Oceanography The Official Magazine of
The Oceanography Society
Volume 31 Issue 04

View Issue TOC
Volume 31, No. 4
Pages 50 - 59

Mixing Processes at the Pycnocline and Vertical Nitrate Supply: Consequences for the Microbial Food Web in San Jorge Gulf, Argentina

Maité P. Latorre Irene R. SchlossGastón O. AlmandozKarine LemarchandXimena Flores-MeloValérie Massé-BeaulneGustavo A. Ferreyra
Article Abstract

Little is known about the base of the food web that could support the high productivity and marine biodiversity found in San Jorge Gulf, Patagonia, Argentina. Here we examine the key components of the microbial food web, including the standing stock and physiological state of the phytoplankton in the context of key oceanographic variables in the gulf. Water samples were collected at 16 stations for biological and chemical analyses, together with measurements of vertical structure and currents. The dynamics of the water column and its impact on nutrient availability for primary producers was evaluated. Our results show that, in spite of the observed low surface nutrient concentrations and low biomass, phytoplankton cells were in good physiological state. This is possible because nutrients are replenished at the pycnocline depth, as estimated by means of Richardson’s dynamic stability. Turbulence created by tides and the shear between overlapping water masses favors the disruption of the pycnocline. We suggest that, during summer, San Jorge Gulf maintains not only high primary productivity but also high phytoplankton biomass turnover rate, which is supported by a high C:N ratio, consistent with strong zooplankton grazing and export of organic carbon to deep waters.


Latorre, M.P., I.R. Schloss, G.O. Almandoz, K. Lemarchand, X. Flores-Melo, V. Massé-Beaulne, and G.A. Ferreyra. 2018. Mixing processes at the pycnocline and vertical nitrate supply: Consequences for the microbial food web in San Jorge Gulf, Argentina. Oceanography 31(4):50–59, https://doi.org/10.5670/oceanog.2018.410.

Supplementary Materials

Agustí, S., C.M. Duarte, D. Vaque, M. Hein, J.M. Gasol, and M. Vidal. 2001. Food-web structure and elemental (C, N and P) fluxes in the eastern tropical North Atlantic. Deep Sea Research Part II 48(10):2,295–2,321, https://doi.org/10.1016/S0967-0645(00)00179-X.

Akselman, R. 1996. Estudios ecológicos en el Golfo San Jorge y aguas adyacentes (Atlántico Sudoccidental). Distribución, abundancia y variación estacional del fitoplancton en relación a factores físico-químicos y la dinámica hidrológica. PhD Thesis, Universidad de Buenos Aires, Buenos Aires, Argentina, 244 pp.

Azam, F., T. Fenchel, J.G. Field, J.S. Gray, L.A. Meyer-Reil, and F. Thingstad. 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10:257–263, https://doi.org/​10.3354/​meps010257.

Belzile, C., S. Brugel, C. Nozais, Y. Gratton, and S. Demers. 2008. Variations of the abundance and nucleic acid content of heterotrophic bacteria in Beaufort Shelf waters during winter and spring. Journal of Marine Systems 74(3–4):946–956, https://doi.org/10.1016/j.jmarsys.2007.12.010.

Belzile, C., and M. Gosselin. 2015. Free-living stage of the unicellular algae Coccomyxa sp. parasite of the blue mussel (Mytilus edulis): Low-light adaptation, capacity for growth at a very wide salinity range and tolerance to low pH. Journal of Invertebrate Pathology 132:201–207, https://doi.org/10.1016/​j.jip.2015.10.006.

Behrenfeld, M.J., R.T. O’Malley, D.A. Siegel, C.R. McClain, J.L. Sarmiento, G.C. Feldman, A.J. Milligan, P.G. Falkowski, R.M. Letelier, and E.S. Boss. 2006. Climate-driven trends in contemporary ocean productivity. Nature 444(7120):752–755, https://doi.org/10.1038/nature05317.

Bianchi, A.A., L. Bianucci, A.R. Piola, D.R. Pino, I. Schloss, A. Poisson, and C.F. Balestrini. 2005. Vertical stratification and air-sea CO2 fluxes in the Patagonian shelf. Journal of Geophysical Research 110(7), C07003, https://doi.org/​10.1029/2004JC002488.

Blomqvist, S., A. Gunnars, and R. Elmgren. 2004. Why the limiting nutrient differs between temperate coastal seas and freshwater lakes: A matter of salt. Limnology and Oceanography 49(6):2,236–2,241, https://doi.org/10.4319/lo.2004.49.6.2236.

Carr, M.-E., M.R. Lewis, and D. Kelley. 1995. A physical estimate of new production in the equatorial Pacific along 150°W. Limnology and Oceanography 40(1):138–147, https://doi.org/​10.4319/lo.1995.40.1.0138.

Childers, A.R., T.E. Whitledge, and D.A. Stockwell. 2005. Seasonal and interannual variability in the distribution of nutrients and chlorophyll a across the Gulf of Alaska shelf: 1998-2000. Deep Sea Research Part II 52(1–2):193–216, https://doi.org/​10.1016/j.dsr2.2004.09.018.

Cucchi Colleoni, A.D., and J.I. Carreto, 2001. Variación estacional de la biomasa fitoplanctonica en Golfo San Jorge. Resultados de las campañas de investigación: OB-01/0, OB-03/00, OB-10/00 y OB-12/00. Instituto Nacional de Desarrollo Pesquero (INIDEP), Mar del Plata, Argentina, 30 pp.

Dave, A.C., and M.S. Lozier. 2013. Examining the global record of interannual variability in stratification and marine productivity in the low-latitude and mid-latitude ocean. Journal of Geophysical Research 118(6):3,114–3,127, https://doi.org/10.1002/jgrc.20224.

Falkowski, P.G., M.E. Katz, A.H. Knoll, A. Quigg, J.A. Raven, O. Schofield, and F.J.R. Taylor. 2004. The evolution of modern eukaryotic phytoplankton. Science 305(5682):354–360, https://doi.org/​10.1126/science.1095964.

Falkowski, P., and Z. Kolber. 1995. Variations in chlorophyll fluorescence yields in phytoplankton in the world oceans. Australian Journal of Plant Physiology 22(2):341–355, https://doi.org/10.1071/PP9950341.

Galperin, B., S. Sukoriansky, and P.S. Anderson. 2007. On the critical Richardson number in stably stratified turbulence. Atmospheric Science Letters 8(3):65–69, https://doi.org/10.1002/asl.153.

Giménez, E.M., G. Winkler, M. Hoffmeyer, and G.A. Ferreyra. 2018. Composition, spatial distribution, and trophic structure of the zooplankton community in San Jorge Gulf, southwestern Atlantic Ocean. Oceanography 31(4):154–163, https://doi.org/​10.5670/oceanog.2018.418.

Glembocki, N.G., G.N. Williams, M.E. Góngora, D.A. Gagliardini, and J.M. (Lobo) Orensanz. 2015. Synoptic oceanography of San Jorge Gulf (Argentina): A template for Patagonian red shrimp (Pleoticus muelleri) spatial dynamics. Journal of Sea Research 95:22–35, https://doi.org/10.1016/​j.seares.2014.10.011.

Glibert, P.M. 2016. Margalef revisited: A new phytoplankton mandala incorporating twelve dimensions, including nutritional physiology. Harmful Algae 55:25–30, https://doi.org/10.1016/​j.hal.2016.01.008.

Gonçalves-Araujo, R., M.S. de Souza, C.R.B. Mendes, V.M. Tavano, and C.A.E. Garcia. 2016. Seasonal change of phytoplankton (spring vs. summer) in the southern Patagonian shelf. Continental Shelf Research 124:142–152, https://doi.org/10.1016/​j.csr.2016.03.023.

Góngora, M.E., D. González-Zevallos, A. Pettovello, and L. Mendía. 2012. Caracterización de las principales pesquerías del golfo San Jorge Patagonia, Argentina. Latin American Journal of Aquatic Research 40(1):1–11, https://doi.org/10.3856/vol40-issue1-fulltext-1.

Gregg, W.W., N.W. Casey, and C.R. McClain. 2005. Recent trends in global ocean chlorophyll. Geophysical Research Letters 32(3), L03606, https://doi.org/10.1029/2004GL021808.

Hillebrand, H., C.-D. Dürselen, D. Kirschtel, U. Pollingher, and T. Zohary. 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35(2):403–424, https://doi.org/​10.1046/j.1529-8817.1999.3520403.x.

Kolber, Z., O. Prasil, and P.G. Falkowski. 1998. Measurements of variable fluorescence using fast repetition rate techniques: Defining methodology and experimental protocols. Biochimica et Biophysica Acta 1367:88–106, https://doi.org/​10.1016/S0005-2728(98)00135-2.

Krock, B., C.M. Borel, F. Barrera, U. Tillmann, E. Fabro, G.O. Almandoz, M. Ferrario, J.E. Garzón Cardona, B.P. Koch, C. Alonso, and others 2015. Analysis of the hydrographic conditions and cyst beds in the San Jorge Gulf, Argentina, that favor dinoflagellate population development including toxigenic species and their toxins. Journal of Marine Systems 148:86–100, https://doi.org/10.1016/​j.jmarsys.2015.01.006.

Legendre, P., and L. Legendre. 1998. Numerical Ecology: Second English Edition. Developments in Environmental Modelling vol. 20, Montréal, Canada, 322 pp.

Legendre, L., and F. Rassoulzadegan. 1995. Plankton and nutrient dynamics in marine waters. Ophelia 41(1):153–172, https://doi.org/10.1080/​00785236.1995.10422042.

Lewandowska, A.M., D.G. Boyce, M. Hofmann, B. Matthiessen, U. Sommer, and B. Worm. 2014. Effects of sea surface warming on marine plankton. Ecology Letters 17(5):614–623, https://doi.org/​10.1111/ele.12265.

Litchman, E., and C.A. Klausmeier. 2008. Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution, and Systematics 39(1):615–639, https://doi.org/10.1146/annurev.ecolsys.39.110707.173549.

Mann, K.H., and J.R. Lazier. 2006. Dynamics of Marine Ecosystems: Biological-Physical Interactions in the Oceans, 3rd ed. Blackwell Publishing, USA, 496 pp.

Margalef, R. 1978. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 1:493–509.

Martin, P., L. Serio, A. Pescio, and W. Dragani. 2016. Persistencia de vientos superficiales del cuadrante este en estaciones costeras de la Patagonia. Asociación Argentina de Geofísicos y Geodestas 40(2):87–97.

Massé-Beaulne, V. 2017. Métabolisme de la communauté microbienne et flux de carbone à court terme dans le golfe San Jorge, Patagonie (Argentine). MSc. thesis, Université du Québec à Rimouski, Québec, Canada, 121 p.

Matano, R.P., and E.D. Palma. 2018. Seasonal variability of the oceanic circulation in the Gulf of San Jorge, Argentina. Oceanography 31(4):16–24, https://doi.org/​10.5670/oceanog.2018.402.

Menden-Deuer, S., and E.J. Lessard. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45(3):569–579, https://doi.org/​10.4319/lo.2000.45.3.0569.

Mojica, K.D.A., W.H. van de Poll, M. Kehoe, J. Huisman, K.R. Timmermans, A.G.J. Buma, H.J. van der Woerd, L. Hahn-Woernle, H.A. Dijkstra, and C.P.D. Brussaard. 2015. Phytoplankton community structure in relation to vertical stratification along a north-south gradient in the Northeast Atlantic Ocean. Limnology and Oceanography 60(5):1,498–1,521, https://doi.org/​10.1002/​lno.10113.

Moore, C.M., D.J. Suggett, A.E. Hickman, Y.-N. Kim, J.F. Tweddle, J. Sharples, R.J. Geider, and P.M. Holligan. 2006. Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnology and Oceanography 51(2):936–949, https://doi.org/​10.4319/lo.2006.51.2.0936.

Oksanen, J., F.G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P.R. Minchin, R.B. O’Hara, G.L. Simpson, P. Solymus, and others 2017. Community Ecology Package, Package ‘vegan.’ Foundation for Statistical Computing, Vienna, 105 pp.

Paparazzo, F.E., L. Bianucci, I.R. Schloss, G.O. Almandoz, M. Solís, and J.L. Esteves. 2010. Cross-frontal distribution of inorganic nutrients and chlorophyll-a on the Patagonian Continental Shelf of Argentina during summer and fall. Revista de Biología Marina Y Oceanografía 45(1):107–119, https://doi.org/10.4067/S0718-19572010000100010.

Paparazzo, F.E., G.N. Williams, J.P. Pisoni, M. Solís, J.L. Esteves, and D.E. Varela. 2017. Linking phytoplankton nitrogen uptake, macronutrients and chlorophyll-a in SW Atlantic waters: The case of the Gulf of San Jorge, Argentina. Journal of Marine Systems 172:43–50, https://doi.org/10.1016/​j.jmarsys.2017.02.007.

Parsons, T.R., Y. Maita, and C.M. Lalli. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, New York, 173 pp.

Putt, M., and D.K. Stoecker. 1989. An experimentally determined carbon:volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnology and Oceanography 34:1,097–1,103, https://doi.org/​10.4319/lo.1989.34.6.1097.

Romero, S.I., A.R. Piola, M. Charo, and C.A. Eiras Garcia. 2006. Chlorophyll-a variability off Patagonia based on SeaWiFS data. Journal of Geophysical Research 111(C5), C05021, https://doi.org/​10.1029/2005JC003244.

Savoye, N., A. Aminot, P. Tréguer, M. Fontugne, N. Naulet, and R. Kérouel. 2003. Dynamics of particulate organic matter δ15N and δ13C during spring phytoplankton blooms in a macrotidal ecosystem (Bay of Seine, France). Marine Ecology Progress Series 255:27–41, https://doi.org/10.3354/meps255027.

Suggett, D., G. Kraay, P. Holligan, M. Davey, J. Aiken, and R. Geider. 2001. Assessment of photosynthesis in a spring cyanobacterial bloom by use of a fast repetition rate fluorometer. Limnology and Oceanography 46(4):802–810, https://doi.org/​10.4319/​lo.2001.46.4.0802.

Suggett, D.J., C.M. Moore, A.E. Hickman, and R.J. Geider. 2009. Interpretation of fast repetition rate (FRR) fluorescence: Signatures of phytoplankton community structure versus physiological state. Marine Ecology Progress Series 376:1–19, https://doi.org/​10.3354/meps07830.

Tarran, G.A., J.L. Heywood, and M.V. Zubkov. 2006. Latitudinal changes in the standing stocks of nano- and picoeukaryotic phytoplankton in the Atlantic Ocean. Deep Sea Research Part II 53(14–16):1,516–1,529, https://doi.org/​10.1016/j.dsr2.2006.05.004.

Thorpe, S.A. 2007. An Introduction to Ocean Turbulence. Cambridge University Press, NY, 293 pp.

Tomas, C.R. 1997. Identifying Marine Phytoplankton. Academic Press, California, 875 pp.

Tonini, M., E. Palma, and A. Rivas. 2006. Modelos de alta resolución de los golfos patagónicos. Mecánica Computacional XXV:1,441–1,460.

Torres, A.I., F.E. Paparazzo, G.N. Williams, A.L. Rivas, M.E. Solís, and J.L. Esteves. 2018. Dynamics of macronutrients in the San Jorge Gulf during spring and summer. Oceanography 31(4):25–32, https://doi.org/​10.5670/oceanog.2018.407.

Tremblay, G., C. Belzile, M. Gosselin, M. Poulin, S. Roy, and J.É. Tremblay. 2009. Late summer phytoplankton distribution along a 3500 km transect in Canadian Arctic waters: Strong numerical dominance by picoeukaryotes. Aquatic Microbial Ecology 54(1):55–70, https://doi.org/10.3354/ame01257.

Utermöhl, H. 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik: Mit 1 Tabelle und 15 abbildungen im Text und auf 1 Tafel. Internationale Vereinigung Für Theoretische Und Angewandte Limnologie: Mitteilungen 9(1):1–38.

Valiadi, M., S.C. Painter, J.T. Allen, W.M. Balch, and M.D. Iglesias-Rodriguez. 2014. Molecular detection of bioluminescent dinoflagellates in surface waters of the Patagonian shelf during early austral summer 2008. PloS One 9(2):e98849, https://doi.org/​10.1371/journal.pone.0098849.

Verity, P.G., and C. Langdon. 1984. Relationships between lorica volume, carbon, nitrogen, and ATP content of tintinnids in Narragansett Bay. Journal of Plankton Research 6(5):859–868, https://doi.org/​10.1093/plankt/6.5.859.

Yorio, P. 2009. Marine protected areas, spatial scales, and governance: Implications for the conservation of breeding seabirds. Conservation Letters 2(4):171–178, https://doi.org/​10.1111/​j.1755-263X.2009.00062.x.

Zubkov, M.V., M.A. Sleigh, P.H. Burkill, and R.J.G. Leakey. 2000. Picoplankton community structure on the Atlantic Meridional Transect: A comparison between seasons. Progress in Oceanography 45(3–4):369–386, https://doi.org/10.1016/S0079-6611(00)00008-2.

Zuur, A.F., E.N. Ieno, and C.S. Elphick. 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1(1):3–14, https://doi.org/​10.1111/j.2041-210X.2009.00001.x.