References

Biogeosciences

1726-4189

Copernicus Publications

Göttingen, Germany

10.5194/bg-10-5755-2013

Enhanced rates of particulate organic matter remineralization by microzooplankton are diminished by added ballast minerals

Le Moigne

F. A. C.

¹ Gallinari

² Laurenceau

² ³ De La Rocha

C. L.

Department of Ocean Biogeochemistry and Ecosystems, National Oceanography Centre, Southampton, UK

CNRS UMR6539, IUEM, Université de Bretagne Occidentale, Brest, France

now at: CSIRO-UTAS Quantitative Marine Sciences Ph.D. Program, Institute for Marine and Antarctic Studies, Antarctic Climate and Ecosystems Cooperative Research Centre, University of Tasmania, Commonwealth Scientific and Industrial Research Organisation, Marine and Atmospheric Research, Hobart, Australia

02 09 2013

10 9 5755 5765

2013

This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/

This article is available from https://bg.copernicus.org/articles/10/5755/2013/bg-10-5755-2013.html

The full text article is available as a PDF file from https://bg.copernicus.org/articles/10/5755/2013/bg-10-5755-2013.pdf

To examine the potentially competing influences of microzooplankton and calcite mineral ballast on organic matter remineralization, we incubated diatoms in darkness in rolling tanks with and without added calcite minerals (coccoliths) and microzooplankton (rotifers). Concentrations of particulate organic matter (POM in suspension or in aggregates), of dissolved organic matter (DOM), and of dissolved inorganic nutrients were monitored over 8 days. The presence of rotifers enhanced the remineralization of ammonium and phosphate, but not dissolved silicon, from the biogenic particulate matter, up to 40% of which became incorporated into aggregates early in the experiment. Added calcite resulted in rates of excretion of ammonium and phosphate by rotifers that were depressed by 67% and 36%, respectively, demonstrating the potential for minerals to inhibit the destruction of POM by zooplankton in the water column. Lastly, the presence of the rotifers and added calcite minerals resulted in a more rapid initial rate of aggregation, although not a greater overall amount of aggregation during the experiment.

References 1

Aminot, A. and Kerouel, R.: An automated photo-oxidation method for the determination of dissolved organic phosphorus in marine and fresh water, Mar. Chem., 76, 113–126, 2001.

Aminot, A. and Kerouel, R.: Dosage automatique des nutriments dans les eaux marines, in, Editions de l'IFREMER, ISBN 978-2-7592-0023-8, 188 pp., 2007.

Armstrong, R. A., Lee, C., Hedges, J. I., Honjo, S., and Wakeham, S. G.: A new, mechanistic model for organic carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals, Deep-Sea Res. II, 49, 219–236, 2002.

Bidle, K. D. and Azam, F.: Bacterial control of silicaon regeneration from diatom dtritus: significance of bacterial ectohydrolases and species identity, Limnol. Oceanogr., 46, 1606–1623, 2001.

Broecker, W. S. and Peng, T.-H.: Tracers in the Sea, Eldigio, New York, 690 pp., 1982.

Castilho, M. S. M. and Arcifa, M. S.: Production of the rotifer Brachionus plicatilis (Ploimida: Brachionidae) in a Brazilian coastal lagoon, Rev. Biol. Trop., 48, 859–865, 2000.

De La Rocha, C. L. and Passow, U.: Factors influencing the sinking of POC and the efficiency of the biological carbon pump, Deep-Sea Res. II, 54, 639–658, 2007.

De La Rocha, C. L., Nowald, N., and Passow, U.: Interactions between diatom aggregates, minerals, particulate organic carbon, and dissolved organic matter: Further implications for the ballast hypothesis, Global Biogeochem. Cy., 22, GB4005, <a href="http://dx.doi.org/10.1029/2007GB003156">https://doi.org/10.1029/2007GB003156</a>, 2008.

Deuser, W. G., Ross, E. H., and Anderson, R. F.: Seasonality in the supply of sediment to the deep Sargasso Sea and implications for the rapid transfer of matter to the deep ocean, Deep-Sea Res., 28, 495–505, 1981.

Ejsmont-Karabin, J.: Ecological characteristics of lakes in North-eastern Poland versus their trophic gradient. VIII. Role of nutrient regeneration by planktonic rotifers and crustaceans in 42 lakes, Ekol. Pol., 31, 411–427, 1983.

Engel, A., Abramson, L., Szlosek, J., Liu, Z., Stewart, G., Hirschberg, D., and Lee, C.: Investigating the effect of ballasting by CaCO3 in Emiliania huxleyi: II. Decomposition of particulate organic matter, Deep-Sea Res. II, 56, 1408–1419, 2009a.

Engel, A., Szlosek, J., Abramson, L., Liu, Z., and Lee, C.: Investigating the effect of ballasting by CaCO3 in Emiliania huxleyi: I. Formation, settling velocities and physical properties of aggregates, Deep-Sea Res. II, 56, 1396–1407, 2009b.

Falkowski, P. G., Barber, R. T., and Smetacek, V.: Biogeochemical controls and feedbacks on ocean primary production, Science, 281, 200–206, 1998.

Fischer, G. and Karakaş, G.: Sinking rates and ballast composition of particles in the Atlantic Ocean: implications for the organic carbon fluxes to the deep ocean, Biogeosciences, 6, 85–102, <a href="http://dx.doi.org/10.5194/bg-6-85-2009">https://doi.org/10.5194/bg-6-85-2009</a>, 2009.

François, R., Honjo, S., Krishfield, R., and Manganini, S.: Factors controlling the flux of organic carbon to the bathypelagic zone of the ocean, Glob. Biogeochem. Cy., 16, 1087, <a href="http://dx.doi.org/10.1029/2001GB001722">https://doi.org/10.1029/2001GB001722</a>, 2002.

Hamm, C. E.: Interactive aggregation and sedimentation of diatoms and clay-sized 700 lithogenic material, Limnol. Oceanogr. 47, 1790–1795, 2002.

Harlay, J., Chou, L., De Bodt, C., Van Oostende, N., Piontek, J., Suykens, K., Engel, A., Sabbe, K., Groom, S., Delille, B., and Borges, A. V.: Biogeochemistry and carbon mass balance of a coccolithophore bloom in the nothern bay Bay of Biscay (June 2006), Deep-Sea Res. I, 58, 111–127, 2011.

Harris, R. P.: Zooplankton grazing on the coccolithore Emiliania huxleyi and its role in organic carbon flux, Mar. Biol., 119, 431–439, 1994.

Henson, S., Sanders, R., Madsen, E., Morris, P. J., Le Moigne, F., Quartly, G. D.: A reduced estimate of the strength of the ocean's biological carbon pump, Geophys. Res. Lett., 38, L046006, <a href="http://dx.doi.org/10.1029/2011GL046735">https://doi.org/10.1029/2011GL046735</a>, 2011.

Hirata, H. and Nagata, W. D.: Excretion rates and excreted components of the rotifer Brachionus plicatilis O.F. MÜLLER in culture, Mem. Fac. Fish. Kagoshima Univ., 31, 161–174, 1982.

Hoppe, H.-G., Kim, S. J., and Gocke, K.: Microbial decomposition in aquatic environments: Combined process of extracellular enzyme activity and substrate uptake, Appl. Environ. Microbiol., 54, 784–790, 1988.

Ignoffo, T. R., Bollens, S. M., and Bochdansky, A. B.: The effects of thin layers on the vertical distribution of the rotifer, Brachionus plicatilis, J. Exp. Mar. Biol. Ecol., 316, 167–181, 2005.

Ingalls, A. E., Liu, Z., and Lee, C.: Seasonal trends in the pigment and amino acid compositions of sinking particles in biogenic CaCO3 and SiO2 dominated regions of the Pacific sector of the Southern Ocean along 170° W, Deep-Sea Res. I, 53, 836–859, 2006.

Iversen, M. H. and Ploug, H.: Ballast minerals and the sinking carbon flux in the ocean: carbon-specific respiration rates and sinking velocity of marine snow aggregates, Biogeosciences, 7, 2613–2624, <a href="http://dx.doi.org/10.5194/bg-7-2613-2010">https://doi.org/10.5194/bg-7-2613-2010</a>, 2010.

Iversen, M. H., Nowald, N., Ploug, H., Jackson, G. A., and Fischer, G.: High resolution profiles of vertical particulate matter export off Cape Blanc, Mauritania: Degradation processes and ballasting effects, Deep-Sea Res. I, 57, 711–784, 2010.

Kirk, K. L.: Suspended clay reduces Daphnia feeding rate. Freshwater Biol. 25, 357–365, 1991.

Klaas, C. and Archer, D. E.: Association of sinking organic matter with various types of mineral ballast in the deep sea: Implications for the rain ratio, Glob. Biogeochem. Cy., 16, 1116, <a href="http://dx.doi.org/10.1029/2001GB001765">https://doi.org/10.1029/2001GB001765</a>, 2002.

Koroleff, F.: Direct determination of ammonia in natural water as indophenol blue, in: Information on Techniques and Methods for Seawater Analysis, Int. Con. Explor. Sea, Interlab Report Number 3, 19–22, 1969.

Le Quéré, C., Takahashi, T.,. Buitenhuis, E. T., Rödenbeck, C., and Sutherland, S. C.: Impact of climate change and variability on the global ocean sink of CO2, Glob. Biogeochem. Cy., 24, GB4007, <a href="http://dx.doi.org/10.1029/2009GB003599">https://doi.org/10.1029/2009GB003599</a>, 2010.

Lee, C., Peterson, M. L. Wakeham, S. G., Armstrong, R. A., Cochran, J. K., Miquel, J. C., Fowler, S. W., Hirschberg, D., Beck, A., and Xue, J.: Particulate organic matter and ballast fluxes measured using time-series and settling velocity sediment traps in the northwestern Mediterranean Sea, Deep-Sea Res. II, 56 1420–1436, 2009.

Lorrain, A., Savoye, N., Chauvaud, L., Paulet, Y.-M., and Naulet, N.: Decarbonation and preservation method for the analysis of organic C and N contents and stable isotope ratios of low-carbonated suspended particulate material, Anal. Chim. Acta, 491, 125–133, 2003.

Pan, X., Sanders, R., Tappin, A. D., Worsfold, P. J., Achterberg, E. P.: Simultaneous determination of dissolved organic carbon and total dissolved nitrogen on a coupled high-temperature combustion total organic carbon-nitrogen chemiluminescence detection (HTC TOC-NCD) system, J. Autom. Methods Manag. Chem., 2005, 240–246, 2005.

Parekh, P., Dutkiewicz, S., Follows, M. J., and Ito, T.: Atmospheric carbon dioxide in a less dusty world, Geophys. Res. Lett., 33, L03610, <a href="http://dx.doi.org/10.1029/2005GL025098">https://doi.org/10.1029/2005GL025098</a>, 2006.

Parkhill, J. P., Maillet, G., Cullen, J. J.: Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress, J. Phycol., 37, 517–529, 2001.

Passow, U. and De La Rocha C. L.: Accumulation of mineral ballast on organic aggregates, Glob. Biogeochem. Cy., 20, GB1013, <a href="http://dx.doi.org/10.1029/2005GB002579">https://doi.org/10.1029/2005GB002579</a>, 2006.

Passow, U., Engel, A., and Ploug, H.: The role of aggregation for the dissolution of diatom frustules, FEMS Microbiol. Ecol., 46, 247–255, 2003.

Pinto-Coehlo, R. M., Texeira de Moura, R., and Moreira, A.: Zooplankton and bacteria contribution to phosphorus and nitrogen internal cycling in a tropical and eutrophic reservoir: Pamulha Lake, Brazil, Int. Revue Ges. Hydrobiol., 82, 185–200, 1997.

Prieto, L., Sommer, F., Stibor, H., and Koeve, W.: Effects of planktonic copepods on transparent exopolymeric particles (TEP) abundance and size spectra, J. Plankton Res., 23, 515–525, 2001.

Ploug, H., Iversen, M. H., Fischer, G.: Ballast, sinking velocity, and apparent diffusivity within marine snow and zooplankton fecal pellets: Implications for substrate turnover by attached bacteria, Limnol. Oceanogr., 53, 1878–1886, 2008.

Poulton, A. J., Sanders, R., Holligan, P. M., Stinchcombe, M. C., Adey, T. R., Brown, L., and Chamberlain, K.: Phytoplankton mineralization in the tropical and subtropical Atlantic Ocean, Glob. Biogeochem. Cy., 20, GB4002, <a href="http://dx.doi.org/10.1029/2006gb002712">https://doi.org/10.1029/2006gb002712</a>, 2006.

Ragueneau, O., Savoye, N., Del Amo, Y., Cotten, J., Tardiveau, B., and Leynaert, A.: A new method for the measurement of biogenic silica in suspended matter of coastal waters: using Si:Al ratios to correct for the mineral interference, Cont. Shelf Res., 25, 697–710, 2005.

Riley, J., Sanders, R., Marsay, C., Le Moigne, F. A. C., Achterberg, E. P., and Poulton, A. J.: The relative contribution of fast and slow sinking particles to ocean carbon export, Glob. Biogeochem. Cy., 26, GB1026, <a href="http://dx.doi.org/10.1029/2011GB004085">https://doi.org/10.1029/2011GB004085</a>, 2012.

Rothhaupt, K. O.: Differences in particle-size dependent feeding efficiencies of closely related rotifer species, Limnol. Oceanogr., 35, 16–23, 1990.

Sanders, R., Morris, P. J., Poulton, A. J., Stinchcombe, M. C., Charalampopoulou, A., Lucas, M. I., and Thomalla S. J.: Does a ballast effect occur in the surface ocean?, Geophys. Res. Lett., 37, L08602, <a href="http://dx.doi.org/10.1029/2010GL042574">https://doi.org/10.1029/2010GL042574</a>, 2010.

Shanks, A. L. and Trent, J. D.: Marine snow – Sinking rates and potential role in vertical flux, Deep-Sea Res., 27, 137–143, 1980.

Theilacker, G. H. and McMaster, M. F.: Mass culture of the rotifer Brachionus plicatilis and it sevaluation as a food larval anchovies, Mar. Biol., 10, 183–188, 1971.

Thomalla, S. J., Poulton, A. J., Sanders, R., Turnewitsch, R., Holligan, P. M., and Lucas, M. I.: Variable export fluxes and efficiencies for calcite, opal, and organic carbon in the Atlantic Ocean: A ballast effect in action?, Glob. Biogeochem. Cy., 22, GB1010, <a href="http://dx.doi.org/10.1029/2007GB002982">https://doi.org/10.1029/2007GB002982</a>, 2008.

Vanderploeg, H. A., Eadie, B. J., Liebig, J. R., Tarapchak, S. J., and Glover, R. M.: Contribution of calcite to the particle-size spectrum of Lake Michigan seston and its interactions with the plankton, Can. J. Fish. Aquat. Sci., 44, 1898–1914, 1987.

Von Brand, T., Rakestraw, N. W., and Renn, C. E.: Decomposition and regeneration of nitrogenous organic matter in sea water, Biol. Bull., 273–282, 1942.

Yoon, W. B. and Rosson, R. A.: Improved method of enumeration of attached bacteria for study of fluctuation in the abundance of attached and free-living bacteria in response to diel variation in seawater turbidity, Appl. Environ. Microbiol., 56, 595–600, 1990.

Zimmermann-Timm, H., Holst, H., and Müller, S.: Seasonal dynamics of aggregates and their typical biocoenosis in the Elbe Estuary, Estuaries, 21, 613–621, 1998.