Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-19T05:45:49.878Z Has data issue: false hasContentIssue false
  • English
  • Français

Colonization on Pinna nobilis at a marine protected area: extent of the spread of two invasive seaweeds

Published online by Cambridge University Press:  19 March 2014

Maite Vázquez-Luis ,
Gàlia Banach-Esteve ,
Elvira Álvarez  and
Salud Deudero
Maite Vázquez-Luis*
Affiliation:
Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma de Mallorca, Spain
Gàlia Banach-Esteve
Affiliation:
Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma de Mallorca, Spain
Elvira Álvarez
Affiliation:
Govern de les Illes Balears, Direcció General de Medi Rural i Marí, C/Foners, 10. 07006 Palma de Mallorca, Spain
Salud Deudero
Affiliation:
Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma de Mallorca, Spain
*
Correspondence should be addressed to: M. Vázquez-Luis, Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma de Mallorca, Spain email: maite.vazquez@ba.ieo.es
Get access Rights & Permissions [Opens in a new window]

Abstract

Introduction of species is a major driver of global change and loss of biodiversity in ecosystems. The Mediterranean Sea is the most heavily invaded region in the world by introduced seaweeds. The fan mussel Pinna nobilis is the largest Mediterranean bivalve, and a protected species, present at depths from 0.5 m to 60 m. In Cabrera National Park marine protected area (MPA) (Balearic Islands, north-western Mediterranean) the population of P. nobilis is affected by the invasive seaweeds Lophocladia lallemandii and Caulerpa racemosa; however the extent of this colonization on the bivalve is unknown. Therefore, the main aims of the present study were to: (1) determine the extent of invasion of L. lallemandii and C. racemosa on the P. nobilis population; and (2) test if this invasion showed differences with depth. This is the first study assessing invasion by seaweeds on a large bivalve in a high density P. nobilis population. Pinna nobilis was distributed in all seagrass meadows surveyed within the MPA; we found a total of 872 live P. nobilis individuals, 449 and 423 of which were found at 10 and 20 m depth, respectively. High cover of L. lallemandii and low presence of C. racemosa were detected in the P. nobilis population, being quantified in 49.37% and 1.38% of the population of P. nobilis, respectively. Bathymetric differences on Lophocladia epizoism over P. nobilis has been recorded in this study; with increasing values of L. lallemandii cover index, biomass and volume at deeper depths. Pinna nobilis could be a preferential substratum for L. lallemandii in Posidonia oceanica meadows in deeper waters, acting as a stepping-stone for invasive seaweeds and facilitating the invasion throughout seagrass meadows.

Keywords

biological invasionsLophocladia lallemandiiCaulerpa racemosaPinna nobilisMediterraneanalien speciesintroduced seaweedsepizoismspecies interactions
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 5 , August 2014 , pp. 857 - 864
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abramoff, M.D., Magelhaes, P.J. and Ram, S.J. (2004) Image processing with ImageJ. Biophotonics International 11, 36–42.Google Scholar
Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Anderson, M.J., Gorley, R.N. and Clarke, K.R. (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: PRIMER-E.Google Scholar
Ballesteros, E. (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanography and Marine Biology: an Annual Review 44, 123–195.Google Scholar
Ballesteros, E., Cebrian, E. and Alcoverro, T. (2007) Mortality of shoots of Posidonia oceanica following meadow invasion by the red alga Lophocladia lallemandii. Botanica Marina 50, 8–13.Google Scholar
Banach-Esteve, G. (2011) Influence of Global Change on Pinna nobilis: Impact of the invasive macroalgae Lophocladia lallemandii and Caulerpa racemosa on the population of Cabrera National Park. Master thesis, 19 pp.Google Scholar
Bartoli, M., Nizzoli, D., Viaroli, P., Turolla, E., Castaldelli, G., Fano, E.A. and Rossi, R. (2001) Impact of Tapes philippinarum farming on nutrient dynamics and benthic respiration in Sacca di Goro. Hydrobiologia 455, 203–212.Google Scholar
Bedini, R., Bonechi, L. and Piazzi, L. (2011) Spread of the introduced alga Lophocladia lallemandii in the Tuscan Archipielago (NW Mediterranean Sea). Cryptogamie Algologie 32, 383–391.Google Scholar
Boudouresque, C.F. and Verlaque, M. (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 44, 32–38.Google Scholar
Box, A., Martin, D. and Deudero, S. (2010) Changes in seagrass polychaete assemblages after invasion by Caulerpa racemosa var. cylindracea (Chlorophyta: Caulerpales): community structure, trophic guilds and taxonomic distinctness. Scientia Marina 74, 317–329.Google Scholar
Box, A., Sureda, A. and Deudero, S. (2009) Antioxidant response of the bivalve Pinna nobilis colonised by invasive red macroalgae Lophocladia lallemandii. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 14, 456–460.Google Scholar
Butler, A.J., Vincente, N. and Gaulejac, B. (1993) Ecology of the pteroid bivalves Pinna bicolor Gmelin and Pinna nobilis Linnaeus. Marine Life 3, 37–45.Google Scholar
Cabanellas-Reboredo, M., Blanco, A., Deudero, S. and 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). Scientia Marina 74, 101–110.Google Scholar
Callaway, R.M. (2007) Positive interactions and interdependence in plant communities. Berlin: Springer-Verlag.Google Scholar
Cebrian, E. and Ballesteros, E. (2009) Temporal and spatial variability in shallow- and deep-water populations of the invasive Caulerpa racemosa var. cylindracea in the western Mediterranean. Estuarine, Coastal and Shelf Science 83, 469–474.Google Scholar
Cebrian, E. and Ballesteros, E. (2010) Invasion of Mediterranean benthic assemblages by red alga Lophocladia lallemandii (Montagne) F. Schmitz: depth-related temporal variability in biomass and phenology. Aquatic Botany 92, 81–85.Google Scholar
Cebrian, E., Ballesteros, E., Linares, C. and Tomas, F. (2011) Do native herbivores provide resistance to Mediterranean marine bioinvasions? A seaweed example. Biological Invasions 13, 1397–1408.Google Scholar
Ceccherelli, G. and Cinelli, F. (1999) Effects of Posidonia oceanica canopy on Caulerpa taxifolia size in a north-western Mediterranean Bay. Journal of Experimental Marine Biology and Ecology 240, 19–36.Google Scholar
Ceccherelli, G., Piazzi, L. and Cinelli, F. (2000) Response of the nonindigenous Caulerpa racemosa (Forsskål) J. Agardh to the native seagrass Posidonia oceanica (L.) Delile: effect of density of shoots and orientation of edges of meadows. Journal of Experimental Marine Biology and Ecology 243, 227–240.Google Scholar
Clarke, K.R. and Gorley, R.N. (2006) PRIMER v6: user manual/tutorial. Plymouth: PRIMER-E.Google Scholar
Clavier, J. and Chardy, P. (1989) Investigation into the ecology of the ormer (Haliotis tuberculata L.), factors influencing spatial distribution. Aquatic Living Resources 2, 191–197.Google Scholar
Colautti, R.I., Ricciardi, A., Grigorovich, I.A. and MacIsaac, H.J. (2004) Does the enemy release hypothesis predict invasion success? Ecology Letters 7, 721–733.Google Scholar
Crooks, J.A. (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97, 153–166.Google Scholar
Deudero, S., Blanco, A., Box, A., Mateu-Vicens, G., Cabanellas-Reboredo, M. and Sureda, A. (2010) Interaction between the invasive macroalga Lophocladia lallemandii and the bryozoan Reteporella grimaldii at seagrass meadows: density and physiological responses. Biological Invasions 12, 41–52.Google Scholar
EEC (1992) Council directive on the conservation of natural habitats and of wild fauna and flora (The habitats and species directive), 92/43/EEC. Official Journal of the European Communities No L 206/7, Brussels.Google Scholar
Garcia-March, J.R. and Márquez-Aliaga, A. (2007) Pinna nobilis L., 1758 age determination by internal shell register. Marine Biology 151, 1077–1085.Google Scholar
Katsanevakis, S. (2006) Population ecology of the endangered fan mussel Pinna nobilis in a marine lake. Endangered Species Research 1, 51–59.Google Scholar
Klein, J. and Verlaque, M. (2008) The Caulerpa racemosa invasion: a critical review. Marine Pollution Bulletin 56, 205–225.Google Scholar
MacDougall, A.S. and Turkington, R. (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86, 42–55.Google Scholar
Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M. and Bazzaz, F.A. (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10, 689–710.Google Scholar
Marba, N., Duarte, C.M., Holmer, M., Martinez, R., Basterretxea, G., Orfila, A., Jordi, A. and Tintore, J. (2002) Assessing the effectiveness of protection on Posidonia oceanica populations in the Cabrera National Park (Spain). Environmental Conservation 29, 509–518.Google Scholar
Maron, J.L. and Vilà, M. (2001) When do herbivores affect plant invasion? Evidence of the natural enemies and biotic resistance hypothesis. Oikos 95, 361–373.Google Scholar
McArdle, B.H. and Anderson, M.J. (2001) Fitting multivariate models to community data: a comment on distance based redundancy analysis. Ecology 82, 290–297.Google Scholar
Occhipinti-Ambrogi, A. and Savini, D. (2003) Biological invasions as a component of global change in stressed marine ecosystems. Marine Pollution Bulletin 46, 542–551.Google Scholar
Panayotidis, P. and Žuljevič, A. (2001) Sexual reproduction of the invasive green alga Caulerpa racemosa var. occidentalis in the Mediterranean Sea. Oceanologica Acta 24, 199–203.Google Scholar
Parker, D.J., Burkepile, D.E. and Hay, M.E. (2006) Opposing effects of native and exotic herbivores on plant invasion. Science 311, 1459–1461.Google Scholar
Patzner, R. (1998) The invasion of Lophocladia (Rhodomelaceae, Lophotalieae) at the northern coast of Ibiza (western Mediterranean Sea). Bolletí de la Societat d'Història Natural de les Balears 41, 75–80.Google Scholar
Piazzi, L., Meinesz, A., Verlaque, M., Akcali, B., Antolič, B., Argyrou, M., Balata, D., Ballesteros, E., Calvo, S., Cinelli, F., Cirik, S., Cossu, A., D' Archino, R., Djellouli, A.S., Javel, F., Lanfranco, E., Mifsud, C., Pala, D., Panayotidis, P., Peirano, A., Pergent, G., Petrocelli, A., Ruitton, S., Žuljevič, A. and Ceccherelli, G. (2005) Invasion of Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptogamie Algologie 26, 189–202.Google Scholar
Richardson, C.A., Kennedy, H., Duarte, C.M., Kennedy, D.P. and Proud, S.V. (1999) Age and growth of the fan mussel Pinna nobilis from south-east Spanish Mediterranean seagrass (Posidonia oceanica) meadows. Marine Biology 133, 205–212.Google Scholar
Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., Baughman, S., Cabin, R.J., Cohen, J.E., Ellstrand, N.C., McCauley, D.E., O'Neil, P., Parker, I.M., Thompson, J.N. and Weller, S.G. (2001). The population biology of invasive species. Annual Review of Ecology, Evolution, and Systematics 32, 305–332.Google Scholar
Sergio, F., Newton, I., Marchesi, L. and Pedrini, P. (2006) Ecologically justified charisma: preservation of top predators delivers biodiversity conservation. Journal of Applied Ecology 43, 1049–1055.Google Scholar
Tahil, A.S. and Juinio-Menez, M.A. (1999) Natural diet, feeding periodicity and functional response to food density of the abalone, Haliotis asinina L., (Gastropoda). Aquaculture Research 30, 95–107.Google Scholar
Tejada, S., Deudero, S., Box, A. and Sureda, A. (2013) Physiological response of the sea urchin Paracentrotus lividus fed with the seagrass Posidonia oceanica and the alien algae Caulerpa racemosa and Lophocladia lallemandii. Marine Environmental Research 83, 48–53.Google Scholar
Templado, J. (2004) Guia de invertebrados y peces marinos protegidos por la legislación nacional e internacional. In Organismo Autónomo de Parques Nacionales. Madrid: Ministerio de Medio Ambiente, pp. 86–89.Google Scholar
Tomas, F., Cebrian, E. and Ballesteros, E. (2011) Differential herbivory of invasive algae by native fish in the Mediterranean Sea. Estuarine, Coastal and Shelf Science 92, 27–34.Google Scholar
Tyler, R.M. (2007) Effects of coverage by benthic seaweeds mats on (Northern Quahog = Hard Clam) Mercenaria mercenaria in a eutrophic estuary. Journal of Shellfish Research 26, 1021–1028.Google Scholar
Vázquez-Luis, M., Guerra-García, J.M., Sanchez-Jerez, P. and Bayle-Sempere, J.T. (2009) Caprellid assemblages (Crustacea: Amphipoda) in shallow waters invaded by Caulerpa racemosa var. cylindracea from southeastern Spain. Helgoland Marine Research 63, 107–117.Google Scholar
Vázquez-Luis, M., Sanchez-Jerez, P. and Bayle-Sempere, J.T. (2008) Changes in amphipod (Crustacea) assemblages associated with shallow-water algal habitats invaded by Caulerpa racemosa var. cylindracea in the western Mediterranean Sea. Marine Environmental Research 65, 416–426.Google Scholar
Vázquez-Luis, M., Sanchez-Jerez, P. and Bayle-Sempere, J.T. (2010) Effects of Caulerpa racemosa var. cylindracea on prey availability: an experimental approach to predation by Thalassoma pavo (Labridae) on amphipods. Hydrobiologia 654, 147–154.Google Scholar
Verlaque, M., Afonso-Carrillo, J., Gil-Rodriguez, M.C., Durand, C., Boudouresque, C.F. and Le Parco, Y. (2004) Blitzkrieg in a marine invasion: Caulerpa racemosa var. cylindracea (Bryopsidales, Chlorophyta) reaches the Canary Islands (NE Atlantic). Biological Invasions 6, 269–281.Google Scholar
Verlaque, M., Durand, C., Huisman, J.M., Boudouresque, C.F. and Le Parco, Y. (2003) On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). European Journal of Phycology 38, 325–339.Google Scholar
Vicente, N. and Moreteau, J.C. (1991) Status of Pinna nobilis L. en Mediterrance (Mollusque Eulamellibranche). In Boudouresque, C.F., Avon, M. and Garvez, M. (eds) Les espèces marines á protèger en Mèditerranèe. Marseilles: GIS Posidonie, pp. 159–168.Google Scholar
Williamson, M.H. and Fitter, A. (1996) The varying success of invaders. Ecology 77, 1661–1666.Google Scholar
Wright, J.T., McKenzie, L.A. and Gribben, P.E. (2007) A decline in the abundance and condition of a native bivalve associated with Caulerpa taxifolia invasion. Marine and Freshwater Research 58, 263–272.Google Scholar
Zavodnik, D. (1967) Contribution to the ecology of Pinna nobilis L. (Mollusca: Bivalvia) in the Northern Adriatic Sea. Thalassia Jugoslavica 3, 93–102.Google Scholar
Zavodnik, D., Hrs-Brenko, M. and Legac, M. (1991) Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic Sea. In Boudouresque, C.F., Avon, M. and Gravez, V. (eds) Les espèces marines à protéger en Méditerranée. Marseilles: GIS Posidonie, pp 169–178.Google Scholar