Abstract
Many invasive species show temporal variations in abundances, such as seasonal cycles and medium to long term variations. The effects of invasive species on native assemblages have, however, mainly been investigated during the maximum abundance of the invasive species and rarely over an entire year. At the north-western limit of its distribution range in the Mediterranean Sea, the invasive marine macrophyte Caulerpa racemosa var. cylindracea shows high temporal variability in its development pattern with complete withdrawal in winter. The present study investigated the variation of the macrophyte assemblage associated with C. racemosa var. cylindracea in the bay of Marseilles (NW Mediterranean, France) over a period of one year. A comparison was made with a non-invaded assemblage at the same site. The results showed a relationship between the development of C. racemosa var. cylindracea and the structure of the macrophyte assemblage. When C. racemosa var. cylindracea was present, the associated assemblage showed significantly lower numbers of species, lower cover of native and introduced macrophytes and lower diversity (Shannon diversity index and Pielou’s evenness) compared to the non-invaded assemblage. During the temporary winter withdrawal of C. racemosa var. cylindracea, an increase in the assemblage descriptors was noted; however, this period was probably not long enough to allow the recovery of a structured macrophyte assemblage comparable to the non-invaded assemblage. Other invasive macrophytes occur in the bay of Marseilles; their cover was, however, greatly reduced in the invaded assemblage, indicating strong competitive interactions between C. racemosa var. cylindracea and the other invasive species.







Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Airoldi, L., F. Rindi & F. Cinelli, 1994. Structure of a subtidal algal assemblage dominated by Polysiphonia setacea Hollenberg in Western Mediterranean. Giornale Botanico Italiano 128: 782–783.
Airoldi, L., F. Rindi & F. Cinelli, 1995. Structure, seasonal dynamics and reproductive phenology of a filamentous turf assemblage on a sediment influenced, rocky subtidal shore. Botanica Marina 38: 227–237.
Arenas, F. & C. Fernandez, 2000. Size structure and dynamics in a population of Sargassum muticum (Phaeophyceae). Journal of Phycology 36: 1012–1020.
Asia, L., S. Mazouz, M. Guiliano, P. Doumenq & G. Mille, 2009. Occurrence and distribution of hydrocarbons in surface sediments from Marseille Bay (France). Marine Pollution Bulletin 58: 443–451.
Balata, D., L. Piazzi & F. Cinelli, 2004. A comparison among assemblages in areas invaded by Caulerpa taxifolia and C. racemosa on a subtidal Mediterranean rocky bottom. Marine Ecology 25: 1–13.
Ballesteros, E., 1986. Métodos de análisis estructural en comunidades naturales, en particular del fitobentos. Oecologia Aquatica 8: 117–131.
Ballesteros, E., 1991. Structure and dynamics of north-western Mediterranean marine communities: a conceptual model. Oecologia Aquatica 10: 223–242.
Ballesteros, E., 1992. Els vegetals i la zonació litoral: espècies, comunitats i factors que influeixen en la seva distribució. Arxius Secció Cienciès, 101. Institut d’Estudis Catalans. Barcelona: 616 p.
Bellan, G. & D. Bellan-Santini, 1972. Influence de la pollution sur les peuplements marins de la région de Marseille. In Ruivo, A. (ed.), Marine Pollution and Sea Life. FAO Publication. Fishing News (Books), Surrey and London, UK: 396–401.
Benedetti-Cecchi, L. & F. Cinelli, 1989. Note on a Polysiphonia sp. (Rhodophyta, Ceramiales) collected at Rosignano Solvay (Western Mediterranean). Giornale Botanico Italiano 123: 49–54.
Boudouresque, C. F., 1971. Méthodes d’étude qualitative et quantitative du benthos (en particulier phytobenthos). Téthys 3: 79–104.
Boudouresque, C. F., 1974. Aire minima et peuplements algaux marins. Bulletin de la Société Phycologique de France 19: 141–157.
Boudouresque, C. F. & T. Belsher, 1979a. Le peuplement algal du port de Port-Vendres: recherches sur l’aire minimale qualitative. Cahier de Biologie Marine 20: 259–269.
Boudouresque, C. F. & T. Belsher, 1979b. Une méthode et determination de l’aire minimale qualitative. Rapport et Procès Verbaux de la Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 25(26): 273–275.
Boudouresque, C. F. & M. Verlaque, 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 44: 32–38.
Buia, M. C., M. C. Gambi, A. Terlizzi & L. Mazzella, 2001. Colonization of Caulerpa racemosa along the southern Italian coasts: I. Distribution, phenological variability and ecological role. In Gravez, V., S. Ruitton, C. F. Boudouresque, L. Le Direach, A. Meinesz, G. Scabbia & M. Verlaque (eds), Fourth International Workshop on Caulerpa taxifolia. GIS Posidonie Publisher, France: 352–360.
Buschbaum, C., A. S. Chapman & B. Saier, 2006. How an introduced seaweed can affect epibiota diversity in different coastal systems. Marine Biology 148: 743–754.
Capiomont, A., E. Breugnot, M. Den Haan & A. Meinesz, 2005. Phenology of a deep-water population of Caulerpa racemosa var cylindracea in the northwestern Mediterranean Sea. Botanica Marina 48: 80–83.
Castric-Fey, A., C. Beaupoil, J. Bouchain, E. Pradier & M. Th. L’Hardy-Halos, 1999. The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the rocky shore ecosystem of the St Malo area: growth rate and longevity of the sporophyte. Botanica Marina 42: 83–96.
Cinelli, F., C. F. Boudouresque, E. Fresi, J. Marcot & L. Mazzella, 1977a. L’aire minima du phytobenthos dans le port de Sant d’Angelo (Ischia, Italie). Rapport et Procès Verbaux de la Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 24: 149–152.
Cinelli, F., E. Fresi, E. Idato & L. Mazzella, 1977b. L’aire minima du phytobenthos dans un peuplement à Cystoseira mediterranea de l’île d’Ischia (Golfe de Naples). Rapport et Procès Verbaux de la Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 24: 113–115.
Cinelli, F., D. Balata & L. Piazzi, 2007. Threats to coralligenous assemblages: sedimentation and biological invasions. In Pergent-Martini, C., S. El Asmi & C. Le Ravallec (eds), Proceedings of the 3rd Mediterranean Symposium on Marine Vegetation (Marseilles, 27–29 March 2007). United Nations Environment Programme, RAC/SPA Publisher, Tunis, Tunisia: 42–47.
Clarke, K. R. & R. H. Green, 1988. Statistical design and analysis for a ‘biological effects’ study. Marine Ecology Progress Series 46: 213–226.
Clarke, K. R. & R. M. Warwick, 2001. Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth.
Coppejans, E., 1980. Phytosociological studies on Mediterranean algal vegetation: rocky surfaces of the photophilic infralittoral zone. In Price, J. H., D. E. G. Irvine & W. F. Farnham (eds), The Shore Environment, Vol. 2: Ecosystems. Academic Press, London, UK and New York, USA: 371–393.
Grime, J. P., 1979. Plant Strategies and Vegetation Processes. John Wiley & Sons, Chichester.
Grime, J. P., 1985. Towards a functional description of vegetation. In White, J. (ed.), The Population Structure of Vegetation. Dr W. Junk, Dordrecht: 501–514.
Guiry, M. D. & G. M. Guiry, 2009. Algaebase. World-Wide Electronic Publication, National University of Ireland, Galway, http://www.algaebase.org; searched on 20 February 2009
Harris, L. G. & M. C. Tyrrell, 2001. Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change. Biological Invasions 3: 9–21.
Hawkes, C. V., I. F. Wren, D. J. Herman & M. K. Firestone, 2005. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecology Letters 8: 976–985.
Hay, C. H. & E. Villouta, 1993. Seasonality of the adventive Asian kelp Undaria pinnatifida in New Zealand. Botanica Marina 36: 461–476.
Hulme, P. E. & E. T. Bremner, 2006. Assessing the impact of Impatiens glandulifera on riparian habitats: partitioning diversity components following species removal. Journal of Applied Ecology 43: 43–50.
Jousson, O., J. Pawlowski, L. Zaninetti, A. Meinesz & C. F. Boudouresque, 1998. Molecular evidence for the aquarium origin of the green alga Caulerpa taxifolia introduced to the Mediterranean Sea. Marine Ecology Progress Series 172: 275–280.
Klein, J. & M. Verlaque, 2008. The Caulerpa racemosa invasion: a critical review. Marine Pollution Bulletin 56: 205–225.
Kourtev, P. S., J. G. Ehrenfeld & M. Häggblom, 2002. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83: 3152–3166.
Meinesz, A., 1979. Contribution à l’étude de Caulerpa prolifera (Forsskål) Lamouroux (Chlorophycée, Caulerpale). I. Morphogénèse et croissance dans une station des côtes continentales françaises de la Méditerranée. Botanica Marina 22: 27–39.
Nizamuddin, M., 1991. The Green Marine Algae of Libya. Elga Publisher, Bern: 227 pp.
Piazzi, L. & G. Ceccherelli, 2006. Persistence of biological invasion effects: recovery of macroalgal assemblages after removal of Caulerpa racemosa var cylindracea. Estuarine, Coastal and Shelf Science 68: 455–461.
Piazzi, L. & F. Cinelli, 1999. Développement et dynamique saisonnière d’un peuplement méditerranéen de l’algue tropicale Caulerpa racemosa (Forsskål) J. Agardh. Cryptogamie Algologie 20: 295–300.
Piazzi, L. & F. Cinelli, 2000. Effets de l’envahissement des Rhodophyceae introduites Acrothamnion preissii et Womersleyella setacea sur les communautés algales des herbiers à Posidonia oceanica de la Méditerranée occidentale. Cryptogamie Algologie 21: 291–300.
Piazzi, L. & F. Cinelli, 2003. Evaluation of benthic macroalgal invasion in a harbour area of the western Mediterranean Sea. European Journal of Phycology 38: 223–231.
Piazzi, L., G. Pardi & F. Cinelli, 1996. Ecological aspects and reproductive phenology of Acrothamnion preissii (Sonder) Wollaston (Ceramiaceae, Rhodophyta) in the Tuscan Archipelago (Western Mediterranean). Cryptogamie Algologie 17: 35–43.
Piazzi, L., G. Ceccherelli & F. Cinelli, 2001a. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Marine Ecology Progress Series 210: 149–159.
Piazzi, L., G. Ceccherelli & F. Cinelli, 2001b. Effet de Caulerpa racemosa sur la structure des communautés algales benthiques. In Gravez, V., S. Ruitton, C. F. Boudouresque, L. Le Direach, A. Meinesz, G. Scabbia & M. Verlaque (eds), Fourth International Workshop on Caulerpa taxifolia. GIS Posidonie Publisher, France: 371–375.
Piazzi, L., A. Meinesz, M. Verlaque, B. Akçali, B. Antolić, M. Argyrou, D. Balata, E. Ballesteros, S. Calvo, F. Cinelli, S. Cirik, A. Cossu, R. D’Archino, A. S. Djellouli, F. Javel, E. Lanfranco, C. Mifsud, D. Pala, P. Panayotidis, A. Peirano, G. Pergent, A. Petrocelli, S. Ruitton, A. Žuljević & G. Ceccherelli, 2005. Invasion of Caulerpa racemosa var cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptogamie Algologie 26: 189–202.
Piazzi, L., D. Balata, L. Foresi, C. Cristaudo & F. Cinelli, 2007. Sediment as a constituent of Mediterranean benthic communities dominated by Caulerpa racemosa var cylindracea. Scientia Marina 71: 129–135.
Plougerné, E., K. Le Lann, S. Connan, G. Jechoux, E. Deslandes & V. Stiger-Pouvreau, 2006. Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aquatic Botany 85: 337–344.
Pradal, M.-A. & B. Millet, 2006. Hétérogénéité spatiale du forçage du vent: fonctionnement des récifs artificiels et circulation des eaux dans la baie sud de Marseille. C.R. Biologies 329: 541–550.
Ruitton, S., M. Verlaque & C. F. Boudouresque, 2005. Seasonal changes of the introduced Caulerpa racemosa var cylindracea (Caulerpales, Chlorophyta) at the northwest limit of its Mediterranean distribution. Aquatic Botany 82: 55–70.
Sala, E. & C. F. Boudouresque, 1997. The role of fishes in the organization of a Mediterranean sublittoral community. I: Algal communities. Journal of Experimental Marine Biology and Ecology 212: 25–44.
Sanchez, I. & C. Fernandez, 2005. Impact of the invasive seaweed Sargassum muticum (Phaeophyta) on an intertidal macroalgal assemblage. Journal of Phycology 41: 923–930.
Sauvageau, C., 1925. Sur quelques algues Floridées renfermant de l’iode à l’état libre. Bulletin de la Station Biologique d’Arcachon 22: 5–45.
Schmidt, A. L. & R. E. Scheibling, 2005. Population dynamics of an invasive green alga, Codium fragile subsp. tomentosoides, in tidepools on a rocky shore in Nova Scotia, Canada. Ecoscience 12: 403–411.
Shannon, C. E. & W. Weaver, 1949. The Mathematical Theory of Communication. University of Illinois Press, Urbana, USA.
Sogreah, L. N. H., 1984. Le catalogue sédimentologique des côtes françaises. Les côtes méditerranéennes. Editions Eyrolles, France.
Verlaque, M., 1994. Checklist of introduced plants in the Mediterranean: origins and impact on the environment and human activities. Oceanologica Acta 17: 1–23.
Verlaque, M. & P. Fritayre, 1994. Mediterranean algal communities are changing in the face of the invasive alga Caulerpa taxifolia (Vahl) C. Agardh. Oceanologica Acta 17: 659–672.
Wallentinus, I., 2002. Introduced marine algae and vascular plants in European aquatic environments. In Leppäkoski, E., S. Gollasch & S. Olenin (eds), Invasive aquatic species in Europe. Distribution, impacts and management. Kluwer Academic Publisher, Dordrecht: 27–52.
Zenetos, A., M. E. Çinar, M. A. Pancucci-Papadopoulou, J. G. Harmelin, G. Furnari, F. Andaloro, N. Bellou, N. Streftaris & H. Zibrowius, 2005. Annotated list of marine alien species in the Mediterranean with records of the worst invasive species. Mediterranean Marine Science 6: 63–118.
Acknowledgements
The authors would like to acknowledge the field work assistance of Sandrine Ruitton, Roland Graille, Bernard De Ligondes and Frederic Zuberer. We are grateful to Sidinei Thomaz, Mauricio Bini and two anonymous reviewers for helpful comments on an earlier draft. We thank Gwenaël Cadiou for the help in drawing Fig. 7 and Michael Paul for correcting the English text. The study was supported by a grant from the Agence de l’Eau Rhône-Méditerranée-Corse, the Conseil Général 13 and the Ville de Marseille to JCK.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: S. M. Thomaz
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Klein, J.C., Verlaque, M. Macrophyte assemblage associated with an invasive species exhibiting temporal variability in its development pattern. Hydrobiologia 636, 369–378 (2009). https://doi.org/10.1007/s10750-009-9966-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-009-9966-7


