Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

A new approach using biomarkers to elucidate the regression state of the invasive alga Caulerpa taxifolia in waters around the Balearic Islands (Western Mediterranean Sea)

Silvia Tejada A and Antoni Sureda B C
+ Author Affiliations
- Author Affiliations

A Experimental Laboratory, Research Unit, Son Llàtzer Hospital, IUNICS, Carretera Manacor km 4, CP 07198, Palma de Mallorca, Balearic Islands, Spain.

B Grup de Nutrició Comunitària i Estrès Oxidatiu, IUNICS, Departament de Biologia Fonamental i Ciències de la Salut, Universitat de les Illes Balears, 07122 Palma de Mallorca, Spain.

C Corresponding author. Email: tosugo@hotmail.com

Marine and Freshwater Research 64(10) 986-991 https://doi.org/10.1071/MF13012
Submitted: 11 January 2013  Accepted: 18 April 2013   Published: 19 July 2013

Abstract

Invasive algae alter the structure and function of ecosystems. The green alga Caulerpa taxifolia is an invasive alga introduced in the Mediterranean Sea, whereas Caulerpa prolifera is a native species in Mediterranean waters. The aim of the current work was to determine the oxidative status of both Caulerpa species by means of biomarker measures as a possible indicator of the regression state of C. taxifolia in waters around the Balearic Islands (western Mediterranean Sea). The levels of markers of lipid peroxidation, glutathione concentration, activities of antioxidant enzymes and caulerpenyne production were measured in C. prolifera and C. taxifolia fronds. The concentration of the end product of lipid peroxidation, malondialdehyde, was significantly higher in C. taxifolia than in C. prolifera samples. Antioxidant enzyme activities, namely superoxide dismutase glutathione peroxidase and glutathione reductase, as well as the reduced glutathione : glutathione disulfide ratio were lower in C. taxifolia than in C. prolifera, although the concentrations of malondialdehyde were higher in the alien species. No differences were found in catalase activity or in the concentration of caulerpenyne. In conclusion, the invasive alga C. taxifolia presented a more oxidised status, which could be related to its regression in Mallorcan coastal waters.

Additional keywords: antioxidant response, Caulerpa species, oxidative stress.


References

Aebi, H. E. (1984). Catalase. In ‘Methods in Enzymatic Analysis’. (Ed H. U. Bergmeyer.) pp. 273–286. (Verlag Chemie: Basel.)

Alessio, H. M. (2000). Lipid peroxidation in healthy and diseased models: influence of different types of exercise. In ‘Handbook of Oxidants and Antioxidants in Exercise’. Eds C. K. Sen, L. Parker and Ö. Hänninen.) pp. 115–127. (Elsevier: Amsterdam.)

Barbier, P., Guise, S., Huitorel, P., Amade, P., Pesando, D., Briand, C., and Peyrot, V. (2001). Caulerpenyne from Caulerpa taxifolia has an antiproliferative activity on tumor cell line SK–N–SH and modifies the microtubule network. Life Sciences 70, 415–429.
Caulerpenyne from Caulerpa taxifolia has an antiproliferative activity on tumor cell line SK–N–SH and modifies the microtubule network.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtVSntro%3D&md5=03754b4e0befeee4a9257c867bcbacdaCAS | 11798011PubMed |

Bellan-Santini, D., Arnaud, P. M., Bellan, G., and Verlaque, M. (1996). The influence of the introduced tropical alga Caulerpa taxifolia on the biodiversity of the Mediterranean marine biota. Journal of the Marine Biological Association of the United Kingdom 76, 235–237.
The influence of the introduced tropical alga Caulerpa taxifolia on the biodiversity of the Mediterranean marine biota.Crossref | GoogleScholarGoogle Scholar |

Boudouresque, C. F. (1998). Follow up of biological introduction in the sea. Biofutur 179, 76–78.
Follow up of biological introduction in the sea.Crossref | GoogleScholarGoogle Scholar |

Boudouresque, C. F., and Verlaque, M. (2002). Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 44, 32–38.
Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsVyruw%3D%3D&md5=ef187195e10a1707420beb54c2c47b32CAS | 11883681PubMed |

Boudouresque, C. F., Meinesz, A., Ribera, M. A., and Ballesteros, E. (1995). Spread of the green alga Caulerpa taxifolia (Caulerpales, Chlorophyta) in the Mediterranean: possible consequences of a major ecological event. Scientia Marina 59, 21–29.

Box, A., Sureda, A., Tauler, P., Terrados, J., Marbá, N., Pons, A., and de la Salud, M. (2010). Seasonality of caulerpenyne content in native Caulerpa prolifera and invasive C. taxifolia and C. racemosa var. cylindracea in the western Mediterranean Sea. Botanica Marina 53, 367–375.
Seasonality of caulerpenyne content in native Caulerpa prolifera and invasive C. taxifolia and C. racemosa var. cylindracea in the western Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar |

Cebrian, J. (2002). Variability and control of carbon consumption, export, and accumulation in marine communities. Limnology and Oceanography 47, 11–22.
Variability and control of carbon consumption, export, and accumulation in marine communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtlSqs7c%3D&md5=0d0928355f8b8bee308fcea8af685920CAS |

Ceccherelli, G., Piazzi, L., and Balata, D. (2002). Spread of introduced Caulerpa species in macroalgal habitats. Journal of Experimental Marine Biology and Ecology 280, 1–11.
Spread of introduced Caulerpa species in macroalgal habitats.Crossref | GoogleScholarGoogle Scholar |

Chisholm, J. R., and Moulin, P. (2003). Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta). Limnology and Oceanography 48, 787–794.
Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVertbk%3D&md5=5fd6b5d6f52e72fc8e837a07e01f12edCAS |

DeLeve, L. D., and Kaplowitz, N. (1991). Glutathione metabolism and its role in hepatotoxicity. Pharmacology & Therapeutics 52, 287–305.
Glutathione metabolism and its role in hepatotoxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsVOlsr0%3D&md5=0fb8bc738796a10c3664bc2b9f207803CAS |

Elias, S. J., Arner, E. S., Zhong, L., and Holmgren, A. (1999). Oxidants and antioxidants. In ‘Methods in Enzymology’. (Ed L. Packer.) pp. 226–239. (Academic Press: San Diego, CA, USA.)

Erickson, A. A., Paul, V. J., Van Alstyne, K. L., and Kwiatkowski, L. M. (2006). Palatability of macroalgae that use different types of chemical defenses. Journal of Chemical Ecology 32, 1883–1895.
Palatability of macroalgae that use different types of chemical defenses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotlCgsb4%3D&md5=870af5d7c8905d728621118aaa5b2f76CAS | 16906362PubMed |

Flohé, L., and Gunzler, W. A. (1984). Assays for glutathione peroxidase. Methods in Enzymology 105, 114–120.
Assays for glutathione peroxidase.Crossref | GoogleScholarGoogle Scholar | 6727659PubMed |

Flohé, L., and Otting, F. (1984). Superoxide dismutase assays. Methods in Enzymology 105, 93–104.
Superoxide dismutase assays.Crossref | GoogleScholarGoogle Scholar | 6328209PubMed |

Galil, B. S. (2007). Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Marine Pollution Bulletin 55, 314–322.
Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1Ciur4%3D&md5=716067c8853fc36fded45c4362839c96CAS | 17222869PubMed |

Gavagnin, M., Marin, A., Castelluccio, F., Villani, G., and Cimino, G. (1994). Defensive relationships between Caulerpa prolifera and its shelled sacoglossan predators. Journal of Experimental Marine Biology and Ecology 175, 197–210.
Defensive relationships between Caulerpa prolifera and its shelled sacoglossan predators.Crossref | GoogleScholarGoogle Scholar |

Goldberg, D. M., Spooner, R. J. (1984). Glutathione reductase. In ‘Methods in Enzymatic Analysis’. (Ed. H.U. Bergmeyer.) pp. 258–265. (Verlag Chemie: Basel, Germany.)

Iveša, L., Jaklin, A., and Devescovi, M. (2006). Vegetation patterns and spontaneous regression of Caulerpa taxifolia (Vahl) C.Agardh in Malinska (northern Adriatic, Croatia). Aquatic Botany 85, 324–330.
Vegetation patterns and spontaneous regression of Caulerpa taxifolia (Vahl) C.Agardh in Malinska (northern Adriatic, Croatia).Crossref | GoogleScholarGoogle Scholar |

Jaubert, J. M., Chisholm, J. R. M., Minghelli-Roman, A., Marchioretti, M., Morrow, J. H., and Ripley, H. T. (2003). Re-evaluation of the extent of Caulerpa taxifolia development in the northern Mediterranean using airborne spectrographic sensing. Marine Ecology Progress Series 263, 75–82.
Re-evaluation of the extent of Caulerpa taxifolia development in the northern Mediterranean using airborne spectrographic sensing.Crossref | GoogleScholarGoogle Scholar |

Jongman, D. N., Campo, D., Dattolo, E., D’Esposito, D., Duchi, A., Grewe, P., Huisman, J., Verlaque, M., Yokes, M. B., and Procaccini, G. (2013). Identity and origin of a slender Caulerpa taxifolia strain introduced into the Mediterranean Sea. Botanica Marina 56, 27–39.

Jos, A., Pichardo, S., Prieto, A. I., Repetto, G., Vazquez, C. M., Moreno, I., and Camean, A. M. (2005). Toxic cyanobacterial cells containing microcystins induce oxidative stress in exposed tilapia fish (Oreochromis sp.) under laboratory conditions. Aquatic Toxicology 72, 261–271.
Toxic cyanobacterial cells containing microcystins induce oxidative stress in exposed tilapia fish (Oreochromis sp.) under laboratory conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFKnt70%3D&md5=9a5763efa8663cac14a37cb3b56b1f1cCAS | 15820106PubMed |

Jung, V., and Pohnert, G. (2001). Rapid wound-activated transformation of the green algal defensive metabolite caulerpenyne. Tetrahedron 57, 7169–7172.
Rapid wound-activated transformation of the green algal defensive metabolite caulerpenyne.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslCms78%3D&md5=e40185df772969f4668288c2a0476d2dCAS |

Lemee, R., Boudouresque, C. F., Gobert, J., Malestroit, P., Mari, X., Meinesz, A., Menager, V., and Ruitton, S. (1996). Feeding behaviour of Paracentrotus lividus in the presence of Caulerpa taxifolia introduced in the Mediterranean Sea. Oceanologica Acta 19, 245–253.

Longepierre, S., Robert, A., Levi, F., and Francour, P. (2005). How an invasive alga species (Caulerpa taxifolia) induces changes in foraging strategies of the benthivorous fish Mullus surmuletus in coastal Mediterranean ecosystems. Biodiversity and Conservation 14, 365–376.
How an invasive alga species (Caulerpa taxifolia) induces changes in foraging strategies of the benthivorous fish Mullus surmuletus in coastal Mediterranean ecosystems.Crossref | GoogleScholarGoogle Scholar |

McKinnon, J. G., Gribben, P. E., Davis, A. R., Jolley, D. F., and Wright, J. T. (2009). Differences in soft-sediment macrobenthic assemblages invaded by Caulerpa taxifolia compared to uninvaded habitats. Marine Ecology Progress Series 380, 59–71.
Differences in soft-sediment macrobenthic assemblages invaded by Caulerpa taxifolia compared to uninvaded habitats.Crossref | GoogleScholarGoogle Scholar |

Meinesz, A., and Hesse, B. (1991). Introduction of the tropical alga Caulerpa taxifolia and its invasion of the northwestern Mediterranean. Oceanologica Acta 14, 415–426.

Meinesz, A., Belsher, T., Thibaut, T., Antolic, B., Mustapha, K. B., Boudouresque, C.-F., Chiaverini, D., Cinelli, F., Cottalorda, J.-M., Djellouli, A., El Abed, A., Orestano, C., Grau, A. M., Ivesa, L., Jaklin, A., Langar, H., Massuti-Pascual, E., Peirano, A., Tunesi, L., de Vaugelas, J., Zavodnik, N., and Zuljevic, A. (2001). The introduced green alga Caulerpa taxifolia continues to spread in Mediterranean. Biological Invasions 3, 201–210.
The introduced green alga Caulerpa taxifolia continues to spread in Mediterranean.Crossref | GoogleScholarGoogle Scholar |

Paul, V. J., and Fenical, W. (1986). Chemical defense in tropical green algae, order Caulerpales. Marine Ecology Progress Series 34, 157–169.
Chemical defense in tropical green algae, order Caulerpales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhsFegs7k%3D&md5=b6fe92f532bf766b825f0cf22647f5e9CAS |

Paul, V. J., and Van Alstyne, K. L. (1992). Activation of chemical defenses in the tropical green-algae Halimeda spp. Journal of Experimental Marine Biology and Ecology 160, 191–203.
Activation of chemical defenses in the tropical green-algae Halimeda spp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1CqsLY%3D&md5=cf0010cd59dd6f6d624c745cc23ae953CAS |

Pohnert, G., and Jung, V. (2003). Intracellular compartmentation in the biosynthesis of caulerpenyne: study on intact macroalgae using stable-isotope-labeled precursors. Organic Letters 5, 5091–5093.
Intracellular compartmentation in the biosynthesis of caulerpenyne: study on intact macroalgae using stable-isotope-labeled precursors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsFOku7c%3D&md5=e09037bb71f958cb367617466445daaeCAS | 14682772PubMed |

Pou, S., Ballesteros, E., Delgado, O., Grau, A. M., Riera, F., and Weitzmann, B. (1993). Sobre la presencia del alga Caulerpa taxifolia (Vahl) C.Agardh (Caulerpales, Chlorophyta) en aguas costeras de Mallorca. Bolletí Societat d’Història Natural de les Illes Balears 36, 83–90.

Raniello, R., Mollo, E., Lorenti, M., Gavagnin, M., and Buia, M. C. (2007). Phytotoxic activity of caulerpenyne from the Mediterranean invasive variety of Caulerpa racemosa: a potential allelochemical. Biological Invasions 9, 361–368.
Phytotoxic activity of caulerpenyne from the Mediterranean invasive variety of Caulerpa racemosa: a potential allelochemical.Crossref | GoogleScholarGoogle Scholar |

Scheibling, R. E., and Anthony, S. X. (2001). Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides. Marine Biology 139, 139–146.
Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides.Crossref | GoogleScholarGoogle Scholar |

Scheibling, R. E., and Gagnon, P. (2006). Competitive interactions between the invasive green alga Codium fragile ssp. tomentosoides and native canopy-forming seaweeds in Nova Scotia (Canada). Marine Biology 325, 1–14.

Schweikert, K., and Burritt, D. J. (2012). The organophosphate insecticide Coumaphos induces oxidative stress and increases antioxidant and detoxification defences in the green macroalgae Ulva pertusa. Aquatic Toxicology 122–123, 86–92.
The organophosphate insecticide Coumaphos induces oxidative stress and increases antioxidant and detoxification defences in the green macroalgae Ulva pertusa.Crossref | GoogleScholarGoogle Scholar | 22728208PubMed |

Sureda, A., Box, A., Ensenat, M., Alou, E., Tauler, P., Deudero, S., and Pons, A. (2006). Enzymatic antioxidant response of a labrid fish (Coris julis) liver to environmental caulerpenyne. Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology 144, 191–196.
Enzymatic antioxidant response of a labrid fish (Coris julis) liver to environmental caulerpenyne.Crossref | GoogleScholarGoogle Scholar |

Sureda, A., Box, A., Deudero, S., and Pons, A. (2009). Reciprocal effects of caulerpenyne and intense herbivorism on the antioxidant response of Bittium reticulatum and Caulerpa taxifolia. Ecotoxicology and Environmental Safety 72, 795–801.
Reciprocal effects of caulerpenyne and intense herbivorism on the antioxidant response of Bittium reticulatum and Caulerpa taxifolia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1ChsL8%3D&md5=df1c4bb2d3cd1a44be5573ea0293a3a0CAS | 18234333PubMed |

Van Alstyne, K. L. (1988). Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69, 655–663.
Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus.Crossref | GoogleScholarGoogle Scholar |

Vandeputte, C., Guizon, I., Genestie-Denis, I., Vannier, B., and Lorenzon, G. (1994). A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biology and Toxicology 10, 415–421.
A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjsF2nsbs%3D&md5=fcde38a2070f977fb1cd06891adad32aCAS | 7697505PubMed |

Verlaque, M., and Fritayre, P. (1994). Mediterranean algal communities are changing in the face of the invasive alga Caulerpa taxifolia (Vahl) C.Agardh. Oceanologica Acta 17, 659–672.

Winston, G. W., and Digiulio, R. T. (1991). Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology 19, 137–161.
Prooxidant and antioxidant mechanisms in aquatic organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1Kgsrc%3D&md5=f1ac83fbe65f5f0183153ecf0b8b53b6CAS |