Scientia Marina, Vol 74, No 4 (2010)

Biochemical features of a Protoceratium reticulatum red tide in Chipana Bay (Northern Chile) in summer conditions

Sergio Rossi
Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona , Spain

Ida Fiorillo
Instituto Ciencias del Mar (CSIC) , Spain


Protoceratium reticulatum is considered a potential toxic dinoflagellate. This paper describes a high-frequency monitoring study performed at Chipana Bay (northern Chile), sampling over 48 hours in a near-bottom shallow coastal area to quantify the biochemical features of a red tide dominated by this microscopic algae. This area belongs to the Humboldt Current upwelling system, and is considered highly productive for artisanal fisheries. Total chlorophyll a, total lipids, particulate organic carbon and nitrogen, fatty acids and major phytoplankton group concentration (i.e. dinoflagellates, diatoms, ciliates and cysts) were studied in 7-hour intervals in February 2007. Our results indicate a high concentration of potential available food in the form of lipids ranging from 50 to 300 μg L-1 for benthic suspension feeders, i.e. bivalves. The dominance of P. reticulatum (60-80% of the total cell concentration per litre, ranging from 55x103 to 384x103 cells L-1) can be considered as a possible interference for harvesting in this productive area, although the toxicity of this algae was not proved in the present study. The main dinoflagellate fatty acid markers [18:0, 18:4(n-3), 20:5(n-3), and 22:6(n-3)] showed high proportions (%) during the short time cycle and in at least two cases [the 18:4 (n-3) and 22:6 (n-3) fatty acids] a highly significant relationship with dinoflagellate concentration (cells L-1). The topographical and benthic structure (mainly kelp forest) of the zone helps to retain particles and nutrients that may in part explain the high productivity and food availability, but the presence of recurrent red tides in this coastal area—if they prove to be toxic—is argued to be a major problem for local fisheries.


Protoceratium reticulatum; red tide; available food; dinoflagellate; fatty acids; upwelling system

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Aguilera, V., R. Escribano and L. Herrera. – 2009. High frequency responses of nanoplankton and microplankton to wind-driven upwelling off Northern Chile. J. Mar. Syst., 78: 124-135. doi:10.1016/j.jmarsys.2009.04.005

Arntz, W.E., V.A. Gallardo, D. Gutiérrez, E. Isla, L.A. Levin, J. Mendo, C. Neira, G.T. Rowe, J. Tarazona and M. Wolff. – 2006. En Niño and similar perturbation effects on the benthos of the Humboldt, California, and Benguela current upwelling ecosystems. Adv. Geosci., 6: 243-265. doi:10.5194/adgeo-6-243-2006

Atkinson, M.J. and S.V. Smith. – 1983. C:N:P ratios of benthic marine plants. Limnol. Oceanogr., 28: 568-574. doi:10.4319/lo.1983.28.3.0568

Barnes, H., and J. Blackstock. – 1973. Estimation of lipids in marine animals tissues: detailed investigation of the sulphophosphovanillin method for “total” lipids. J. Exp. Mar. Biol. Ecol., 12: 103-118. doi:10.1016/0022-0981(73)90040-3

Broglio, E., S.H. Jónasdóttir, A. Calbet, H.H. Jakobsen and E. Saiz. – 2003. Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat. Micro. Ecol., 31: 267-278. doi:10.3354/ame031267

Budge, S.M., C.C. Parrish, and C.H. McKenzie. – 2001. Fatty acid composition of phytoplankton, settling particulate organic matter and sediments at a sheltered bivalve aquaculture site. Mar. Chem., 2001: 285-303. doi:10.1016/S0304-4203(01)00068-8

Cembella, A.D., M.A. Quilliam, N.I. Lewis, A.G. Bauder, C. Dell’Aversano, K. Thomas, J. Jellet and F. Cusack. – 2002. The toxigenic marine dinoflagellate Alexandrium tamarese as the probable cause of mortality of caged salmon in Nova Scotia. Harm. Algae, 1: 313-325. doi:10.1016/S1568-9883(02)00048-3

Claustre, H., S.A. Poulet, R. Williams, J.C. Marty, S. Coombs, F. Ben Mlih, A.M. Hapette and V. Martin-Jezequel. – 1990. A biochemical investigation of Pheocystis sp bloom in the Irish Sea. J. Mar. Biol. Ass. U. K., 70: 197-207. doi:10.1017/S0025315400034317

Cloern, J.E. – 1982. Does the benthos control phytoplankton biomass in south San Francisco Bay? Mar. Ecol. Progr. Ser., 9: 191-202. doi:10.3354/meps009191

Dalsgaard, J. and M. St. John. – 2004. Fatty acid biomarkers: validation of food web and trophic markers using 13C–labeled fatty acids in juvenile sandeel (Ammodytes tobianus). Can. J. Fish. Aquat. Sci., 61: 1671-1680. doi:10.1139/f04-095

Dalsgaard, J., M. St. John, G. Kattner, D. Müller-Navarra and W.Hagen. – 2003. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol., 46: 225-340. doi:10.1016/S0065-2881(03)46005-7

Escribano, R., G. Danieri, L. Farías, V.A. Gallardo, H.E. González, D. Gutiérrez, C.B. Lange, C.E. Morales, O. Pizarro, M. Ulloa and P. Braun. – 2004. Biological and chemicals consequences of the 1997-1998 El Niño in the Chilean coastal upwelling system: a synthesis. Deep Sea Res. Part II, 51: 2389-2411. doi:10.1016/j.dsr2.2004.08.011

Fabiano, M. and A. Pusceddu. – 1998. Total and hydrolizable particulate organic matter (carbohydrates, proteins and lipids) at a coastal station in Terra Nova Bay (Ross Sea, Antarctica). Pol. Biol., 19: 125-132. doi:10.1007/s003000050223

Fahl, K. and G. Kattner. – 1993. Lipid content and fatty acid composition of algal communities in sea-ice and water from Weddell Sea (Antarctica). Pol. Biol., 13: 405-409. doi:10.1007/BF01681982

Fegley, S.R., B.A. MacDonald and T.R. Jacobsen. – 1992. Short-term variation in the quantity and quality of seston available to benthic suspension feeders. Est. Coast. Shelf Sci., 34: 393-412. doi:10.1016/S0272-7714(05)80078-2

Fernández-Reiriz, M.J., J.M. Navarro, A.M. Contreras and U. Labarta.– 2008. Trophic interactions between the toxic dinoflagellate Alexandrium catenella and Mytilus chilensis: feeding and digestive behaviour to long-term exposure. Aquat. Tox., 87: 245-251. doi:10.1016/j.aquatox.2008.02.011 PMid:18394727

Garcés, E., M. Masó and J. Camp. – 1999. A recurrent and localized dinoflagellate bloom in Mediterranean beach. J. Plank. Res., 21: 2373-2391. doi:10.1093/plankt/21.12.2373

Gasol, J.M., E. Garcés and M. Vila. – 2005. Strong small-scale temporal bacterial changes associated with the migrations of bloom-forming dinoflagellates. Harm. Algae, 4: 771-781. doi:10.1016/j.hal.2004.12.007

González, H.E., R. Giesecke, C.A. Vargas, M. Pavez, J. Iriarte, P. Santibañez, L. Castro, R. Escribano and F. Pagès. – 2004. Carbon cycling through the pelagic foodweb in the northern Humboldt Current off Chile (23ºS). I.C.E.S. J. Mar. Sci., 61: 572-584. doi:10.1016/j.icesjms.2004.03.021

Grémare, A., A. Marsh and K. Tenore. – 1988. Short-term reproductive responses of Capitella sp. I (Annelida: Polychaeta) fed on different diets. J. Exp. Mar. Biol. Ecol., 123: 147-162. doi:10.1016/0022-0981(88)90166-9

Grémare, A., J.M. Amouroux, F. Charles, A. Dinet, C. Riaux-Gobin, J. Baudart, L. Medernach, J.Y. Bodiou, G.Vétion, J.C. Colomines and P. Albert. – 1997. Temporal changes in the biochemical composition and nutritional value of the particulate organic matter available to surface deposit-feeders: a two year study. Mar. Ecol. Progr. Ser., 150: 195-206. doi:10.3354/meps150195

Guerrini, F., P. Ciminiello, C. Dell’Aversano, L. Tartaglione, E. Fattorusso, L. Boni and R. Pistocchi. – 2007. Influence of temperature, salinity and nutrient limitation on yessotoxin production and release by the dinoflagellate Protoceratium reticulatum in batch cultures. Harm. Algae, 6: 707-717. doi:10.1016/j.hal.2007.02.006

Hallegraeff, G.M., P.D. Nichols, J.K. Volkman, S.I. Blackburn and D.A. Everitt. – 1991. Pigments, fatty acids, and sterols of the toxic dinoflagellate Gymnodinium catenatum. J. Phycol., 27: 591-599. doi:10.1111/j.0022-3646.1991.00591.x

Hernández-Miranda, E., A.T. Palma and F.P. Ojeda. – 2003. Larval fish assemblages in nearshore coastal waters off central Chile: temporal and spatial patterns. Est. Coast. Shelf Sci., 56: 1075-1092. doi:10.1016/S0272-7714(02)00308-6

Herrera, L. and R. Escribano. – 2006. Factors structuring the phytoplankton community in the upwelling site off El Loa River in northern Chile. J. Mar. Syst., 61: 13-38. doi:10.1016/j.jmarsys.2005.11.010

Hitchcock, G.L. – 1982. A comparative study of the size-dependent organic composition of marine diatoms and dinoflagellates. J. Plank. Res., 4: 363-377. doi:10.1093/plankt/4.2.363

Klungsøyr, J., S. Tilseth, S. Wilhelmsen, S. Falk-Petersen and J.R. Sargent. – 1989. Fatty acid composition as an indicator of food intake in cod larvae Gadus morhua from Lofoten, Northern Norway. Mar. Biol., 102: 183-188. doi:10.1007/BF00428278

Kuwata, A., T. Hama and M. Takahashi. – 1993. Ecophysiological characterization of two life forms, resting spores and resting cells, of a marine planktonic diatom, Chaetoceros pseudocurvisetus, formed under nutrient depletion. Mar. Ecol. Progr. Ser., 102: 245-255. doi:10.3354/meps102245

Li, S.C., W.X. Wang and D.P.H. Hsie. – 2002. Effects of toxic dinoflagellate Alexandrium tamarese on the energy budgets and growth of two marine bivalves. Mar. Environ. Res., 53: 145-160. doi:10.1016/S0141-1136(01)00117-9

MacKenzie, L., P. Holland, P. McNabb, V. Beuzenberg, A. Selwood and T. Suzuki. – 2002. Complex toxin profiles in phytoplankton and greenshell mussels (Perna canaliculus), revealed by LC-MS/MS analysis. Toxicon, 40: 1321-1330. doi:10.1016/S0041-0101(02)00143-5

Mansour, M.P., J.K. Volkman, A.E. Jackson and S.I. Blackburn. – 1999. The fatty acid and sterol composition of five marine dinoflagellates. J. Phycol., 35: 710-720. doi:10.1046/j.1529-8817.1999.3540710.x

Masó, M. and E. Garcés. – 2006. Harmful microalgae blooms (HAB): problematic conditions that induce them. Mar. Poll. Bull., 53: 620-630. doi:10.1016/j.marpolbul.2006.08.006 PMid:17010385

Nielsen, M.V. and T. Stromgrem. – 1991. Shell growth response of mussels (Mytilus edulis) exposed to toxic microalgae. Mar. Biol., 108: 263-267. doi:10.1007/BF01344341

Palma, W., R. Escribano and S.A. Rosales. – 2006. Modelling study and inter-annual variability of circulation in the coastal upwelling site of the El Loa River off northern Chile. Est. Coast. Shelf Sci., 67: 93-107. doi:10.1016/j.ecss.2005.11.011

Parsons, T.R., Y. Maita and C.M. Lalli. – 1985. Fluorometric determination of Chlorophylls. In: A manual of chemical and biological methods for sea water analysis. Pergamon Press, Oxford: pp 201-203.

Paz, B., P. Riobó, I. Ramilo and J.M. Franco. – 2007. Yessotoxins profile in strains of Protoceratium reticulatum from Spain and USA. Toxicon, 50: 1-17. doi:10.1016/j.toxicon.2007.02.005 PMid:17395228

Pitcher, G.C. and D. Calder. – 2000. Harmful algal blooms of the southern Benguela Current: a review and appraisal of monitoring from 1989 to 1997. South Afr. J. Mar. Sci., 22: 255-271.

Quiroga, E., R. Quiñones, M. Palma, J. Sellanes, V.A. Gallardo, D. Gerdes and G. Rowe. – 2005. Biomass size-spectra of macrobenthic communities in the oxygen minimum zone off Chile. Est. Coast. Shelf Sci., 62: 217-231. doi:10.1016/j.ecss.2004.08.020

Reguera, B., I. Bravo, J. Mariño, M.J. Campos, S. Fraga and A. Carbonell.– 1993. Trends in the occurrence of Dinoiphysis spp in Galician coastal waters. In: T.J. Samyda and Y. Shimizu (eds.) Toxic phytoplankton blooms in the sea, pp. 559-564. Elsevier, Amsterdam.

Reuss, N. and L.K. Poulsen. – 2002. Evaluation of fatty acids as biomarkers for a natural plankton community. A field study of a spring bloom and a post-bloom period off West Greenland. Mar. Biol., 141: 423-434. doi:10.1007/s00227-002-0841-6

Rossi, S. and J.M. Gili. – 2005. Composition and temporal variation of the near-bottom seston in a Mediterranean coastal area. Est. Coast. Shelf Sci., 65: 385-395. doi:10.1016/j.ecss.2005.05.024

Rossi, S. and J.M. Gili. – 2007. Short-time-scale variability of near bottom seston composition during spring in a warm temperate sea. Hydrobiologia, 557: 373-388. doi:10.1007/s10750-006-0390-y

Rossi, S., M. Youngbluth, C. Jacoby, F. Pagès and X. Garrofé. – 2008. Fatty acid composition and trophic links among seston, crustacean zooplankton and the siphonophore Nanomia cara in Georges Basin and Oceanographer Canyon (NW Atlantic). Sci. Mar., 72(2): 403-416.

Ruiz, J., T. Antequera, A.I. Andres, M.J. Petron and E. Muriel. – 2004. Improvement of a solid phase extraction method for analysis of lipid fractions in muscle foods. Anal. Chem. Acta, 520: 201-205. doi:10.1016/j.aca.2004.04.059

Russell, J.M. and J.P. Werne. – 2007. The use of solid phase extraction columns in fatty acid purification. Org. Geochem., 38: 48-51. doi:10.1016/j.orggeochem.2006.09.003

Samdal, I.A., L.J. Naustvoll, P. Olseng, L.R. Briggs and C.O. Miles, 2004. Use of ELISA to identify Protoceratium reticulatum as a source of yessotoxin in Norway. Toxicon, 44: 75-82. doi:10.1016/j.toxicon.2004.04.010 PMid:15225565

Satake, M., L. MacKenzie and T. Yasumoto. – 1997. Identification of Protoceratium reticulatum as the biogenic origin of yessotoxin. Nat. Tox., 5: 164-167. doi:10.1002/19970504NT7

Sekiguchi, K., T. Ogata, S. Kaga, M. Yoshida, Y. Fukuyo and M. Kodama. – 2001. Accumulation of paralytic shellfish toxins in the scallop Patinopecten yessoensis caused by the dinoflagellate Alexandrium catenella in Otsichi Bay, Iwate Prefecture, northern Pacifis coast of Japan. Fish. Sci., 67: 1157-1162. doi:10.1046/j.1444-2906.2001.00374.x

St. John, M.A. and T. Lund. – 1996. Lipid biomarkers: linking the utilization of frontal plankton biomass to enhanced condition of juvenile North Sea cod. Mar. Ecol. Progr. Ser., 131: 75-85. doi:10.3354/meps131075

Taylor, C.D. and B.L. Howes. – 1994. Effect of sampling frequency on measurements of seasonal primary production and oxygen status in near-shore coastal ecosystems. Mar. Ecol. Progr. Ser., 108: 193-203. doi:10.3354/meps108193

Thatje, S., O. Heilmayer and J. Laudien. – 2008. Climate variability and El Niño Southern Oscillation: implications for natural coastal resources and management. Helg. Mar. Res., 62(suppl 1): S5-S14. doi:10.1007/s10152-008-0104-0

Uribe, P. and R.T. Espejo. – 2003. Effect of associated bacteria on the growth and toxicity of Alexandrium catenella. Appl. Environ. Microb., 69: 659-662. doi:10.1128/AEM.69.1.659-662.2003 PMid:12514056    PMCid:152396

Utermöhl, M. – 1958. Zur vervolkommung der qualitativen Phytoplankton metodik. Mitt. Intern. Verein. Limnol., 9: 1-38.

Vargas, C.A., R. Escribano and S. Poulet. – 2006. Phytoplankton food quality determines time windows for successful zooplankton reproductive pulses. Ecology, 87: 2992-2999. doi:10.1890/0012-9658(2006)87[2992:PFQDTW]2.0.CO;2

Villegas, M.J., J. Laudien, W. Sielfeld and W.E. Arntz. – 2008. Macrocystis integriflora and Lessonia trabeculata (Laminares; Phaeophyceae) kelp habitat structures and associated macrobenthic community off northern Chile. Helg. Mar. Res., 62(1): 33-43. doi:10.1007/s10152-007-0096-1

Zingone, A. and H.O. Enevoldsen. – 2000. The diversity of harmful algal blooms: a challenge for science and management. Oceanogr. Coast. Manag., 43: 725-748. doi:10.1016/S0964-5691(00)00056-9

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