Cymodocea nodosa vs. Caulerpa prolifera: Causes and consequences of a long term history of interaction in macrophyte meadows in the Mar Menor coastal lagoon (Spain, southwestern Mediterranean)

Estuarine, Coastal and Shelf Science

Volumn 110, Issue , 2012, Pages 101-115

  Pérez Ruzafa, Angel ^a   Marcos, Concepción ^a   Bernal, Carmen M ^a   Quintino, Victor ^c   Freitas, Rosa ^c   Rodrigues, Ana Maria ^c   García Sánchez, Marta ^a   Pérez Ruzafa, Isabel M ^b  

^a UNIVERSITY OF MURCIA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

Caulerpa prolifera; Coastal lagoon; Competition; Cymodocea nodosa; Macrophytes; Seagrass meadows; Transitional waters

Indexed keywords

ADAPTATION; ANTHROPOGENIC EFFECT; BIOMASS; COASTAL LAGOON; COLONIZATION; EVOLUTIONARY BIOLOGY; HYDROGRAPHY; INTERSPECIFIC COMPETITION; MACROALGA; MACROPHYTE; MEADOW; PHYSIOLOGY; POPULATION DISTRIBUTION; SEAGRASS; SEAWEED; SILT; SULFIDE;

MAR MENOR; MURCIA [SPAIN]; SPAIN;

ALGAE; CAULERPA; CAULERPA PROLIFERA; CYMODOCEA NODOSA;

EID: 84865315305     PISSN: 02727714     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecss.2012.04.004     Document Type: Article

References (91)

1. Anderson M.J. A new method for non-parametric multivariate analysis of variance. Austral Ecology 2001, 26:32-46.
2. Anderson M.J. PERMANOVA: A FORTRAN Computer Program for Permutational Multivariate Analysis of Variance 2005, Department of Statistics, University of Auckland, New Zealand, 24 pp.
3. Aravio-Torre J., Arévalo A. La salinidad del Mar Menor, sus variaciones.- Algunas consideraciones sobre el intercambio de aguas con el Mar Mediterráneo. Boletín del Instituto Español de Oceanografía 1971, 146:3-20.
4. Arévalo A., Aravio-Torre J. La salinidad de las lagunas litorales. El Mar Menor (Murcia). Apéndice. Tablas hidrográficas para salinidades de 47'32 a 53'10 por 1000. Boletín del Instituto Español de Oceanografía 1969, 139:1-37.
5. Arévalo L. El Mar Menor como sistema forzado por el Mediterráneo. Control hidráulico y agentes fuerza. Boletín del Instituto Español de Oceanografía 1988, 5(1):63-96.
6. Atkinson M.J., Smith S.V. C:N:P ratios of benthic marine plants. Limnology and Oceanography 1983, 28(3):568-574.
7. Bachelet G., de Montaudouin X., Auby I., Labourg P.J. Seasonal changes in macrophyte and macrozoobenthos assemblages in three coastal lagoons under varying degrees of eutrophication. ICES Journal of Marine Science 2000, 57(5):1495-1506.
8. Best E.P.H., Buzzelli C.P., Bartell S.M., Wetzel R.L., Boyd W.A., Doyle R.D., Campbell K.R. Modeling submersed macrophyte growth in relation to underwater light climate: modeling approaches and application potential. Hydrobiologia 2001, 444:43-70.
9. Borcard D., Legendre P., Drapeau P. Partialling out the spatial component of ecological variation. Ecology 1992, 73:1045-1055.
10. Boudouresque C.F., Bernard G., Pergent G., Shili A., Verlaque M. Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Botanica Marina 2009, 52:395-418.
11. Bremner J.M. Total nitrogen. Methods of Soil Analysis. Part 2 ' Chemical and Microbiological Properties 1965, 1149-1400. American Society of Agronomy, Inc. Publisher, Wiscosin. C.A. Black (Ed.).
12. Buchanan J.B. Sediment analysis. Methods for the Study of Marine Benthos 1984, 41-65. Blackwell, Oxford. N.A. Holme, A.D. Mcintyre (Eds.).
13. Burkholder J.M., Tomasko D.A., Touchette B.W. Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 2007, 350:46-72.
14. Butigieg J. La despoblación del Mar Menor y sus causas. Boletín de Pescas. Dirección General de Pesca del Ministerio de Marina 1927, vol. 133. Instituto Español de Oceanografía, 251-286.
15. Calleja M.L., Marba N., Duarte C.M. The relationship between seagrass (Posidonia oceanica) decline and sulfide porewater concentration in carbonate sediments. Estuarine, Coastal and Shelf Science 2007, 73(3-4):583-588.
16. Ceccherelli G., Campo D. Different effects of Caulerpa racemosa on two Co-occurring seagrasses in the Mediterranean. Botanica Marina 2002, 45:71-76.
17. Charpentier A., Grillas P., Lescuyer F., Coulet E., Auby I. Spatio-temporal dynamics of a Zostera noltii dominated community over a period of fluctuating salinity in a shallow lagoon, Southern France. Estuarine, Coastal and Shelf Science 2005, 64:307-315.
18. Chubarenko B., Koutitonsky V.G., Neves R., Umgiesser G. Modeling concepts. Coastal Lagoons: Ecosystem Processes and Modeling for Sustainable Use and Development 2005, 231-306. CRC Press, Boca Ratón. I.E. Gönenç, J.P. Wolflin (Eds.).
19. Costanza R., dArge R., deGroot R., Farber S., Grasso M., Hannon B., Limburg K., Naeem S., ONeill R.V., Paruelo J., Raskin R.G., Sutton P., vandenBelt M. The value of the world's ecosystem services and natural capital. Nature 1997, 387(6630):253-260.
20. De Pascalis, F., Pérez-Ruzafa, A., Gilabert, J., Marcos, C., Umgiesser, G., Climate change response of the Mar Menor coastal lagoon (Spain) using a hydrodynamic finite element model. Estuarine, Coastal and Shelf Science, doi:10.1016/j.ecss.2011.12.002.
21. Duarte C.M. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 1995, 41:87-112.
22. Duarte C.M., Terrados J., Agawin N.S.R., Fortes M.D., Bach S., Kenworthy W.J. Response of a mixed Philippine seagrass meadow to experimental burial. Marine Ecology Progress Series 1997, 147:285-294.
23. Duchaufour P. Manual de Edafología 1975, Toray-Masson, Barcelona, 476 pp.
24. Eklof J.S., McMahon K., Lavery P.S. Effects of multiple disturbances in seagrass meadows: shading decreases resilience to grazing. Marine and Freshwater Research 2009, 60(12):1317-1327.
25. Erftemeijer P.L.A., Middelburg J.J. Sediment-nutrient interactions in tropical seagrass beds: a comparison between a terrigenous and a carbonate sedimentary environment in South Sulawesi (Indonesia). Marine Ecology Progress Series 1993, 102:187-198.
26. European Environment Agency Eutrophication in Europe's Coastal Waters 2001, Topic report No. 7, Copenhagen.
27. Gab-Alla A.A.-F.A. Ecological study on community of exotic invasive seaweed Caulerpa prolifera in Suez Canal and its associated macro invertebrates. Journal of Applied Sciences 2007, 7(5):679-686.
28. Gamito S., Gilabert J., Marcos C., Pérez-Ruzafa A. Effects of changing environmental conditions on lagoon ecology. Coastal Lagoons: Ecosystem Processes and Modeling for Sustainable Use and Development 2005, 193-229. CRC Press, Boca Ratón, Florida. I.E. Gönenç, J.P. Wolflin (Eds.).
29. Garcia Carrascosa A.M. Contribución al conocimiento del bentos del Mar Menor: poblamientos bentónicos de las islas Perdiguera, Redonda y del Sujeto. Estudio descriptivo y cartografía bionómica. Actas I Simpósio Ibérico de Estudios del Bentos Marino, San Sebastián 1982, 795-812.
30. García-Sánchez, M., Korbee, N., Pérez-Ruzafa, I.M., Marcos, C., Domínguez, B., Figueroa, F.L., Pérez-Ruzafa, A. Physiological response and photoacclimation capacity of macrophyte meadows in the Mar Menor lagoon (SE Spain). Marine Environmental Research, in press.
31. Gilabert, J., 1992. Análisis del ecosistema planctónico del Mar Menor. Ciclo anual, distribución de tamaños y red trófica. PhD thesis, Universidad de Murcia, 147 pp.
32. Gilabert J., Pérez-Ruzafa A., Gutiérrez J.M., Bel-Lan A., Moreno V. Light attenuation coefficient in shallow coastal waters from airborne multispectral data: implications for water quality and bottom features estimation. EARSeL Advances in Remote Sensing 1995, 4(1-IX):76-86.
33. Hastings K., Hesp P., Kendrick G.A. Seagrass loss associated with boat moorings at Rottnest Island, Western Australia. Ocean and Coastal Management 1995, 26(3):225-246.
34. Hegazi, M.M.I., 1999. Composición pigmentaria y propiedades ópticas de la vegetación submarina costera del Mediterráneo Occidental. PhD thesis, Universidad de Murcia, 348 pp.
35. Hemminga M.A. The root/rhizome system of seagrasses: an asset and a burden. Journal of Sea Research 1998, 39:183-196.
36. Hughes A.R., Williams S.L., Duarte C., Heck K.L., Waycott M. Associations of concern: declining seagrasses and threatened dependent species. Frontiers in Ecology and the Environment 2009, 7(5):242-246.
37. Keddy P.A. Quantifying a within-lake gradient of wave energy in Gillfillan Lake, Nova scotia. Canadian Journal of Botany 1983, 62:301-309.
38. Kjerfve B. Coastal lagoons. Elsevier Oceanography Series 1994, vol. 60:1. Elsevier, Amsterdam. B. Kjerfve (Ed.).
39. Leoni V., Vela A., Pasqualini V., Pergent-Martini C., Pergent G. Effects of experimental reduction of light and nutrient enrichments (N and P) on seagrasses: a review. Aquatic Conservation-Marine and Freshwater Ecosystems 2008, 18(2):202-220.
40. Likens G.E. Eutrophication and aquatic ecosystems. Limnology and Oceanography 1972, 1(Special Symposia):3.
41. Lillo M.J. Geomorfología del Mar Menor. Papeles del Departamento de Geografía 1981, 8:9-48.
42. Lloret J., Marin A., Marin-Guirao L., Velasco J. Changes in macrophytes distribution in a hypersaline coastal lagoon associated with the development of intensively irrigated agriculture. Ocean and Coastal Management 2005, 48(9-10):828-842.
43. Lozano F. Una campaña de prospección pesquera en Mar Menor (Murcia). Boletín del Instituto Español de Oceanografía 1954, 66:1-34.
44. Marba N., Duarte C.M., Holmer M., Calleja M.L., Alvarez E., Diaz-Almela E., Garcias-Bonet N. Sedimentary iron inputs stimulate seagrass (Posidonia oceanica) population growth in carbonate sediments. Estuarine, Coastal and Shelf Science 2008, 76(3):710-713.
45. Meinesz, A., 1979. Contribution à l'étude des Caulerpales (Chlorophytes). PhD thesis, Université de Nice, France, 262 pp.
46. Minello T.J., Able K.W., Weinstein M.P., Hays C.G. Salt marshes as nurseries for nekton: testing hypotheses on density, growth and survival through meta-analysis. Marine Ecology Progress Series 2003, 246:39-59.
47. Moreno F. Estudio de un ciclo anual del plancton en el Mar Menor. CRIS Rev. de la Mar 1975, 149:12-17.
48. Navarro F.de P. Observaciones sobre el Mar Menor (Murcia). Notas y Resúmenes Instituto Español de Oceanografía ser.II 1927, 16. 63 p.
49. Navarro M.C., Pérez-Sirvent C., Martínez-Sanchez M.J., Vidal J., Tovar P.J., Bech J. Abandoned mine sites as a source of contamination by heavy metals: a case study in a semi-arid zone. Journal of Geochemical Exploration 2008, 96:183-193.
50. Nixon S.W. Coastal marine eutrophication: a definition, social causes and future concerns. Ophelia 1995, 41:199-219.
51. Obrador B., Pretus J.L. Spatiotemporal dynamics of submerged macrophytes in a Mediterranean coastal lagoon. Estuarine, Coastal and Shelf Science 2010, 87:145-155.
52. Orth R.J., Carruthers T.J.B., Dennison W.C., Duarte C.M., Fourqurean J.W., Heck K.L., Hughes A.R., Kendrick G.A., Kenworthy W.J., Olyarnik S., Short F.T., Waycott M., Williams S.L. A global crisis for seagrass ecosystems. Bioscience 2006, 56(12):987-996.
53. Parsons T.R., Maita Y., Lalli C.M. A Manual of Chemical and Biological Methods for Sea Water Analysis 1984, Pergamon Press, Oxford, 173 pp.
54. Pérez-Ruzafa, A., 1989. Estudio ecológico y bionómico de los poblamientos bentónicos del Mar Menor (Murcia, SE de España). PhD thesis, Universidad de Murcia,751 p.
55. Pérez-Ruzafa A. Red de Control y Vigilancia de la Calidad de las Aguas Litorales - Mar Menor 2003, Informe técnico C.A.R M. Grupo de Investigación: Ecología y ordenación de ecosistemas marinos costeros. Universidad de Murcia, 77 p.
56. Pérez-Ruzafa A. Red de Control y Vigilancia de la Calidad de las Aguas Litorales - Mar Menor 2007, Informe técnico C.A.R M. Grupo de Investigación: Ecología y ordenación de ecosistemas marinos costeros. Universidad de Murcia, 85, pp.
57. Pérez-Ruzafa A., Aragón R. Implicaciones de la gestión y el uso de las aguas subterráneas en el funcionamiento de la red trófica de una laguna costera. Conflictos entre el desarrollo de las aguas subterráneas y la conservación de los humedales: litoral mediterráneo 2003, 215. Fundación Marcelino Botín-Mundiprensa, Madrid. J.M. Fornés, M.R. Llamas (Eds.).
58. Perez-Ruzafa A., Marcos C. Los sustratos arenosos y fangosos del Mar Menor (Murcia), su cubierta vegetal y su posible relación con la disminución del mújol en la laguna. Cuadernos Marisqueros Publicación Técnica 1987, 11:111-123.
59. Pérez-Ruzafa A., Marcos C., Pérez-Ruzafa I.M., Ros J.D. Evolución de las características ambientales y de los poblamientos del Mar Menor (Murcia, SE de España). Anales de Biología 12 (Biología ambiental 1987, 3):53-65.
60. Pérez-Ruzafa A., Ros J.D., Marcos C., Pérez-Ruzafa I.M., Ballester R. Distribution and biomass of the macrophyte beds in a hypersaline coastal lagoon (the Mar Menor, SE Spain) and its recent evolution following major environmental changes. International Workshop on Posidonia Beds 2 1989, 49-62. G.I.S. Posidonie Publisher, Marseille. C.-F. Boudouresque, A. Meinesz, E. Fresi, V. Gravez (Eds.).
61. Pérez-Ruzafa A., Marcos C., Ros J. Environmental and Biological changes related to recent human activities in the Mar Menor. Marine Pollution Bulletin 1991, 23:747-751.
62. Pérez-Ruzafa A., Gilabert J., Bel-Lan A., Moreno V., Gutiérrez J.M. New approach to chlorophyll a determination in shallow coastal waters by remote sensing. Scientia Marina 1996, 60(Supl.1):19-27.
63. Pérez-Ruzafa A., Navarro S., Barba A., Marcos C., Camara M.A., Salas F., Gutierrez J.M. Presence of pesticides throughout trophic compartments of the food web in the Mar Menor lagoon (SE of Spain). Marine Pollution Bulletin 2000, 40(2):140-151.
64. Pérez-Ruzafa A., Gilabert J., Gutiérrez J.M., Fernández A.I., Marcos C., Sabah S. Evidence of a planktonic food web response to changes in nutrient input dynamics in the Mar Menor coastal lagoon, Spain. Hydrobiologia 2002, 475/476:359-369.
65. Pérez-Ruzafa A., Fernández A.I., Marcos C., Gilabert J., Quispe J.I., García-Charton J.A. Spatial and temporal variations of hydrological conditions, nutrients and chlorophyll a in a Mediterranean coastal lagoon (Mar Menor, Spain). Hydrobiologia 2005, 550:11-27.
66. Pérez-Ruzafa A., Marcos C., Gilabert J. The ecology of the Mar Menor coastal lagoon: a fast-changing ecosystem under human pressure. Coastal Lagoons: Ecosystem Processes and Modeling for Sustainable Use and Development 2005, 392-422. CRC Press, Boca Ratón, Florida. I.E. Gönenç, J.P. Wolflin (Eds.).
67. Pérez-Ruzafa A., García-Charton J.A., Barcala E., Marcos C. Changes in benthic fish assemblages as a consequence of coastal works in a coastal lagoon: the Mar Menor (Spain, Western Mediterranean). Marine Pollution Bulletin 2006, 53:107-120.
68. Pérez-Ruzafa A., Hegazi M.I., Pérez-Ruzafa I.M., Marcos C. Differences in spatial and seasonal patterns of macrophyte assemblages between a coastal lagoon and the open sea. Marine Environmental Research 2008, 65:291-314.
69. Pergent G., Boudouresque C.-F., Dumay O., Pergent-Martini C., Wyllie-Echeverria S. Competition between the invasive macrophyte Caulerpa taxifolia and the seagrass Posidonia oceanica: contrasting strategies. BMC Ecology 2008, 8:20.
70. Pergent-Martini C., Rico-Raimondino V., Pergent G. Impact des nutrients sur les herbiers à Posidonia oceanica. Données préliminaires. Journal of Research in Océanography 1996, 21:35-39.
71. Pergent-Martini C., Boudouresque C.F., Pasqualini V., Pergent G. Impact of fish farming facilities on Posidonia oceanica meadows: a review. Marine Ecology 2006, 27:310-319.
72. Quintino V., Freitas R., Mamede R., Ricardo F., Rodrigues A.M., Mota J., Pérez-Ruzafa A., Marcos C. Remote sensing of underwater vegetation using single-beam acoustics. ICES Journal of Marine Science 2010, 67(3):594-605.
73. Ros M., Miracle R.M. Variación estacional del fitoplancton del Mar Menor y su relación con la de un punto próximo en el Mediterráneo. Limnética 1984, 1:32-42.
74. Ruiz J.M., Perez M., Romero J. Effects of fish farm loadings on seagrass (Posidonia oceanica) distribution, growth and photosynthesis. Marine Pollution Bulletin 2001, 42(9):749-760.
75. Sand-Jensen K., Borum J. Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquatic Botany 1991, 41:137-175.
76. Schaffelke B., Hewitt C.L. Impacts of introduced seaweeds. Botanica Marina 2007, 50:397-417.
77. Soil Conservation Service Investigación de suelos. Métodos de laboratorio v procedimientos para recoger muestras 1973, Trillas, México.
78. Sfriso A., Birkemeyer T., Ghetti P.F. Benthic macrofauna changes in areas of Venice lagoon populated by seagrasses or seaweeds. Marine Environmental Research 2001, 52(4):323-349.
79. Sfriso A., Facca C., Ghetti P.F. Temporal and spatial changes of macroalgae and phytoplankton in a Mediterranean coastal area: the Venice lagoon as a case study. Marine Environmental Research 2003, 56:617-636.
80. Simonneau, J. 1973. Mar Menor: Evolution sédimentologique et géochimique récente en remplissage. Thése.
81. Taplin K.A., Irlandi E.A., Raves R. Interference between the macroalga Caulerpa prolifera and the seagrass Halodule wrightii. Aquatic Botany 2005, 83(3):175-186.
82. ter Braak C.J.F., Šmilauer P. CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (Version 4.5) 2002, Microcomputer Power, Ithaca, NY, USA.
83. Terrados, J., 1986. Pigmentos fotosintéticos y producción primaria de las comunidades bentónicas del Mar Menor, Murcia. Tesis de licenciatura. Universidad de Murcia.
84. Terrados J., Ros J.D. Production dynamics in a macrophyte-dominated ecosystem: the Mar Menor coastal lagoon (SE Spain). Oecologia Aquatica 1991, vol. 10:255-270. J.D. Ros, N. Prat (Eds.).
85. Terrados J., Ros J.D. Temporal variation of the biomass and structure of Caulerpa prolifera (Forsskali) Lamouroux meadows in the Mar Menor lagoon (SE Spain). Scientia Marina 1995, 59(1):49-56.
86. Terrados J., Duarte C.M., Fortes M.D., Borum J., Agawin N.S.R., Bach S., Thampanya U., Kamp-Nielsen L., Kenworthy W.J., Geertz-Hansen O., Vermaat J. Changes in community structure and biomass of seagrass communities along gradients of siltation in SE Asia. Estuarine, Coastal and Shelf Science 1998, 46:757-768.
87. Terrados J., Duarte C.M., Kamp-Nielsen L., Agawin N.S.R., Gacia E., Lacap D., Forte s M.D., Borum J., Lubanski M., Grevec T. Are seagrass growth and survival constrained by the reducing conditions of the sediment?. Aquatic Botany 1999, 65:175-197.
88. Thomsen M.S., Wernberg T., Engelen A.H., Tuya F., Vanderklift M.A., Holmer M., McGlathery K.J., Arenas F., Kotta J., Silliman B.R. A Meta-Analysis of Seaweed Impacts on Seagrasses: Generalities and Knowledge Gaps. PLoS ONE 2012, 7(1):e28595. 10.1371/journal.pone.0028595.
89. Umgiesser G., Cucco A. Computation of transport time scales through numerical modelling. Geomatic Solutions for Coastal Environments 2010, 229-250. Nova Science Publishers, New York. M. Maanan, M. Robin (Eds.).
90. Underwood A.J. Experiments in Ecology 1997, Cambridge University Press, Cambridge.
91. Waycott M., Duarte C.M., Carruthers T.J.B., Orth R.J., Dennison W.C., Olyarnik S., Calladine A., Fourqurean J.W., Heck K.L., Hughes A.R., Kendrick G.A., Kenworthy W.J., Short F.T., Williams S.L. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 2009, vol. 106(30):12377-12381.