2802ebfe23473cdfbCAS |

Lee, C. W., Bong, C. W., and Hii, Y. S. (2009). Temporal variation of bacterial respiration and growth efficiency in tropical coastal waters. Applied and Environmental Microbiology 75, 7594–7601.
Temporal variation of bacterial respiration and growth efficiency in tropical coastal waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Whu7fP&md5=51fa121e1782e2594ec631bedc0b3cd0CAS | 19820145PubMed |

Lugomela, C., Wallberg, P., and Nielsen, T. G. (2001). Plankton composition and cycling of carbon during the rainy season in a tropical coastal ecosystem, Zanzibar, Tanzania. Journal of Plankton Research 23, 1121–1136.
Plankton composition and cycling of carbon during the rainy season in a tropical coastal ecosystem, Zanzibar, Tanzania.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFGgt7s%3D&md5=baa304740a40d5550bd4350b53e34147CAS |

McManus, G. B. (1993). Growth rates of natural populations of heterotrophic nanoplankton. In ‘Handbook of Methods in Aquatic Microbial Ecology’. (Eds P. F. Kemp, B. F. Sherr, E. B. Sherr and J. J. Cole.) pp. 557–562. (Lewis Publishers: Boca Raton.)

Murrel, M. C., and Lores, E. M. (2004). Phytoplankton and zooplankton seasonal dynamics in a subtropical estuary: importance of cyanobacteria. Journal of Plankton Research 26, 371–382.
Phytoplankton and zooplankton seasonal dynamics in a subtropical estuary: importance of cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitV2kur0%3D&md5=41e6d64f892a481413f2821024a9eb95CAS |

Pagano, M., Champalbert, G., Aka, M., Kouassi, E., Arfi, R., et al. (2006). Herbivorous and microbial grazing pathways of metazooplankton in the Senegal River Estuary (West Africa). Estuarine, Coastal and Shelf Science 67, 369–381.
Herbivorous and microbial grazing pathways of metazooplankton in the Senegal River Estuary (West Africa).Crossref | GoogleScholarGoogle Scholar |

Parsons, T. R., Maita, Y., and Lalli, C. M. (1984). ‘A Manual of Chemical and Biological Methods for Seawater Analysis.’ (Pergamon Press: Oxford.)

Pedrós-Alió, C., and Mas, J. (1993). Bacterial sinking losses. In ‘Handbook of Methods in Aquatic Microbial Ecology’. (Eds P. F. Kemp, B. F. Sherr, E. B. Sherr and J. J. Cole.) pp. 677–684. (Lewis Publishers: Boca Raton.)

Peduzzi, P., and Herndl, G. J. (1992). Zooplankton activity fueling the microbial loop: differential growth response of bacteria from oligotrophic and eutrophic waters. Limnology and Oceanography 37, 1087–1092.
Zooplankton activity fueling the microbial loop: differential growth response of bacteria from oligotrophic and eutrophic waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhtlWnt74%3D&md5=4fceca69f055659f35a1d0289d353022CAS |

Pomeroy, L. R. (1974). The ocean’s food web, a changing paradigm. BioScience 24, 499–504.
The ocean’s food web, a changing paradigm.Crossref | GoogleScholarGoogle Scholar |

Pomeroy, L. R., and Wiebe, W. J. (2001). Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquatic Microbial Ecology 23, 187–204.
Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2010). ‘R: A Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna.)

Rejas, D., Muylaert, K., and De Meester, L. (2005). Trophic interactions within the microbial food web in a tropical floodplain lake (Laguna Bufeos, Bolivia). Revista de Biologia Tropical 53, 85–96.
| 17354422PubMed |

Riegman, R., Kuipers, B. R., Noordeloos, A. A. M., and Witte, H. J. (1993). Size-differential control of phytoplankton and the structure of plankton communities. Netherlands Journal of Sea Research 31, 255–265.
Size-differential control of phytoplankton and the structure of plankton communities.Crossref | GoogleScholarGoogle Scholar |

Safi, K. A., and Hall, J. A. (1999). Mixotrophic and heterotrophic nanoflagellate grazing in the convergence zone east of New Zealand. Aquatic Microbial Ecology 20, 83–93.
Mixotrophic and heterotrophic nanoflagellate grazing in the convergence zone east of New Zealand.Crossref | GoogleScholarGoogle Scholar |

Safi, K. A., Vant, W. N., and Hall, J. A. (2002). Growth and grazing within the microbial food web of a large coastal embayment. Aquatic Microbial Ecology 29, 39–50.
Growth and grazing within the microbial food web of a large coastal embayment.Crossref | GoogleScholarGoogle Scholar |

Sanders, R. W., Caron, D. A., and Berninger, U. G. (1992). Relationships between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Marine Ecology Progress Series 86, 1–14.
Relationships between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison.Crossref | GoogleScholarGoogle Scholar |

Sherr, E. B., and Sherr, B. F. (2002). Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81, 293–308.
Significance of predation by protists in aquatic microbial food webs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1Sgt7Y%3D&md5=91d9365c7dea58abe1b2945e0dc70887CAS | 12448728PubMed |

Sherr, E. B., Sherr, B. F., and Fessenden, L. (1997). Heterotrophic protists in the central Arctic Ocean. Deep-Sea Research, Part II: Topical Studies in Oceanography 44, 1665–1682.
Heterotrophic protists in the central Arctic Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisVWjurw%3D&md5=882b303d184526594030865be44667d8CAS |

Sherr, B. F., Sherr, E. B., Caron, D. A., Vaulot, D., and Worden, A. Z. (2007). Oceanic protists. Oceanography 20, 130–134.

Šolić, M., and Krstulović, N. (1994). Role of predation in controlling bacterial and heterotrophic nanoflagellate standing stocks in the coastal Adriatic Sea: seasonal patterns. Marine Ecology Progress Series 114, 219–235.
Role of predation in controlling bacterial and heterotrophic nanoflagellate standing stocks in the coastal Adriatic Sea: seasonal patterns.Crossref | GoogleScholarGoogle Scholar |

Strom, S. L. (2000). Bacterivory: Interactions between bacteria and their grazers. In ‘Microbial Ecology of the Oceans’. (Ed. D. L. Kirchman.) pp. 351–386. (Wiley-Liss: New York.)

Suttle, C. A. (2007). Marine viruses – major players in the global ecosystem. Nature Reviews Microbiology 5, 801–812.
Marine viruses – major players in the global ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeis7nK&md5=b2590969827b364a04d7e7b1cde2b846CAS | 17853907PubMed |

Troussellier, M., Got, P., Mboup, M., Corbin, D., Giuliano, L., et al. (2005). Daily bacterioplankton dynamics in a sub-Saharan estuary (Senegal River, West Africa): a mesocosm study. Aquatic Microbial Ecology 40, 13–24.
Daily bacterioplankton dynamics in a sub-Saharan estuary (Senegal River, West Africa): a mesocosm study.Crossref | GoogleScholarGoogle Scholar |

Wikner, J., Rassoulzadegan, F., and Hagström, Å. (1990). Periodic bacterivore activity balances bacterial growth in the marine environment. Limnology and Oceanography 35, 313–324.
Periodic bacterivore activity balances bacterial growth in the marine environment.Crossref | GoogleScholarGoogle Scholar |