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Blitzkrieg in a Marine Invasion: Caulerpa racemosa var. cylindracea (Bryopsidales, Chlorophyta) Reaches the Canary Islands (North-East Atlantic)

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Abstract

On the basis of morphological and genetic studies (rDNA ITS1, 5.8S, ITS2, and a 18S rDNA intron), we confirm here that Caulerpa racemosa var. cylindracea (Sonder) Verlaque, Huisman et Boudouresque, a southwestern Australian taxon recently introduced into the Mediterranean Sea also occurs in the Canary Islands. This is the first report of C. racemosa var. cylindracea in the Atlantic. It was observed for the first time in the Canary Archipelago in 1997–1998. The speed and regional scale of expansion (north Atlantic Ocean and the Mediterranean Sea) of this invasive species appear to be among the most dramatic ever recorded. The possible outcome of this introduction in the Atlantic is discussed.

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References

  • Afonso-Carrillo J and Gil-Rodr'ýguez MC (1980) Datos para la flora marina de la Isla de Fuerteventura. Vieraea 10(1-2): 147–170

    Google Scholar 

  • Afonso-Carrillo J and Gil-Rodr'ýguez MC (1982) Aspectos bio-geogr' aficos de la flora ficol' ogica marina de las Islas Canarias. Actas II Simposio Ibèrico de Estudios Bentos Marino 3: 41–48 Anonymous (1980) Activitè de l'Institut des Pêches en 1979. Principales actions en matière de cultures marines. Science et Pêche, Bulletin de l'Institut des Pêches Maritimes 306: 1–39

    Google Scholar 

  • Athanasiadis A (1997) North Aegean marine algae. IV. Womersleyella setacea (Hollenberg) R.E. Norris (Rhodophyta Ceramiales). Botanica Marina 40: 473–476

    Google Scholar 

  • Børgesen F (1925) Marine algae from the Canary Islands, especially from Teneriffe and Gran Canaria. I. Chlorophyceae. Kongelige Danske Videnskabernes Selskab, Biologiske Meddelelser 5(3): 1–123

    Google Scholar 

  • Boudouresque CF and Verlaque M (2002a) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 44: 32–38

    Google Scholar 

  • Boudouresque CF and 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, pp 53–61. Monaco

  • Boudouresque CF, Gerbal M and Knoepffler-Pèguy M (1985) —L'algue japonaise Undaria pinnatifida (Phaeophyceae, Laminariales) en Mèditerranèe. Phycologia 24: 364–366

    Google Scholar 

  • Cantasano N (2001) Prima segnalazione di Caulerpa racemosa (Forsskål) J. Agardh sulla costa tirrennica calabrese. Informatore Botanico Italiano 33: 327–329

    Google Scholar 

  • Cecere E, Petrocelli A and Saracino OD (2000) Benthic algal flora of the Gulf of Taranto (Italy, Ionian Sea). In: PNUE (ed) First Mediterranean Symposium on Marine Vegetation, Ajaccio, 3–4 October 2000, pp 119–123. RAC/SPA Publisher, Tunisia

    Google Scholar 

  • Cinelli F and Sartoni G (1969) Acrothamnion J. Ag. (Rhodophyta, Ceramiaceae): genere algale nuovo per il mare Mediterraneo. Pubblicazione della Stazione Zoologica di Napoli 37: 567–574

    Google Scholar 

  • Cinelli F, Salguetti-Drioli U and Serena F (1984) Nota sull'areale di Acrothamnion preissii (Sonder) Wollaston nell'Alto Tirreno. Quaderni del Museo di Storia Naturale di Livorno 5: 57–60

    Google Scholar 

  • Coppejans E (1982) Zeewierengids voor de Belgische en Noordfranse Kust. Deel II. Beschrijvingen Groen-en Bruinwieren. Wetenschappelijk Tijdschrift van de Belgische Jeugdbond voor Natuurstudie v.z.w. 17 (extra nummer): 157–254

    Google Scholar 

  • Costantino G, Quaranta L, De Zio V, Pastorelli AM, Rositani L and Ungaro N (2001) Sulla recente presenza di Caulerpa racemosa (Forsskål) J. Agardh sui fondi costieri dell'Adriatico sud-occidentale. ATTI XXXII e Congresso Societ' a Italiana di Biologia Marina, abstract: 107

  • Critchley AT, Farnham WF and Morrell SL (1983) A chronology of new European sites of attachment for the invasive brown alga Sargassum muticum, 1973–1981. Journal of Marine Biological Association, United Kingdom 63: 799–811

    Google Scholar 

  • Dappiano M, Iacono B and Gambi MC(2001) Ruolo della metodologia di census visuale nella valutazione della biodiversit' a del benthos: un esempio nelle isole Flegree (Golfo di Napoli). ATTI XXXII e Congresso Societ' a Italiana di Biologia Marina, abstract: 93

  • Di Martino V and Giaccone G (1995) La dispersione in Mediterraneo di alghe tropicali del genere Caulerpa. Bolletin Accademia Gioenia Scienza Naturale, Catania 28(349): 693–705

    Google Scholar 

  • Djellouli A (2000) Caulerpa racemosa (Forsskål) J. Agardh en Tunisie. In: PNUE (ed) First Mediterranean Symposium on Marine Vegetation, Ajaccio, 3–4 October 2000, pp 124–127. RAC/SPA Publisher, Tunisia

    Google Scholar 

  • Djellouli A, Verlaque M and Rais C (2000) Macroflore benthique de la lagune de Bizerte. In: PNUE (ed) First Mediterranean Symposium on Marine Vegetation, Ajaccio, 3–4 October 2000, pp 128–131. RAC/SPA Publisher, Tunisia

    Google Scholar 

  • Durand C, Manuel M, Boudouresque CF, Meinesz A, Verlaque M and Le Parco Y (2002) Molecular data suggest a hybrid origin for the invasive Caulerpa racemosa (Caulerpales, Chlorophyta) in the Mediterranean Sea. Journal of Evolutionary Biology 15: 122–133

    Google Scholar 

  • Fam' a P, Olsen J, Wytzet S and Procaccini G (2000) High levels of intra-and inter-individual polymorphism in the rDNA ITS1 of Caulerpa racemosa (Chlorophyta). European Journal of Phycology 35: 349–356

    Google Scholar 

  • Farnham WF and Irvine LM (1973) The addition of a foliose species of Grateloupia to the British marine flora. British Phycological Journal 8: 208–209

    Google Scholar 

  • Feldmann J and Feldmann G(1942) Recherches sur les Bonnemaiso-niacèes et leur alternance de gènèrations. Annales des sciences naturelles. Botanique, 111/4ñêôŒ'Sèrie 3: 75–175

    Google Scholar 

  • Felsenstein J (1992) Phylip Manual. University of Washington, Seattle

    Google Scholar 

  • Floc'h JY, Pajot R and Mouret V (1996) Undaria pinnatifida (Laminariales, Phaeophyta) 12 years after its introduction into the Atlantic Ocean. Hydrobiologia 326/327: 217–222

  • Gambi MC, Dappiano M, Iannotta A, Esposito A, Zupo V and Buia MC (2001) Aspetti storici ed attuali della biodiversit' a del benthos mediterraneo: un esempio in alcune aree del Golfo di Napoli. ATTI XXXII e Congresso Societ' a Italiana di Biologia Marina, abstract: 51

  • Gavio B and Fredericq S (2002) Grateloupia turuturu (Halymeniaceae, Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora. European Journal of Phycology 37: 349–359

    Google Scholar 

  • Gil-Rodr'ýguez MC and Afonso-Carrillo J (1980) Cat' alogo de las algas marinas bent' onicas (Cyanophyta, Chlorophyta, Phaeophytay Rhodophyta) para el Archipièlago Canario. Aula de Cultura de Tenerife, 47 pp

  • Gil-Rodr'ýguez MC and Wildpret de la Torre W(1978) —Contribuci' on a la ficolog'ýa de la Isla del Hierro. Vieraea 8(2): 245–260 (published in 1980)

    Google Scholar 

  • Gil-Rodr'ýguez MC, del Arco Aguilar M, Wildpret de la Torre W, Hern' andez-Gonz' alez CL and Haroun R (2002) Halophiletum decipientis Wildpret & MC Gil in Canary Islands. An ecological and chorological study. Abstracts IV Symposium on Fauna and Flora of the Atlantic Islands. Praia, Cabo Verde, p 59

  • Gonz' alez Henr'ýquez N and Santos Guerra A (1983) —El gènero Caulerpa Lamouroux en las islas Canarias. Botanica Macaronèsica 11: 3–24.

    Google Scholar 

  • Haroun Tabraue RJ, Gil-Rodr'ýguez MC, Afonso-Carrillo J and Wildpret de la Torre W (1984) Estudio ecologico y fenologico de algunas especies del genero Caulerpa Lamouroux presentes en el archipielago Canario. In: Monteiro Marques V(ed) Actas IV Simposio Ibèrico de Estudios Benthos Marinho, Vol 3, pp 75–82. Faculdade de Ciencias de Lisboa

  • Haroun RJ, Gil-Rodr'ýguez MC, D'ýaz de Castro J and Prud'homme van Reine WF (2002) A checklist of the marine plants from the Canary Islands (Central Eastern Atlantic Ocean). Botanica Marina 45: 139–169

    Google Scholar 

  • Jousson O, Pawlowski J, Zaninetti L, Zechman FW, Dini F, Di Giuseppe G, Woodfield R, Millar A and Meinesz A (2000) Invasive alga reaches California. Nature 408: 157–158

    Google Scholar 

  • Kimura M(1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120

    Google Scholar 

  • Kooistra WHCF (2002) Molecular phylogenies of Udoteaceae (Bryopsidales, Chlorophyta) reveal nonmonophyly for Udotea, Penicillus and Chlorodesmis. Phycologia 41: 453–462

    Google Scholar 

  • Lorenzo Nespereira JM and Brito Hern' andez A (1997) Fauna marina de Canarias y subiodiversidad. In: Pèrez de Paz (ed) Ecosistemas Insulares Canarios. Usos y Aprovechamientos en el Territorio, pp 169–175. M'aster en Gesti' on Ambiental, Santa Cruz de Tenerife

  • Maggs CA and Stegenga H (1999) Red algal exotics on North Sea coasts. Helgol¨ ander Meeresuntersuchungen 52: 243–258

    Google Scholar 

  • Marino G, Blundo MC and Giaccone G (2001) Capo Murro di Porco (SR) come osservatorio per l'evoluzione della biodiver-sit' a bentonica del Mediterraneo: un ulteriore motivo di tutela. ATTI XXXII e Congresso Societ' a Italiana di Biologia Marina, abstract: 95

  • Mascareño D (1972) —Algunas consideraciones oceanogr' aficas de las aguas del Archipièlago Canario. Bolet'ýn del Instituto Español de Oceanograf'ýa 158: 1–79

    Google Scholar 

  • Meinesz A and Hesse B (1991) —Introduction et invasion de l'algue tropicale Caulerpa taxifolia en Mèditerranèe nord-occidentale. Oceanologica Acta 14: 415–426

    Google Scholar 

  • Meinesz A, Belsher T, Thibaut T, Antolic B, Ben Mustapha K, Boudouresque CF, Chiaverini D, Cinelli F, Cottalorda JM, Djellouli A, El Abed A, Orestano C, Grau AM, Ivesa M, 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 the Mediterranean. Biological Invasions 3: 201–210

    Google Scholar 

  • Mifsud C (2000) Malta country report: marine vegetation. In: PNUE (ed) First Mediterranean Symposium on Marine Vegetation, Ajaccio, 3–4 October 2000, pp 159–161. RAC/SPA Publisher, Tunisia

    Google Scholar 

  • Montagne C (1839–1841) Plantae cellulares. In: Barker-Webb P and Berthelot S (eds) Histoire Naturelle des Iles Canaries. Phytographia Canariensis, Vol 3, part 2, sect. 4, Paris, XV +208 pp, 9 pls

  • Nizamuddin M(1991) The Green Marine Algae of Libya. Elga Publ., Bern, 227 pp

  • Okudan ES, Yurdabak F, Tuncer S, Erdemir CC and Aysel V (2002) The distribution of Caulerpa racemosa (Forsskål) J. Agardh on the coast of Turkey. In: ¨ Ozt¨ urk B and Ba+usta N (eds) Proceedings of the Workshop on Lessepsian Migration, Turkish Marine Research Foundation Publication 9, pp 46–49. Istanbul

  • Olsen JL, Valero M, Meusnier I, Boele-Bos S and Stam WT (1998) Mediterranean Caulerpa taxifolia and C. mexicana (Chlorophyta) are not conspecific. Journal of Phycology 34: 850–856

    Google Scholar 

  • Pèrez R, Lee JY and Juge C (1981) Observations sur la biologie de l'algue japonaise Undaria pinnatifida (Harvey) Suringar introduite accidentellement dans l'Etang de Thau. Science et Pêche, France 315: 1–12

    Google Scholar 

  • Piccone A (1884) Crociera del Corsaro alle Isole Madera e Canarie del Capitano Enrico D'Albertis. Alghe. Genova, 60 pp, 1 pl

  • Renoncourt L and Meinesz A (2002) Formation of propagules on invasive strain of Caulerpa racemosa (Chlorophyta) in the Mediterranean Sea. Phycologia 41: 533–535

    Google Scholar 

  • Reyes JM, Sans'on M and Afonso-Carrillo J (1995) Distribution and reproductive phenology of the seagrass Cymodocea nodosa (Ucria) Ascherson in the Canary Islands. Aquatic Botany 50: 171–180

    Google Scholar 

  • Ribera MA and Boudouresque CF (1995) Introduced marine plants, with special reference to macroalgae: mechanisms and impact. In: Round FE and Chapman DJ (eds) Progress in Phycological Research 11, pp 187–268. Biopress Ltd Publ., UK

  • Ribera-Siguan MA(2002) Review of non-native marine plants in the Mediterranean Sea. In: Lapp¨akoski E, Gollasch S and Olenin S (eds) Invasive Aquatic Species of Europe. Distribution, Impacts and Management, pp 291–310. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Rivas-Mart'ýnez S, D'ýaz T, Fern'andez-Gonz'alez F, Izco J, Loidi J, Lousã Mand Penas A(2002) Vascular plant communities of Spain and Portugal. Addenda to the syntaxonomical checklist of 2001. Itinera Geobotanica 15: 115–116

    Google Scholar 

  • Rojas-Gonz' alez B and Afonso-Carrillo J (2000) Notes on Rhodomelaceae (Rhodophyta) from the Canary Islands: observations on reproductive morphology and new records. Botanica Marina 43: 147–155

    Google Scholar 

  • Saitou N and Nei M (1987) The neighbor-joining method: a new method of reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425

    Google Scholar 

  • Sanger F, Nicklen S and Coulson AR (1977) DNA sequencing with chain terminating inhibitor. Proceedings of National Academy of Sciences 74: 5463–5467

    Google Scholar 

  • Sans'on Mand Reyes J (1995) Morphological and geographical observations on four species of Ceramiaceae (Rhodophyta) new to the Canary Islands. Botanica Marina 38: 89–95

    Google Scholar 

  • Sartoni G and Rossi S (1998) New records for the benthic algal flora of the Northern Adriatic Sea. Flora Mediterranea 8: 9–15

    Google Scholar 

  • Sauvageau C (1925) Sur la naturalisation en France d'une floridèe australasienne (Asparagopsis armata Harv.) et sur ses ioduques. Comptes Rendus hebdomadaires de l'Acadèmie des Sciences, Paris 180

  • Silva PC (1955) The dichotomous species of Codium in Britain. Journal of the Marine Biological Association of the United Kingdom 34: 565–577 +1 pl

    Google Scholar 

  • Sonder G (1845) Nova algarum genera et species, quas in itinere ad oras occidentales Novae Hollandiae, collegit L. Priess, h. Dr. Botanische Zeitung 3: 49–57

    Google Scholar 

  • Th'elin I (1984) Nouvelle signalisation d'Acrothamnion preissii (Sonder) Wollaston sur les côtes franc¸aises de la Mèditerran'ee. Travaux Scientifiques du Parc National de Port-Cros, France 10: 171–172.

    Google Scholar 

  • Thompson JD, Higgins DG and Gibson TJ (1994) Clustal W/ improvind sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680

    Google Scholar 

  • Tolay M, Evirgen A and Cirik S (2001a) Observations of Caulerpa racemosa in the Eagean Sea and the Mediterranean Sea of Turkish region. In: Gravez V, Ruitton S, Boudouresque CF, Le Direach L, Meinesz A, Scabbia G and Verlaque M (eds) 4th International Workshop on Caulerpa taxifolia, Lerici, 1–2 February 1999, pp 328–333. GIS Posidonie Publisher, France

    Google Scholar 

  • Tolay MA, Evirgen A, Piazzi L and Cirik S (2001b) Determination of variations in Caulerpa racemosa in the Bodrum-G¨ okova coast of Turkey. XVIIth International Seaweed Symposium, Cape Town, South Africa, abstract: 93

  • Van Goor ACJ (1923) Die holl¨ andischen Meeresalgen (Rhodophyceae, Phaeophyceae und Chlorophyceae) ins-besondere der Umgebung von Helder, des Wattenmeeres und der Zuidersee. Verhandelingen Koninklijke Akademie van Wetenschappen Amsterdam, Section 2, 23(2): 1–232

    Google Scholar 

  • Verlaque M (1989) Contribution'a la flore des algues marines de M'editerran'ee: espèces rares ou nouvelles pour les côtes franc¸aises. Botanica Marina 32: 101–113

    Google Scholar 

  • Verlaque M (1994) Inventaire des plantes introduites en M'editerran'ee: origine et r'epercussions sur l'environnement et les activitès humaines. Oceanologica Acta 17: 1–23

    Google Scholar 

  • Verlaque M (2001) Checklist of the macroalgae of Thau Lagoon (Hèrault, France), a hot spot of marine species introduction in Europe. Oceanologica Acta 24: 29–49

    Google Scholar 

  • Verlaque M and Boudouresque CF (1991) Stypopodium schimperi (Buchinger ex K¨ utzing) Verlaque et Boudouresque comb. nov. (Dictyotales, Fucophyceae), algue de Mer Rouge rècemment apparue en Mèditerranèe. Cryptogamie, Algologie 12: 195–211

    Google Scholar 

  • Verlaque M, Boudouresque CF, Meinesz A and Gravez V(2000) The Caulerpa racemosa complex (Caulerpales, Ulvophyceae) in the Mediterranean Sea. Botanica Marina 43: 49–68

    Google Scholar 

  • Verlaque M, Durand C, Huisman JM, Boudouresque CF and Le Parco Y (2003) On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Cauler-pales, Chlorophyta). European Journal of Phycology 38: 325–339

    Google Scholar 

  • Vickers A (1896) Contribution ' a la flore algologique des Canaries. Annales des Sciences Naturelles, S'erie 8, Botanique 4: 293–306

    Google Scholar 

  • Wallentinus I (2002) Introduced marine algae and vascular plants in European aquatic environments. In: Lapp¨ akoski E, Gollasch S and Olenin S (eds) Invasive Aquatic Species of Europe. Distribution, Impacts and Management, pp 27–52. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Weber-van Bosse A (1898) Monographie des Caulerpes. Annales du Jardin Botanique de Buitenzorg 15: 243–401, pls XX–XXXIV

    Google Scholar 

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Verlaque, M., Afonso-Carrillo, J., Candelaria Gil-Rodríguez, M. et al. Blitzkrieg in a Marine Invasion: Caulerpa racemosa var. cylindracea (Bryopsidales, Chlorophyta) Reaches the Canary Islands (North-East Atlantic). Biological Invasions 6, 269–281 (2004). https://doi.org/10.1023/B:BINV.0000034589.18347.d3

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