Skip to main content

Advertisement

SpringerLink
Log in

Effect of increasing sea water temperature on the growth and toxin production of the benthic dinoflagellate Prorocentrum lima

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

In future decades, harmful algae blooms may increase in frequency in aquatic environments as a result of higher global temperatures (warming). This study tested the hypothesis that cell growth rate and Diarrethic Shellfish Poisoning (DSP) toxin (okadaic acid, OA; dinophysistoxin 1, DTX1) per cell of the benthic dinoflagellate Prorocentrum lima increases with temperature. P. lima cells were grown in f/2 medium at irradiances of 50 ± 15 µmol m−2 s−1 and photoperiod of 12 h L:12 h D. Cell abundance, photosynthetic efficiency (Fv/Fm), and nutrient consumption (NO3− + NO2− and PO43−) were also determined. P. lima optimum growth temperature was at 15 and 25°C but the highest Fv/Fm values showed no association to the maximum growth rate. P. lima showed lower cell growth rates and Fv/Fm values at both 5 and 30°C. Only free OA concentration per cell showed an increase with temperature up to 15°C. Highest lipophilic toxicity in P. lima was found during the stationary growth phase at low (10–15°C) and elevated (30°C) temperatures. Results from this study suggest that future changes to climatic conditions in coastal waters may lead to higher growth rates and cellular toxin levels in P. lima populations worldwide.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aligizaki, K., G. Nikolaidis, P. Katikou, A. D. Baxevanis & T. J. Abatzopoulos, 2009. Potentially toxic epiphytic Prorocentrum (Dinophyceae) species in Greek coastal waters. Harmful Algae 8: 299–311.

    Article  CAS  Google Scholar 

  • Ben-Gharbia, H., O. K.-D. Yahia, Z. Amzil, N. Chomérat, E. Abadie, E. Masseret, M. Sibat, M., H. Z. Triki, H. Nouri & M. Laabir, 2016. Toxicity and growth assessments of three thermophilic benthic dinoflagellates (Ostreopsis cf. ovata, Prorocentrum lima and Coolia monotis) developing in the southern Mediterranean basin. Toxins 8: 297.

  • Berges, J. A., D. E. Varela & P. J. Harrison, 2002. Effects of temperature on growth rate, cell composition and nitrogen metabolism in the marine diatom Thalassiosira pseudonana (Bacillariophyceae). Marine Ecology Progress Series 225: 139–146.

    Article  Google Scholar 

  • Bravo, I., M. L. Fernandez, I. Ramilo & A. Martinez, 2001. Toxin composition of the toxic dinoflagellate Prorocentrum lima isolated from different locations along the Galician coast (NW Spain). Toxicon 39: 1537–1545.

    Article  CAS  PubMed  Google Scholar 

  • Bresnan, E., L. Fernand, K. Davidson, M. Edwards, S. Milligan, R. Gowan, J. Silke, S. Kroger & R. Raine, 2010. Climate change impacts on harmful algal blooms (HABs) in MCCIP Annual Report Card 2010–2011, MCCIP Science Review, 10 pp. www.mccip.org.uk/arc

  • Calbet, A., M. Bertos, C. Fuentes-Grünewald, E. Alacid, R. Figueroa, B. Renom & E. Garcés, 2011. Intraspecific variability in Karlodinium veneficum: Growth rates, mixotrophy, and lipid composition. Harmful Algae 10: 654–667.

    Article  Google Scholar 

  • Dale, B., M. Edwards & P. Reid, 2006. Climate change and harmful algal blooms. In Granéli, E. & J. T. Turner (eds), Ecology of Harmful Algae. Springer, Berlin: 367–378.

    Chapter  Google Scholar 

  • Daranas, A. H., M. Norte & J. J. Fernandez, 2001. Toxic marine microalgae. Toxicon 39: 1101–1132.

    Article  CAS  PubMed  Google Scholar 

  • FAO (Food and Agriculture Organization of the United Nations), 2004. Marine biotoxins. FAO Food and Nutrition Paper 80. Food and Agriculture Organization, Rome, Italy

  • Faust, M. A., 1991. Morphology of ciguatera-causing Prorocentrum lima (Pyrrophyta) from widely differing sites. Journal of Phycology 27: 642–648.

    Article  Google Scholar 

  • Foden, J., D. A. Purdie, S. Morris & S. Nascimento, 2005. Epiphytic abundance and toxicity of Prorocentrum lima populations in the Fleet Lagoon, UK. Harmful Algae 4: 1063–1074.

    Article  CAS  Google Scholar 

  • Fujiki, H. & M. Suganuma, 1999. Unique features of the okadaic acid activity class of tumor promoters. Journal of Cancer Research and Clinical Oncology 125: 150–155.

    Article  CAS  PubMed  Google Scholar 

  • Geider, R. & J. La Roche, 2002. Redfield revisited: variability of C:N: P in marine microalgae and its biochemical basis. European Journal of Phycology 37: 1–17.

    Article  Google Scholar 

  • Gerseen, A., P. Mulder & J. De Boer, 2007. A novel LC method for the separation of marine lipophilic biotoxins. Third International Symposium on Recent Advances in Food Analysis. Prague, Czech Republic. 249 pp.

  • GEOHAB, 2001. Global ecology and oceanography of harmful algal blooms. Science Plan. In Glibert P. & Pitcher G. (eds). SCOR and IOC, Baltimore and Paris: 87.

  • Giussani, V., V. Asnaghi, A. Pedroncini & M. Chiantore, 2017. Management of harmful benthic dinoflagellates requires targeted sampling methods and alarm thresholds. Harmful Algae 68: 97–104.

    Article  PubMed  Google Scholar 

  • Glibert, P. M., J. M. Burkholder & T. M. Kana, 2012. Recent insights about relationships between nutrient availability, forms, and stoichiometry, and the distribution, ecophysiology, and food web effects of pelagic and benthic Prorocentrum species. Harmful Algae 14: 231–259.

    Article  Google Scholar 

  • Grasshoff, K., 1976. Methods of Seawater Analysis. Verlag Chemie, New York: 317.

    Google Scholar 

  • Hallegraeff, G. M., 2003. Harmful algal blooms: a global overview. In Hallegraeff, G. M., D. M. Anderson & A. D. Cembella (eds), Manual on Harmful Marine Microalgae. UNESCO, France: 25–49.

    Google Scholar 

  • Hallegraeff, G. M., 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. Journal of Phycology 46: 220–235.

    Article  CAS  Google Scholar 

  • Heisler, J., P. M. Glibert, J. M. Burkholder, D. M. Anderson, W. Cochlan, W. C. Dennison, Q. Dortch, C. J. Gobler, C. A. Heil, E. Humphries, A. Lewitus, R. Magnien, H. G. Marshall, K. Sellner, D. A. Stockwell, D. K. Stoecker & M. Suddleson, 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8: 3–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heredia-Tapia, A., B. O. Arredondo-Vega, E. J. Nuñez-Vázquez, T. Yasumoto, M. Yasuda & J. L. Ochoa, 2002. Isolation of Prorocentrum lima (Syn. Exuviella lima) and diarrhetic shellfish poisoning (DSP) risk assessment in the Gulf of California, México. Toxicon 40: 1121–1127.

    Article  CAS  PubMed  Google Scholar 

  • Hou, D. Y., J. J. Liang, C. Zou, H. Y. Li, J. S. Liu & W. D. Yang, 2015. MRP functional activity and character in the dinoflagellate Prorocentrum lima. Journal of Applied Phycology 28: 1667–1676.

    Article  Google Scholar 

  • Islabão, C. A., C. R. B. Mendes, A. D. P. G. Russo & C. Odebrecht, 2016. Effects of irradiance on growth, pigment content and photosynthetic efficiency on three peridinin-containing dinoflagellates. Journal of Experimental Marine Biology and Ecology 485: 73–82.

    Article  Google Scholar 

  • Islam, M. A. & J. Beardall, 2017. Growth and photosynthetic characteristics of toxic and non-toxic strains of the cyanobacteria Microcystis aeruginosa and Anabaena circinalis in relation to light. Microorganisms 5: 45.

    Article  PubMed Central  Google Scholar 

  • Kirkwood, D., 1996. Nutrients: practical notes on their determination in sea water. 25 pp.

  • Koike, K., S. Sato, M. Yamaji, Y. Nagahama, Y. Kotaki, T. Ogata & M. Kodama, 1998. Occurrence of okadaic acid-producing Prorocentrum lima on the Sanriku coast, Northern Japan. Toxicon 36: 2039–2042.

    Article  CAS  PubMed  Google Scholar 

  • Kolber, Z. S., O. Prášil & P. G. Falkowski, 1998. Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochimica et Biophysica Acta 1367: 88–106.

    Article  CAS  PubMed  Google Scholar 

  • Kremp, A., A. Godhe, J. Egardt, S. Dupont, S. Suikkanen, S. Casabianca & A. Penna, 2012. Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecology and Evolution 2: 1195–1207.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lakeman, M. B., P. von Dassow & R. A. Cattolico, 2009. The strain concept in phytoplankton ecology. Harmful Algae 8: 746–758.

    Article  Google Scholar 

  • Landsberg, J. H., G. H. Balazs, K. A. Steidinger, D. G. Baden, T. M. Work & D. J. Russell, 1999. The potential role of natural tumor promoters in marine turtle fibropapillomatosis. Journal of Aquatic Animal Health 11: 199–210.

    Article  Google Scholar 

  • Lawrence, J. E., J. Grant, M. A. Quilliam, A. G. Bauder & A. D. Cembella, 2000. Colonization and growth of the toxic dinoflagellate Prorocentrum lima and associated fouling macroalgae on mussels in suspended culture. Marine Ecology Progress Series 201: 147–154.

    Article  Google Scholar 

  • Lee, J.-S., T. Igarashi, S. Fraga, E. Dahl, P. Hovgaard & T. Yasumoto, 1989. Determination of diarrhetic shellfish toxins in various dinoflagellate species. Journal of Applied Phycology 1: 147–152.

    Article  Google Scholar 

  • Lee, T. C.-H., F. L.-Y. Fong, K.-C. Ho & F. W.-F. Lee, 2016. The mechanism of diarrhetic shellfish poisoning toxin production in Prorocentrum spp. Physiological and molecular perspectives. Toxins 8(10): 272.

    Article  PubMed Central  Google Scholar 

  • Levasseur, M., J. Y. Couture, A. M. Weise, S. Michaud, M. Elbrachter, G. Sauve & E. Bonneau, 2003. Pelagic and epiphytic summer distributions of Prorocentrum lima and P. mexicanum at two mussel farms in the Gulf of St. Lawrence, Canada. Aquatic Microbial Ecology 30: 283–293.

    Article  Google Scholar 

  • Li, J., M. Li, J. Pan, J. Liang, Y. Zhou & J. Wu, 2012. Identification of the okadaic acid-based toxin profile of a marine dinoflagellate strain Prorocentrum lima by LC-MS/MS and NMR spectroscopic data. Journal of Separation Science 35: 782–789.

    Article  CAS  PubMed  Google Scholar 

  • López-Rosales, L., J. J. Gallardo-Rodríguez, A. Sánchez-Mirón, M. C. Cerón-García, E. H. Belarbi, F. García-Camacho & E. Molina-Grima, 2014. Simultaneous effect of temperature and irradiance on growth and okadaic acid production from the marine dinoflagellate Prorocentrum belizeanum. Toxins 6: 229–253.

    Article  PubMed  PubMed Central  Google Scholar 

  • MacIntyre, H. L. & J. J. Cullen, 2005. Using cultures to investigate the physiological ecology of microalgae. In Andersen, R. A. (ed.), Algal Culturing Techniques. Phycological Society of America, London: 287–326.

    Google Scholar 

  • MacKenzie, L. A., A. I. Selwood, P. McNabb & L. Rhodes, 2011. Benthic dinoflagellate toxins in two warm-temperate estuaries: rangaunu and Parengarenga Harbours, Northland, New Zealand. Harmful Algae 10: 559–566.

    Article  CAS  Google Scholar 

  • Masó, M. & E. Garcés, 2006. Harmful microalgae blooms (HAB); problematic and conditions that induce them. Marine Pollution Bulletin 53: 620–630.

    Article  PubMed  Google Scholar 

  • Maranda, L., S. Corwin, S. Dover & S. L. Morton, 2007. Prorocentrum lima (Dinophyceae) in northeastern USA coastal waters—II: toxin load in the epibiota and in shellfish. Harmful Algae 6: 632–641.

    Article  CAS  Google Scholar 

  • Marques, A., M. L. Nunes, S. K. Moore & M. S. Strom, 2010. Climate change and seafood safety: human health implications. Food Research International 43: 1766–1779.

    Article  Google Scholar 

  • MCCIP, 2010. Marine climate change impacts annual report card 2010–2011. In Baxter, J. M., P. J. Buckley & C. J. Wallace (eds), Summary Report. MCCIP, Lowestoft: 12.

    Google Scholar 

  • McLachlan, J. L., J. C. Marr, A. Conlon-Kelly & A. Adamson, 1994. Effects of nitrogen concentration and cold temperature on DSP-toxin concentrations in the dinoflagellate Prorocentrum lima (Prorocentrales, Dinophyceae). Natural Toxins 2: 263–270.

    Article  CAS  PubMed  Google Scholar 

  • Montagnes, D. J. S., S. A. Kimmance & D. Atkinson, 2003. Using Q10: can growth rates increase linearly with temperature? Aquatic Microbial Ecology 32: 307–313.

    Article  Google Scholar 

  • Moore, C. M., D. J. Suggett, A. E. Hickman, Y. N. Kim, J. F. Tweddle, J. Sharples, R. J. Geider & P. M. Holligan, 2006. Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnology and Oceanography 51: 936–949.

    Article  Google Scholar 

  • Morton, S. L., D. R. Norris & J. W. Bomber, 1992. Effect of temperature, salinity and light-intensity on the growth and seasonality of toxic dinoflagellates associated with ciguatera. Journal of Experimental Marine Biology and Ecology 157: 79–90.

    Article  Google Scholar 

  • Morton, S. L. & D. R. Tindall, 1995. Morphological and biochemical variability of the toxic dinoflagellate Prorocentrum lima isolated from three locations at Heron Island, Australia. Journal of Phycology 31: 914–921.

    Article  CAS  Google Scholar 

  • Mountfort, D. O., T. Suzuki & P. Truman, 2001. Protein phosphatase inhibition assay adapted for determination of total DSP in contaminated mussels. Toxicon 39: 383–390.

    Article  CAS  PubMed  Google Scholar 

  • Murchie, E. H. & T. Lawson, 2013. Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. Journal of Experimental Botany 64: 3983–3998.

    Article  CAS  PubMed  Google Scholar 

  • Nascimento, S. M., 2003. Phytoplankton blooms and water quality of the Fleet Lagoon, Dorset, UK, including studies of isolated toxic strains of Alexandrium minutum and Prorocentrum lima. PhD thesis. University of Southampton, United Kingdom.

  • Nascimento, S. M., D. A. Purdie & S. Morris, 2005. Morphology, toxin composition and pigment content of Prorocentrum lima strains isolated from a coastal lagoon in southern UK. Toxicon 45: 633–649.

    Article  CAS  PubMed  Google Scholar 

  • Nascimento, S. M., F. Salgueiro, M. Menezes, F. A. de Oliveira, V. C. P. Magalhães, J. C. De Paula & S. Morris, 2016. Prorocentrum lima from the South Atlantic: morphological, molecular and toxicological characterization. Harmful Algae 57: 39–48.

    Article  CAS  Google Scholar 

  • Okolodkov, Y. B., G. Campos-Bautista, I. Garate-Lizarraga, J. A. G. Gonzalez-Gonzalez, M. Hoppenrath & V. Arenas, 2007. Seasonal changes of benthic and epiphytic dinoflagellates in the Veracruz reef zone, Gulf of Mexico. Aquatic Microbial Ecology 47: 223–237.

    Article  CAS  Google Scholar 

  • Pan, Y., A. D. Cembella & M. A. Quilliam, 1999. Cell cycle and toxin production in the benthic dinoflagellate Prorocentrum lima. Marine Biology 134: 541–549.

    Article  CAS  Google Scholar 

  • Patil, J. S., R. V. Rodrigues, P. Paul, K. Sathish, M. Rafi & A. C. Anil, 2017. Benthic dinoflagellate blooms in tropical intertidal rock pools: elucidation of photoprotection mechanisms. Marine Biology 164: 89.

    Article  Google Scholar 

  • Peperzak, L., 2003. Climate change and harmful algal blooms in the North Sea. Acta Oecologica 24: S139–S144.

    Article  Google Scholar 

  • Peperzak, L., 2005. Future increase in harmful algal blooms in the North Sea due to climate change. Water Science and Technology 51: 31–36.

    CAS  PubMed  Google Scholar 

  • Pistocchi, R., F. Guerrini, L. Pezzolesi, M. Riccardi, S. Vanucci, P. Ciminiello, C. Dell’Aversano, M. Forino, E. Fattorusso, L. Tartaglione, A. Milandri, M. Pompei, M. Cangini, S. Pigozzi & E. Riccardi, 2012. Toxin levels and profiles in microalgae from the north-western Adriatic Sea-15 years of studies on cultured species. Marine Drugs 10: 140–162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quilliam, M. A. & N. W. Ross, 1996. Analysis of diarrhetic shellfish poisoning toxins and metabolites in plankton and shellfish by ion-spray liquid chromatography mass spectrometry. ACS Symposium Series 619: 351–364.

    CAS  Google Scholar 

  • Quilliam, M. A., W. R. Hardstaff, N. Ishida, J. L. McLachlan, A. R. Reeves, N. W. Ross & A. J. Windust, 1996. Production of diarrhetic shellfish poisoning (DSP) toxins by Prorocentrum lima in culture and development of analytical methods. In Yasumoto, T., Y. Oshima & Y. Fukuyo (eds), Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission of UNESCO, Paris.

    Google Scholar 

  • Raven, J. A. & R. J. Geider, 1988. Temperature and algal growth. New Phytologist 110: 441–461.

    Article  CAS  Google Scholar 

  • Schofield, O., J. Grzymski, M. M. A. Moline & R. V. M. Jovine, 1998. Impact of temperature acclimation on photosynthesis in the toxic red-tide dinoflagellate Alexandrium fundyense (Ca28). Journal of Plankton Research 20: 1241–1258.

    Article  Google Scholar 

  • Sparrow, L., P. Momigliano, G. R. Russ & K. Heimann, 2017. Effects of temperature, salinity and composition of the dinoflagellate assemblage on the growth of Gambierdiscus carpenteri isolated from the Great Barrier Reef. Harmful Algae 65: 52–60.

    Article  PubMed  Google Scholar 

  • Suganuma, M., M. Tatematsu, J. Yatsunami, S. Yoshizama, S. Okabe, D. Uemura & H. Fujiki, 1992. An alternative theory of tissue-specidicity by tumor promotion of okadaic acid in glandular stomach of rats. Carcinogenesis 13: 1841–1845.

    Article  CAS  PubMed  Google Scholar 

  • Sugg, L. M. & F. M. Vandolah, 1999. No evidence for an allelopathic role of okadaic acid among ciguatera-associated dinoflagellates. Journal of Phycology 35: 93–103.

    Article  CAS  Google Scholar 

  • Suggett, D. J., C. M. Moore, A. E. Hickman & 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.

    Article  Google Scholar 

  • Tirado, M. C., R. Clarke, L. A. Jaykus, A. McQuatters-Gollop & J. M. Frank, 2010. Climate change and food safety: a review. Food Research International 43: 1745–1765.

    Article  Google Scholar 

  • Tomas, C. R. & D. G. Baden, 1993. The influence of phosphorus on the growth and cellular toxin content of the benthic dinoflagellate Prorocentrum lima. In Smayda, T. J. & Y. Shimizu (eds), Toxic Phytoplankton Blooms in the Sea. Elsevier Scientific, New York: 565–570.

    Google Scholar 

  • Vale, P., V. Veloso & A. Amorim, 2009. Toxin composition of a Prorocentrum lima strain isolated from the Portuguese coast. Toxicon 54: 145–152.

    Article  CAS  PubMed  Google Scholar 

  • Vanucci, S., F. Guerrini, A. Milandri & R. Pistocchi, 2010. Effects of different levels of N- and P-deficiency on cell yield, okadaic acid, DTX-1, protein and carbohydrate dynamics in the benthic dinoflagellate Prorocentrum lima. Harmful Algae 9: 590–599.

    Article  CAS  Google Scholar 

  • Varkitzi, I., K. Pagou, E. Granéli, I. Hatzianestis, C. Pyrgaki, A. Pavlidou, B. Montesanto & A. Economou-Amilli, 2010. Unbalanced N:P ratios and nutrient stress controlling growth and toxin production of the harmful dinoflagellate Prorocentrum lima (Ehrenberg) Dodge. Harmful Algae 9: 304–311.

    Article  CAS  Google Scholar 

  • Wang, S., J. Chen, Z. Li, Y. Wang, B. Fu, X. Han & L. Zheng, 2015. Cultivation of the benthic microalga Prorocentrum lima for the production of diarrhetic shellfish poisoning toxins in a vertical flat photobioreactor. Bioresource Technology 179: 243–248.

    Article  CAS  PubMed  Google Scholar 

  • Welschmeyer, N. A., 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography 39: 1985–1992.

    Article  CAS  Google Scholar 

  • Winder, M. & U. Sommer, 2012. Phytoplankton response to a changing climate. Hydrobiologia 698: 5–16.

    Article  Google Scholar 

  • Windust, A. J., J. L. Wright & J. L. Mclachlan, 1996. The effects of the diarrhetic shellfish poisoning toxins, okadaic acid and dinophysistoxin1, on the growth of microalgae. Marine Biology 126: 19–25.

    Article  CAS  Google Scholar 

  • Xu, N., D. Shunshan, A. Li, C. Zhang, Z. Cai & Z. Hu, 2010. Effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful Algae 9: 13–17.

    Article  Google Scholar 

  • Yasumoto, T., M. Murata, Y. Oshima, M. Sano, G. K. Matsumoto & J. Clardy, 1985. Diarrhetic shellfish toxins. Tetrahedron 41: 1019–1411.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

AA-C gratefully acknowledges Mike Zubkov and Manuela Hartmann for allowing this study to be possible in the Molecular and Ecology Laboratory of the National Oceanography Centre Southampton. Mark Stinchcombe is thanked for his assistance with nutrient analysis in the Biogeochemistry Laboratory of the NOCS.

Funding

This research was funded by the Consejo Nacional de Ciencia y Tecnología of México (CONACyT) through a PhD scholarship to AA-C.

Author information

Author notes

  1. Aldo Aquino-Cruz

    Present address: Universidad Autónoma Metropolitana, Unidad Xochimilco. Departamento El Hombre y su Ambiente, Laboratorio de Plancton y Bioenergética, Calzada del Hueso 1100, Col. Villa Quietud, 04960, Coyoacán, Ciudad de México, México

Authors and Affiliations

  1. Ocean and Earth Science, University of Southampton, National Oceanography Centre Southampton, Southampton, SO14 3ZH, UK

    Aldo Aquino-Cruz & Duncan A. Purdie

  2. Centre for Environment, Fisheries and Aquaculture Science, Barrack Road, Weymouth, DT4 8UB, UK

    Steve Morris

Authors
  1. Aldo Aquino-Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Duncan A. Purdie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Steve Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aldo Aquino-Cruz.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling editor: David Philip Hamilton

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aquino-Cruz, A., Purdie, D.A. & Morris, S. Effect of increasing sea water temperature on the growth and toxin production of the benthic dinoflagellate Prorocentrum lima. Hydrobiologia 813, 103–122 (2018). https://doi.org/10.1007/s10750-018-3512-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3512-4

Keywords

Search

Navigation