Biological Invasions

, Volume 16, Issue 8, pp 1599–1610 | Cite as

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

  • Diego K. Kersting
  • Enric Ballesteros
  • Sònia De Caralt
  • Cristina Linares
Original Paper


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.


Invasive species L. lallemandii C. racemosa Coral C. caespitosa Mediterranean Sea Bioactivity 



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.


  1. 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 53Google Scholar
  2. 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 414:91–105CrossRefGoogle Scholar
  3. 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 30:337–345CrossRefGoogle Scholar
  4. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195Google Scholar
  5. Ballesteros E, Cebrian E, Alcoverro T (2007) Mortality of shoots of Posidonia oceanica following meadow invasion by the red alga Lophocladia lallemandii. Bot Mar 50:8–13Google Scholar
  6. 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 168:187–196CrossRefGoogle Scholar
  7. Bedini R, Bonechi L, Piazzi L (2012) Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptog algol 32:383–391CrossRefGoogle Scholar
  8. Botsford JL (2002) A comparison of ecological tests. ATLA 30:539–550PubMedGoogle Scholar
  9. Boudouresque CF, Verlaque M (2002a) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44:32–38PubMedCrossRefGoogle Scholar
  10. 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 53–61Google Scholar
  11. 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 74:101–110Google Scholar
  12. 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 34–41Google Scholar
  13. 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 83:469–474CrossRefGoogle Scholar
  14. 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 92:81–85CrossRefGoogle Scholar
  15. Cebrian E, Ballesteros E, Linares C, Tomas F (2011) Do native herbivores provide resistance to Mediterranean marine bioinvasions? A seaweed example. Biol Invasions 13:1397–1408Google Scholar
  16. Cebrian E, Linares C, Marschal C, Garrabou J (2012) Exploring the effects of invasive algae on the persistence of gorgonian populations. Biol Invasion 14:2647–2656CrossRefGoogle Scholar
  17. 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 11:489–503PubMedCentralPubMedCrossRefGoogle Scholar
  18. 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 115:169–178CrossRefGoogle Scholar
  19. 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 12:41–52CrossRefGoogle Scholar
  20. 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 63:2845–2849CrossRefGoogle Scholar
  21. Herndl GJ, Velimirov B (1986) Microheterotrophic utilization of mucus released by the Mediterranean coral Cladocora caespitosa. Mar Biol 90:363–369CrossRefGoogle Scholar
  22. Hirota H, Tomono Y, Fusetani N (1996) Terpenoids with antifouling activity against barnacle larvae from the marine sponge Acanthella cavernosa. Tetrahedron 52(2359):2368Google Scholar
  23. 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:e28059PubMedCentralPubMedCrossRefGoogle Scholar
  24. Kersting DK, Linares C (2012) Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain, NW Mediterranean): distribution, size structure and growth. Mar Ecol 33:427–436CrossRefGoogle Scholar
  25. Kersting DK, Bensoussan N, Linares C (2013a) Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS ONE 8:e70820PubMedCentralPubMedCrossRefGoogle Scholar
  26. 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
  27. Klein J, Verlaque M (2008) The Caulerpa racemosa invasion: a critical review. Mar Pollut Bull 56:205–225PubMedCrossRefGoogle Scholar
  28. Kružić P, Benković L (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea (Croatia). Mar Ecol 29:125–139CrossRefGoogle Scholar
  29. 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 27:441CrossRefGoogle Scholar
  30. 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 305:127–137Google Scholar
  31. Linares C, Cebrian E, Coma R (2012) Effects of turf algae on recruitment and juvenile survival of gorgonian corals. Mar Ecol Prog Ser 452:81–88CrossRefGoogle Scholar
  32. Martí R, Fontana A, Uriz MJ, Cimino G (2003) Quantitative assessment of natural toxicity in sponges: toxicity bioassay versus compound quantification. J Chem Ecol 29:1307–1318PubMedCrossRefGoogle Scholar
  33. McCook LJ (2001) Competition between coral and algal turfs along a gradient of terrestrial influence in the nearshore central Great Barrier Reef. Coral Reefs 19:419–425CrossRefGoogle Scholar
  34. McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417CrossRefGoogle Scholar
  35. Molnar JL, Gamboa R, Revenga C, Spalding M (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492CrossRefGoogle Scholar
  36. 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 1:371–373Google Scholar
  37. Morri C, Peirano A, Bianchi CN (2001) Is the Mediterranean coral Cladocora caespitosa an indicator of climate change? Arch Oceanogr Limnol 22:139–144Google Scholar
  38. Nizamuddin M (1991) The green marine algae of Libya. Elga Publisher, BernGoogle Scholar
  39. Patzner R (1998) The invasion of Lophocladia (Rhodomelaceae, Lophotaliae) at the northern coast of Ibiza (Western Mediterranean Sea). Boll Soc Hist Nat Balears 41:75–80Google Scholar
  40. 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 52:59–74Google Scholar
  41. 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 32:865CrossRefGoogle Scholar
  42. 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 210:149–159CrossRefGoogle Scholar
  43. 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 26:189–202Google Scholar
  44. 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 71:129–135Google Scholar
  45. 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 51:1159–1166CrossRefGoogle Scholar
  46. 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 13:291–299Google Scholar
  47. 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 7:289–300CrossRefGoogle Scholar
  48. 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 50:1061–1068PubMedCrossRefGoogle Scholar
  49. 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 152:273–283CrossRefGoogle Scholar
  50. Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae- a growing concern. Proceedings of the International Seaweed Symposium. J Appl Phycol 18:529–541CrossRefGoogle Scholar
  51. Smith JE, Hunter CL, Smith CM (2002) Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian Islands. Pac Sci 56:299–315CrossRefGoogle Scholar
  52. 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 19:343–357CrossRefGoogle Scholar
  53. Thomsen MS, Wernberg T, Tuya F, Silliman B (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–819CrossRefGoogle Scholar
  54. Tomas F, Cebrian E, Ballesteros E (2011) Differential herbivory of invasive algae by native fish in the Mediterranean Sea. Estuar Coast Shelf Sci 92:27–34Google Scholar
  55. Verlaque M (1994) Inventaire des plantes introduites en Méditerranée: origines et répercussions sur l’environnement et les activités humaines. Oceanol Acta 17:1–23Google Scholar
  56. 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 38:325–339CrossRefGoogle Scholar
  57. 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:e14312PubMedCentralPubMedCrossRefGoogle Scholar
  58. 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 19:291–299CrossRefGoogle Scholar
  59. 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 18:39–49Google Scholar
  60. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359CrossRefGoogle Scholar
  61. Wright JT, Gribben PE (2008) Predicting the impact of an invasive seaweed on the fitness of native fauna. J Appl Ecol 45:1540–1549CrossRefGoogle Scholar
  62. 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 11:381–493Google Scholar
  63. 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 13:328–352CrossRefGoogle Scholar
  64. 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 13:2303–2308CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Diego K. Kersting
    • 1
  • Enric Ballesteros
    • 2
  • Sònia De Caralt
    • 2
  • Cristina Linares
    • 1
  1. 1.Departament d’EcologiaUniversitat de Barcelona (UB)BarcelonaSpain
  2. 2.Centre d’Estudis Avançats de Blanes (CSIC)BlanesSpain

Personalised recommendations