Skip to main content

Advertisement

Log in

Invasive macrophytes in a marine reserve (Columbretes Islands, NW Mediterranean): spread dynamics and interactions with the endemic scleractinian coral Cladocora caespitosa

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The invasive algae Lophocladia lallemandii and Caulerpa racemosa are becoming an important threat to benthic assemblages in the Mediterranean Sea. Both species were first detected in Illa Grossa Bay (Columbretes Islands Marine Reserve, NW Mediterranean) in 2006, and their invasion was monitored until 2012. L. lallemandii showed a rapid outburst, spreading around the entire bay in just 2 years and showing the highest abundances between 5 and 10 m of depth (82.07 ± 3.53 % (±SE) in 2011). Caulerpa racemosa showed a slower but steady spread and remained in deeper areas during the first years; however, drastic changes in the depth distribution, with algae invading toward shallower areas, were noted beginning in 2010 and reached abundances of 57.76 ± 1.07 % (±SE) between 10 and 20 m of depth in 2011. Illa Grossa Bay hosts one of the most important populations of the endemic coral Cladocora caespitosa. This study is the first to quantitatively assess interactions between the coral and invasive algae. Although both invasive species L. lallemandii and C. racemosa had overlapping distributions with C. caespitosa, we did not find any lethal or sublethal effects of either invasive algal species. On the other hand, C. caespitosa exhibited toxic activity, which could explain the low overgrowth of living colony parts by C. racemosa.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aranda A, Mallol J, Solano I (1999) Presencia del alga Caulerpa racemosa (Forsskål) J. Agardh (Chlorophyta, Caulerpales) en el Mediterráneo ibérico. Actas XIII Congreso Nac. Bot. Criptogámica, p 53

  • Arnold SN, Steneck RS, Mumby PJ (2010) Running the gauntlet: inhibitory effects of algal turfs on the processes of coral recruitment. Mar Ecol Prog Ser 414:91–105

    Article  Google Scholar 

  • Baldacconi R, Corriero G (2009) Effects of the spread of the alga Caulerpa racemosa var. cylindracea on the sponge assemblage from coralligenous concretions of the Apulian coast (Ionian Sea, Italy). Mar Ecol 30:337–345

    Article  Google Scholar 

  • Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195

    Google Scholar 

  • Ballesteros E, Cebrian E, Alcoverro T (2007) Mortality of shoots of Posidonia oceanica following meadow invasion by the red alga Lophocladia lallemandii. Bot Mar 50:8–13

    Google Scholar 

  • Becerro MA, Paul VJ, Starmer J (1998) Intracolonial variation in chemical defences of the sponge Cacospongia sp. And its consequences on generalist fish predators and the specialist nudibranch predator Glossodoris pallida. Mar Ecol Prog Ser 168:187–196

    Article  Google Scholar 

  • Bedini R, Bonechi L, Piazzi L (2012) Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptog algol 32:383–391

    Article  Google Scholar 

  • Botsford JL (2002) A comparison of ecological tests. ATLA 30:539–550

    CAS  PubMed  Google Scholar 

  • Boudouresque CF, Verlaque M (2002a) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44:32–38

    Article  CAS  PubMed  Google Scholar 

  • Boudouresque CF, Verlaque M (2002b) Assessing scale and impact of ship-transported alien macrophytes in the Mediterranean Sea. In: CIESM (ed) Alien marine organisms introduced by ships in the mediterranean and black seas. CIESM Workshop Monographs 20, Monaco, pp 53–61

  • Cabanellas-Reboredo M, Blanco A, Deudero S, Tejada S (2010) Effects of the invasive macroalga Lophocladia lallemandii on the diet and trophism of Pinna nobilis (Mollusca: Bivalvia) and its guests Pontonia pinnophylax and Nepinnotheres pinnotheres (Crustacea: Decapoda). Sci Mar 74:101–110

  • Cebrian E, Balleresteros E (2007) Invasion of the alien species Lophocladia lallemandii in Eivissa-Formentera (Balearic Islands). In: Pergent Martini C, El Asmi S, (eds) Proceedings of the 3rd Med. Symp. Mar. Vegetation, Marseilles, France. C. Le Ravallec Ed., RAC/SPA publ., Tunis, pp 34–41

  • Cebrian E, Balleresteros E (2009) Temporal and spatial variability in shallow- and deep-water populations of the invasive Caulerpa racemosa var. cylindracea in the Western Mediterranean. Est Coast Shelf Sci 83:469–474

    Article  Google Scholar 

  • Cebrian E, Ballesteros E (2010) Invasion of Mediterranean benthic assemblages by red alga Lophocladia lallemandii (Montagne) F. Schmitz: depth-related temporal variability in biomass and phenology. Aquat Bot 92:81–85

    Article  Google Scholar 

  • Cebrian E, Ballesteros E, Linares C, Tomas F (2011) Do native herbivores provide resistance to Mediterranean marine bioinvasions? A seaweed example. Biol Invasions 13:1397–1408

    Google Scholar 

  • Cebrian E, Linares C, Marschal C, Garrabou J (2012) Exploring the effects of invasive algae on the persistence of gorgonian populations. Biol Invasion 14:2647–2656

    Article  Google Scholar 

  • De Caralt S, Bry D, Bontemps N, Turon X, Uriz MJ, Banaigs B (2013) Source of secondary metabolite variation in Dysidea avara (Porifera: demospongiae): the importance of having good neighbors. Mar Drugs 11:489–503

    Article  PubMed Central  PubMed  Google Scholar 

  • De Ruyter van Steveninck ED, Van Mulekom LL, Breeman AM (1988) Growth inhibition of Lobophora variegate (Lamouroux) Womersley by scleractinian corals. J Exp Mar Biol Ecol 115:169–178

    Article  Google Scholar 

  • Deudero S, Blanco A, Box A, Mateu-Vicens G, Cabanellas-Reboredo M, Sureda A (2010) Interaction between the invasive macroalga Lophocladia lallemandii and the bryozoan Reteporella grimaldii at seagrass meadows: density and physiological responses. Biol Invasion 12:41–52

    Article  Google Scholar 

  • Fontana A, Ciavatta ML, Cimino G (1998) Cladocoran A and B: two novel γ-Hidroxybutenolide Sesterpenes from the Mediterranean coral Cladocora caespitosa. J Org Chem 63:2845–2849

    Article  CAS  Google Scholar 

  • Herndl GJ, Velimirov B (1986) Microheterotrophic utilization of mucus released by the Mediterranean coral Cladocora caespitosa. Mar Biol 90:363–369

    Article  Google Scholar 

  • Hirota H, Tomono Y, Fusetani N (1996) Terpenoids with antifouling activity against barnacle larvae from the marine sponge Acanthella cavernosa. Tetrahedron 52(2359):2368

    Google Scholar 

  • Ivanisevic J, Thomas OP, Pedel L, Pénez N, Ereskovsky AV et al (2011) Biochemical trade-offs: evidence for ecologically linked secondary metabolism of the sponge Oscarella balibaloi. PLoS ONE 6:e28059

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kersting DK, Linares C (2012) Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar Ecol 33:427–436

    Article  Google Scholar 

  • Kersting DK, Bensoussan N, Linares C (2013a) Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS ONE 8:e70820

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kersting DK, Casado C, López-Legentil S, Linares C (2013b) Unexpected divergent patterns in the sexual reproduction of the Mediterranean scleractinian coral Cladocora caespitosa. Mar Ecol Prog Ser. doi:10.3354/meps10356

    Google Scholar 

  • Klein J, Verlaque M (2008) The Caulerpa racemosa invasion: a critical review. Mar Pollut Bull 56:205–225

    Article  CAS  PubMed  Google Scholar 

  • Kružić P, Benković L (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea (Croatia). Mar Ecol 29:125–139

    Article  Google Scholar 

  • Kružić P, Zuljević A, Nikolić V (2008) The highly invasive alga Caulerpa racemosa var. cylindracea poses a new threat to the banks of the coral Cladocora caespitosa in the Adriatic Sea. Coral Reefs 27:441

    Article  Google Scholar 

  • Linares C, Coma R, Diaz D, Zabala M, Hereu B, Dantart L (2005) Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Mar Ecol Prog Ser 305:127–137

    Google Scholar 

  • Linares C, Cebrian E, Coma R (2012) Effects of turf algae on recruitment and juvenile survival of gorgonian corals. Mar Ecol Prog Ser 452:81–88

    Article  Google Scholar 

  • Martí R, Fontana A, Uriz MJ, Cimino G (2003) Quantitative assessment of natural toxicity in sponges: toxicity bioassay versus compound quantification. J Chem Ecol 29:1307–1318

    Article  PubMed  Google Scholar 

  • McCook LJ (2001) Competition between coral and algal turfs along a gradient of terrestrial influence in the nearshore central Great Barrier Reef. Coral Reefs 19:419–425

    Article  Google Scholar 

  • McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417

    Article  Google Scholar 

  • Molnar JL, Gamboa R, Revenga C, Spalding M (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492

    Article  Google Scholar 

  • Morri C, Peirano A, Bianchi CN, Sassarini M (1994) Present day bioconstructions of the hard coral, Cladocora caespitosa (L.) (Anthozoa, Scleractinia), in the Eastern Ligurian Sea (NW Mediterranean). Biol Mar Med 1:371–373

    Google Scholar 

  • Morri C, Peirano A, Bianchi CN (2001) Is the Mediterranean coral Cladocora caespitosa an indicator of climate change? Arch Oceanogr Limnol 22:139–144

    Google Scholar 

  • Nizamuddin M (1991) The green marine algae of Libya. Elga Publisher, Bern

    Google Scholar 

  • Patzner R (1998) The invasion of Lophocladia (Rhodomelaceae, Lophotaliae) at the northern coast of Ibiza (Western Mediterranean Sea). Boll Soc Hist Nat Balears 41:75–80

    Google Scholar 

  • Peirano A, Morri C, Mastronuzzi G, Bianchi CN (1998) The coral Cladocora caespitosa (Anthozoa, Scleractinia) as a bioherm builder in the Mediterranean Sea. Mem Descr Carta Geol d’Italia 52:59–74

    Google Scholar 

  • Pérez-Estrada CJ, Rodríguez-Estrella R, Palacios-Salgado DS, Paz-García DA (2013) Initial spread of the invasive green alga Caulerpa verticillata over coral communities in the Gulf of California. Coral Reefs 32:865

    Article  Google Scholar 

  • Piazzi L, Ceccherelli G, Cinelli F (2001) Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar Ecol Prog Ser 210:149–159

    Article  Google Scholar 

  • Piazzi L, Meinesz A, Verlaque M, Akçali B, Antolic B, Argyrou M, Balata D, Ballesteros E, Calvo S, Cinelli F, Cirik S, Cossu A, D’Archin R, Djellouli SA, Javel F, Lanfranco E, Mifsud C, Pala D, Panayotidis P, Peirano A, Pergent G, Petrocelli A, Ruitton S, Žuljević A, Ceccherelli G (2005) Invasion of Caulerpa racemosa (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptog Algol 26:189–202

    Google Scholar 

  • Piazzi L, Balata D, Foresi L, Cristaudo C, Cinelli F (2007) Sediment as a constituent of Mediterranean benthic communities dominated by Caulerpa racemosa var. cylindracea. Sci Mar 71:129–135

  • Quan-Young LI, Espinoza-Avalos J (2006) Reduction of zooxanthellae density, chlorophyll a concentration, and tissue thickness of the coral Montastraea faveolata (Scleractinia) when competing with mixed turf algae. Limnol Oceanogr 51:1159–1166

    Article  Google Scholar 

  • Rodolfo-Metalpa R, Peirano A, Morri C, Bianchi CN (1999) Coral calcification rates in the Mediterranean Scleractinian coral Cladocora caespitosa. Atti Assoc Ital Oceanol Limnol 13:291–299

    Google Scholar 

  • Rodolfo-Metalpa R, Martin S, Ferrier-Pagès C, Gattuso JP (2009) Response of the temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences 7:289–300

    Article  Google Scholar 

  • Ruitton S, Javel F, Culioli JM, Meinesz A, Pergent G, Verlaque M (2005) First assessment of the Caulerpa racemosa (Caulerpales, Chlorophyta) invasion along the French Mediterranean coast. Mar Pollut Bull 50:1061–1068

    Article  CAS  PubMed  Google Scholar 

  • Sala E, Ballesteros E (1997) Partitioning of space and food resources by three fishes of the genus Diplodus (Sparidae) in a Mediterranean rocky infralittoral ecosystem. Mar Ecol Progr Ser 152:273–283

    Article  Google Scholar 

  • Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae- a growing concern. Proceedings of the International Seaweed Symposium. J Appl Phycol 18:529–541

    Article  Google Scholar 

  • Smith JE, Hunter CL, Smith CM (2002) Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian Islands. Pac Sci 56:299–315

    Article  Google Scholar 

  • Stimson J, Larned ST, Conklin E (2001) Effects of herbivory, nutrient levels, and introduced algae on the distribution and abundance of the invasive macroalga Dictyosphaeria cavernosa in Kaneohe Bay, Hawaii. Coral Reefs 19:343–357

    Article  Google Scholar 

  • Thomsen MS, Wernberg T, Tuya F, Silliman B (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–819

    Article  Google Scholar 

  • Tomas F, Cebrian E, Ballesteros E (2011) Differential herbivory of invasive algae by native fish in the Mediterranean Sea. Estuar Coast Shelf Sci 92:27–34

    Google Scholar 

  • Verlaque M (1994) Inventaire des plantes introduites en Méditerranée: origines et répercussions sur l’environnement et les activités humaines. Oceanol Acta 17:1–23

    Google Scholar 

  • Verlaque M, Durand C, Huisman JM, Boudouresque CF, Le Parco Y (2003) On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Eur J Phycol 38:325–339

    Article  Google Scholar 

  • Vermeij MJA, van Moorselaar I, Engelhard S, Hönlein C, Vonk SM, Visser PM (2010) The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS ONE 5:e14312

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ 19:291–299

    Article  Google Scholar 

  • Weitzmann B, García M, Cebrian E, Ballesteros E (2009) Les invasions biològiques en el medi marí: exemples i impactes a la Mediterrània Occidental. L’Atzavara 18:39–49

    Google Scholar 

  • Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359

    Article  Google Scholar 

  • Wright JT, Gribben PE (2008) Predicting the impact of an invasive seaweed on the fitness of native fauna. J Appl Ecol 45:1540–1549

    Article  Google Scholar 

  • Zenetos A, Gofas S, Verlaque M, Cinar ME, Raso JEG, Bianchi CN, Morri C, Azzurro E, Bilecenoglu M, Froglia C, Siokou I, Violanti D, Sfriso A, San Martin G, Giangrande A, Katagan T, Ballesteros E, Ramos-Espla A, Mastrototaro F, Ocana O, Zingone A, Gambi MC, Streftaris N (2010) Alien species in the Mediterranean sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Medit Mar Sci 11:381–493

    Google Scholar 

  • Zenetos A, Gofas S, Morri C, Rosso A, Violanti D, García Raso JE, Çinar ME, Almogi-Labin A, Ates AS, Azzurro E, Ballesteros E, Bianchi CN, Bilecenoglu M, Gambi MC, Giangrande A, Gravili C, Hyams-Kaphzan O, Karachle V, Katsanevakis S, Lipej L, Mastrototaro F, Mineur F, Pancucci-Papadopoulou MA, Ramos-Espla A, Salas C, San Martín G, Sfriso A, Streftaris N, Verlaque M (2012) Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends and pathways. Medit Mar Sci 13:328–352

    Article  Google Scholar 

  • Žuljević A, Thibaut T, Despalatović M, Cottalorda JM, Nikolić V, Cvitković I, Antolić B (2011) Invasive alga Caulerpa racemosa var cylindracea makes a strong impact on the Mediterranean sponge Sarcotragus spinosulus. Biol Invasion 13:2303–2308

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge M. Zabala for continuous encouragement during this study and E. Aspillaga, E. Cebrian, S. Jiménez, L. Mangialajo and F. Tomas for their assistance in the field. We thank the Secretaría General de Pesca (MAGRAMA) and the Columbretes Islands Marine Reserve staff for their logistic support. The study has been partially funded by the Spanish Ministry of Economy and Innovation through the Biorock project (CTM2009–08045), the SMART project (CGL2012-32194), a Ramón y Cajal contract to CL (RyC-2011-08134) and a Juan de la Cierva Postdoctoral Fellowship to SC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Diego K. Kersting.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kersting, D.K., Ballesteros, E., De Caralt, S. et al. Invasive macrophytes in a marine reserve (Columbretes Islands, NW Mediterranean): spread dynamics and interactions with the endemic scleractinian coral Cladocora caespitosa . Biol Invasions 16, 1599–1610 (2014). https://doi.org/10.1007/s10530-013-0594-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0594-9

Keywords

Navigation