Scientia Marina, Vol 74, No 1 (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)

Miguel Cabanellas-Reboredo
Laboratorio de Biología Marina. Departamento de Biología, Universidad de las Islas Baleares , Spain

Andreu Blanco
Laboratorio de Biología Marina. Departamento de Biología, Universidad de las Islas Baleares , Spain

Salud Deudero
Laboratorio de Biología Marina. Departamento de Biología, Universidad de las Islas Baleares , Spain

Silvia Tejada
Laboratorio de Biología Marina. Departamento de Biología, Universidad de las Islas Baleares , Spain


Pinna nobilis and its guests Pontonia pinnophylax and Nepinnotheres pinnotheres were sampled from Posidonia oceanica meadows invaded and non-invaded by the red alga Lophocladia lallemandii. Understanding the interactions among native and invasive species was the primary aim. Therefore, the effects of the invasive L. lallemandii on the percentage contribution of the food sources of P. nobilis and its guests and their trophic associations were investigated by applying mixing models to the δ13C and δ15N stable isotopes. Isotopic analyses revealed that the guests of P. nobilis occupied a higher trophic level than their host due to their capacity for food selection. The invasion of L. lallemandii altered the percentage contribution of the food sources to the consumers’ diet. Whereas the percentage contribution of the food sources to the δ13C signatures did not really change, L. lallemandii produced variations in the percentage contribution to the δ15N signatures. This red macroalga represented one of the main food sources for P. nobilis, with a real contribution of 19.4% in the invaded meadows. Moreover, L. lallemandii slightly decreased the trophic level of the consumers. This study provides the first isotopic and trophic data for the pea crab N. pinnotheres.


Pinna nobilis; Pontonia pinnophylax; Nepinnotheres pinnotheres; food sources; stable isotopes; mixing models; Lophocladia lallemandii; Posidonia oceanica

Full Text:



Baeza, J.A. – 2008. Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlanica, off the Pacific coast of Panama. Mar. Biol., 153: 387-395. doi:10.1007/s00227-007-0815-9

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

Ballesteros, E., E. Cebrian and T. Alcoverro. – 2007. Mortality of shoots of Posidonia oceanica following meadow invasion by the red alga Lophocladia lallemandii. Bot. Mar., 50: 8-13. doi:10.1515/BOT.2007.002

Boudouresque, C.F. and M. Verlaque. – 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Pollut. Bull., 44: 32-38. doi:10.1016/S0025-326X(01)00150-3 PMid:11883681

Butler, A., N. Vicente and B. De Gaulejac. – 1993. Ecology of de Pterioid bivalves Pinna bicolor Gmelin and Pinna nobilis L. Mar. Life, 3: 37-45.

Calafiore, N., G. Costanzo and S. Giacobbe. – 1991. Mediterranean species of the genus Pontonia latreille, 1829. I. Developmental stages of Pontonia pinnophylax (Otto, 1821) (Decapoda, Natantia, Pontoniinae) reared in the laboratory. Crustac. Int. J. Crustac. Res., 60: 52-75.

Carabel, S., E. Godínez-Domínguez, P. Verísimo, L. Fernández and J. Freire. – 2006. An assessment of sample processing methods for stable isotope analyses of marine food webs. J. Exp. Mar. Biol. Ecol., 336: 254-261. doi:10.1016/j.jembe.2006.06.001

Cardona, L., M. Revelles, M. Sales, A. Aguilar and A. Borrell. – 2007. Meadows of the seagrass Posidonia oceanica are a significant source of organic matter for adjoining ecosystems. Mar. Ecol. Progr. Ser., 335: 123-131. doi:10.3354/meps335123

Centoducati, G., E. Tarsitano, A. Bottalico, M. Marvulli, O.R. Lai and G. Crescenzo. – 2007. Monitoring of the endangered Pinna nobilis Linne, 1758 in the Mar Grande of Taranto (Ionian Sea, Italy). Environ. Monit. Assess., 131: 339-347. doi:10.1007/s10661-006-9479-z PMid:17171265

Decottignies, P., P.G. Beninger, Y. Rince, R.J. Robins and P. Riera. – 2007. Exploitation of natural food sources by two sympatric, invasive suspension-feeders: Crassostrea gigas and Crepidula fornicata. Mar. Ecol. Progr. Ser., 334: 179-192. doi:10.3354/meps334179

Deudero, S., A. Blanco, A. Box, G. Mateu-Vicens, M. Cabanellas-Reboredo and A. Sureda. – 2009. Interaction between the invasive macroalga Lophocladia lallemandii and the bryozoan Reteporella grimaldii at seagrass meadows: density and physiological responses. Biol. Invasions.

EEC. – 1992. Council Directive on the conservation of natural habitats and of wild fauna and flora (the habitats and species directive), 94/43/EEC. Official Journal of the European Communities, No L2006/7, Brussels.

Fisher, S.J., M.L. Brown and D.W. Willis. – 2001. Temporal food web variability in an upper Missouri River backwater: energy origination points and transfer mechanisms. Ecol. Freshw. Fish., 10: 154-167. doi:10.1034/j.1600-0633.2001.100305.x

Galil, B.S. – 2007. Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar. Pollut. Bull., 55: 314-322. doi:10.1016/j.marpolbul.2006.11.008 PMid:17222869

Galinou-Mitsoudi, S., G. Vlahavas and O. Papoutsi. – 2006. Population study of the protected bivalve Pinna nobilis (Linnaeus, 1758) in Thermaikos Gulf (North Aegean Sea). J. Biol. Res., 5: 47-53.

García-March, J.R. – 2003. Contribution to the knowledge of the status of Pinna nobilis (L.) 1758 in Spanish coasts. Mem. Inst. Oc. Paul Ricard., pp 29-41.

García-March, J.R., A.M. García-Carrascosa and A.L. Pena. – 2002. In situ measurement of Pinna nobilis shells for age and growth studies: Anew device. Mar. Ecol. -Publ. Staz. Zool. Napoli I., 23: 207-217.

Gross, H., Goeger, D.E., Hills, P., Mooberry, S.L., Ballantine, D.L., Murray, T.F., F.A. Valeriote and W.H. Gerwick. – 2006. Lophocladines, Bioactive Alkaloids from the Red Alga Lophocladia sp. J. Nat. Prod., 69: 640-644. doi:10.1021/np050519e PMid:16643042    PMCid:2668242

Hemminga, M.A. and C.M. Duarte. – 2000. Seagrass Ecology, Cambridge.

Ince, R., G.A. Hyndes, P. Lavery and M.A. Vanderklift. – 2007. Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuar. Coast. Shelf Sci., 74: 77-86. doi:10.1016/j.ecss.2007.03.029

Katsanevakis, S. – 2007. Growth and mortality rates of the fan mussel Pinna nobilis in Lake Vouliagmeni (Korinthiakos Gulf, Greece): a generalized additive modelling approach. Mar. Biol., 152: 1319-1331. doi:10.1007/s00227-007-0781-2

Kennedy, H., C.A. Richardson, C.M. Duarte and D.P. Kennedy. – 2001a. Diet and association of Pontonia pinnophylax occurring in Pinna nobilis: insights from stable isotope analysis. J. Mar. Biol. Assoc. UK, 81: 177-178. doi:10.1017/S0025315401003575

Kennedy, H., C.A. Richardson, C.M. Duarte and D.P. Kennedy. – 2001b. Oxygen and carbon stable isotopic profiles of the fan mussel, Pinna nobilis, and reconstruction of sea surface temperatures in the Mediterranean. Mar. Biol., 139: 1115-1124. doi:10.1007/s002270100673

Lagana, G., S. Gjacobbe, E. Bellocco, C. Mannucci, A. Galtieri, S. Ficarra, A. Kotyk and U. Leuzzia. – 2007. Lactate and malate dehydrogenase in the fan-shell associated shrimp, Pontonia pinnophylax (Otto): Effects of temperature and urea. J. Exp. Mar. Biol. Ecol., 349: 27-34. doi:10.1016/j.jembe.2007.03.017

Le Loc’h, F., C. Hily and J. Grall. – 2008. Benthic community and food web structure on the continental shelf of the Bay of Biscay (North Eastern Atlantic) revealed by stable isotopes analysis. J. Marine Syst., 72: 17-34. doi:10.1016/j.jmarsys.2007.05.011

MacDougall, A.S. and R. Turkington. – 2005. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology, 86: 42-55. doi:10.1890/04-0669

Marin, F., B. Pokroy, G. Luquet, P. Layrolle and K. De Groot. – 2007. Protein mapping of calcium carbonate biominerals by immunogold. Biomaterials., 28: 2368-2377. doi:10.1016/j.biomaterials.2007.01.029 PMid:17306364

Mercado-Silva, N. – 2005. Condition index of the eastern oyster, Crassostrea virginica (Gmelin, 1791) in Sapelo Island Georgia - Effects of site, position on bed and pea crab parasitism. J. Shellfish Res., 24: 121-126.

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

Peter, K.L.N. and R.B. Manning. – 2003. On two new genera of pea crabs parasitic in holothurians (Crustacea: Decapoda: Brachyura: Pinnotheridae) from the Indo-West Pacific, with notes on allied genera. Proc. Biol. Soc. Washington, 116: 901-919.

Phillips, D.L. and J.W. Gregg. – 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia, 136: 261-269. doi:10.1007/s00442-003-1218-3 PMid:12759813

Phillips, D.L., S.D. Newsome and J.W. Gregg. – 2005. Combining sources in stable isotope mixing models: alternative methods. Oecologia, 144: 520-527. doi:10.1007/s00442-004-1816-8 PMid:15711995

Piazzi, L., G. Pardi, D. Balata, E. Cecchi and F. Cinelli. – 2002. Seasonal dynamics of a subtidal north-western Mediterranean macroalgal community in relation to depth and substrate inclination. Bot. Mar., 45: 243-252. doi:10.1515/BOT.2002.023

Pinnegar, J.K. and N.V.C. Polunin. – 1999. Differential fractionation of δ13C and delta δ15Namong fish tissues: implications for the study of trophic interactions. Funct. Ecol., 13: 225-231. doi:10.1046/j.1365-2435.1999.00301.x

Pinnegar, J.K. and N.V.C. Polunin. – 2000. Contributions of stable isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia, 122: 399-409. doi:10.1007/s004420050046

Pitt, K.A., A. Clement, R.M. Connolly and D. Thibault-Botha. – 2008. Predation by jellyfish on large and emergent zooplankton: implications for benthic-pelagic coupling. Estuar. Coast. Shelf Sci., 76: 827-833. doi:10.1016/j.ecss.2007.08.011

Post, D.M. – 2002. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology, 83: 703-718.

Rabaoui, L., S.T. Zouari, S. Katsanevakis and O.K. Ben Hassine. – 2007. Comparison of absolute and relative growth patterns among five Pinna nobilis populations along the Tunisian coastline: an information theory approach. Mar. Biol., 152: 537-548. doi:10.1007/s00227-007-0707-z

Rabaoui, L., S.T. Zouari and O.K. Ben Hassine. – 2008. Two species of Crustacea (Decapoda) associated with the fan mussel, Pinna nobilis Linnaeus, 1758 (Mollusca, Bivalvia). Crustac. Int. J. Crustac. Res., 81: 433-446.

Richardson, C.A., H. Kennedy, C.M. Duarte and S.V. Proud. – 1997. The occurrence of Pontonia pinnophylax (Decapoda: Natantia: Pontoniinae) in Pinna nobilis (Mollusca: Bivalvia: Pinnidae) from the Mediterranean. J. Mar. Biol. Assoc. UK, 77: 1227-1230. doi:10.1017/S0025315400038741

Richardson, C.A., H. Kennedy, C.M. Duarte, D.P. Kennedy and S.V. Proud. – 1999. Age and growth of the fan mussel Pinna nobilis from south-east Spanish Mediterranean seagrass (Posidonia oceanica) meadows. Mar. Biol., 133: 205-212. doi:10.1007/s002270050459

Sarà, G., D. Scilipoti, A. Mazzola and A. Modica. – 2004. Effects of fish farming waste to sedimentary and particulate organic matter in a southern Mediterranean area (Gulf of Castellammare, Sicily): a multiple stable isotope study (δ13C and δ15N). Aquaculture, 234: 199-213. doi:10.1016/j.aquaculture.2003.11.020

Sun, W.M., S.C. Sun, Y.Q. Wang, B.W. Yang and W.B. Song. – 2006. The prevalence of the pea crab, Pinnotheres sinensis, and its impact on the condition of the cultured mussel, Mytilus galloprovincialis, in Jiaonan waters (Shandong Province, China). Aquaculture., 253: 57-63. doi:10.1016/j.aquaculture.2005.07.037

Sureda, A., A. Box, M. Ensenat, E. Alou, P. Tauler, S. Deudero and A. Pons. – 2006. Enzymatic antioxidant response of a labrid fish (Coris julis) liver to environmental caulerpenyne. Comp. Biochem. Phys., 144: 191-196.

Sureda, A., A. Box, J. Terrados, S. Deudero and A. Pons. – 2008. Antioxidant response of the seagrass Posidonia oceanica when epiphytized by the invasive macroalgae Lophocladia lallemandii. Mar. Environ. Res., 66: 359-363. doi:10.1016/j.marenvres.2008.05.009 PMid:18639925

Templado, J., M. Calvo, A. García, A.A. Luque, M. Maldonado and L. Moro. – 2004. Guía de invertebrados y peces marinos protegidos por la legislación nacional e internacional. Ministerio de Medio Ambiente, Serie técnica, Madrid.

Vicente, N. – 1984. Grand coquillage plein de distinction. La grande nacre de Méditerranée Pinna nobilis. Rev. Fond. Océanogr. Paul Ricard, 7: 30-34.

Williams, S.L. – 2007. Introduced species in seagrass ecosystems: Status and concerns. J. Exp. Mar. Biol. Ecol., 350: 89-110. doi:10.1016/j.jembe.2007.05.032

Yonge, C.M. – 1953. Form and habit in Pinna carnea Gmelin. Phil. Trans. Royal Soc. London BBiol. Sci., 237: 335-374. doi:10.1098/rstb.1953.0006

Zavodnik, D., M. Hrs-Brenko and M. Legac. – 1991. Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic sea. In: C.F. Boudouresque, M. Avon and V. Gravez (eds.), Les Espèces Marines à Protéger en Méditerranée, pp. 169-178. GISPosidonie Publications Marseille, France.

Copyright (c) 2010 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Contact us

Technical support