Assessing the expansion and success of a restored population of Gongolaria barbata (Stackhouse) Kuntze (Fucales, Phaeophyceae) using high-precision positioning tools and size distribution frequencies

Published: Nov 9, 2022
cartography Cystoseira sensu lato Fucales marine forests monitoring rocky infralittoral

Ongoing human pressures over recent decades have caused the loss and ensuing impoverishment of the complexity and diversity of Mediterranean habitats dominated by algal species of the order Fucales. Gongolaria barbata, a habitat-forming Fucales species that has disappeared in several places across the Mediterranean, was reintroduced in a cove (Cala Teulera, Maó Bay, Menorca) where it was known to have been locally extinct for more than 40 years. Reintroduction was performed in 2011 using innovative non-destructive techniques. Here we describe the expansion patterns of the population ten years after its reintroduction, and we look at the size-structure distribution of the restored population compared to one of the only natural populations known in Spain (Fornells Bay, Menorca). Newly settled individuals exhibit a progressive dispersal pattern from restoration sites, favouring rocky substrates at the shallowest level parallel to the shore. The area occupied by G. barbata has increased by almost three orders of magnitude in ten years, from approximately 3.6 m2 of the initially restored area to a current restored area of 2093 m2. Recruits and juveniles dominate the restored population but some individuals have reached large size classes, the overall size distribution resembling the reference population. The high-resolution cartography included in our study enables an accurate mid to long-term assessment of the expansion of G. barbata. Incorporating such tools in restored marine forests would facilitate the implementation of efficient management policies that will help reinforce their conservation

Article Details
  • Section
  • Research Article
Download data is not yet available.
Ang, P.O., 1991. Age and size-dependent growth and mortality in a population of Fucus distichus. Marine Ecology Progress Series, 78, 173-187.
Arévalo, R., Pinedo, S., Ballesteros, E., 2007. Changes in the composition and structure of Mediterranean rocky-shore communities following a gradient of nutrient enrichment: Descriptive study and test of proposed methods to assess water quality regarding macroalgae. Marine Pollution Bulletin, 55, 104-113.
Badreddine, A., Abboud-Abi Saab, M., Gianni, F., Ballesteros, E., Mangialajo, L., 2018. First assessment of the ecological status in the Levant Basin: Application of the CARLIT index along the Lebanese coastline. Ecological Indicators, 85, 37-47.
Bahbah, L., Bensari, B., Chabane, K., Torras, X., Ballesteros, E. et al., 2020. Cartography of littoral rocky-shore communities to assess the ecological status of water bodies through the application of CARLIT method in Algeria (South-Western Mediterranean Sea). Marine Pollution Bulletin, 157, 111356.
Ballesteros, E., 1989. Production of seaweeds in Northwestern Mediterranean marine communities: its relation with environmental factors. Scientia Marina, 53, 357-364.
Ballesteros, E., 1992. Els vegetals i la zonació litoral: espècies, comunitats i factors que influeixen en la seva distribució. PhD Thesis. Arxius Secció Ciències Institut d’Estudis Catalans, Spain, 616 pp.
Ballesteros, E., Sala, E., Garrabou, J., Zabala, M., 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa Sauvageau in the Northwestern Mediterranean. European Journal of Phycology, 33, 121- 128.
Ballesteros, E., Sant, N., 2022. Homogeneity of photosynthetic features in canopy-forming algae of the order Fucales from shallow and sheltered environments. Cryptogamie, Algologie, 43, 107-115.
Ballesteros, E., Torras, X., Pinedo, S., García, M., Mangialajo, L. et al., 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Marine Pollution Bulletin, 55, 172-180.
Ballesteros, E., Garrabou, J., Hereu, B., Zabala, M., Cebrian, E. et al., 2009. Deep-water stands of Cystoseira zosteroides (Fucales, Phaeophyta) in the Northwestern Mediterranean: insights into assemblage structure and population dynamics. Estuarine, Coastal and Shelf Science, 82, 477-484.
Bayraktarov, E., Saunders, M.I., Abdullah, S., Mills, M., Beher, J. et al., 2016. The cost and feasibility of marine coastal restoration. Ecological Applications, 26, 1055-1074.
Berg, E.E., Hamrick, J.L., 1994. Spatial and genetic structure of two sandhill oaks: Quercus laevis and Quercus margaretta (Fagaceae). American Journal of Botany, 81, 7-14.
Blanfuné, A., Boudouresque, C.F., Verlaque, M., Beqiraj, S., Kashta, L. et al., 2016. Response of rocky shore communities to anthropogenic pressures in Albania (Mediterranean Sea): Ecological status assessment through the CARLIT method. Marine Pollution Bulletin, 109, 409-418.
Borja, Á., Dauer, D.M., Elliott, M., Simenstad, C.A., 2010. Medium- and long-term recovery of estuarine and coastal ecosystems: Patterns, rates and restoration effectiveness. Estuaries and Coasts, 33, 1249-1260.
Cebrian, E., Tamburello, L., Verdura, J., Guarnieri, G., Medrano, A. et al., 2021. A roadmap for the restoration of Mediterranean macroalgal forests. Frontiers in Marine Science, 8, 709219.
Chemello, R., Milazzo, M., 2002. Effect of algal architecture on associated fauna: Some evidence from phytal molluscs. Marine Biology, 140, 981-990.
Cheminée, A., Sala, E., Pastor, J., Bodilis, P., Thiriet, P. et al., 2013. Nursery value of Cystoseira forests for Mediterranean rocky reef fishes. Journal of Experimental Marine Biology and Ecology, 442, 70-79.
Clayton, M.N., 1992. Propagules of marine macroalgae: Structure and development. British Phycological Journal, 27, 219-232.
Cousens, R., 1985. Frond size distributions and the effects of the algal canopy on the behaviour of Ascophyllum nodosum (L.) Le Jolis. Journal of Experimental Marine Biology and Ecology, 92, 231-249.
de la Fuente, G., Chiantore, M., Gaino, F., Asnaghi, V., 2018. Ecological status improvement over a decade along the Ligurian coast according to a macroalgae based index (CARLIT). PLoS ONE, 13, e0206826.
de la Fuente, G., Chiantore, M., Asnaghi, V., Kaleb, S., Falace, A., 2019. First ex situ outplanting of the habitat-forming seaweed Cystoseira amentacea var. stricta from a restoration perspective. Peer J, 7, e7290.
del Hoyo-Bernat, X., 1981. El port de Maó: un ecosistema de gran interès ecològic i didàctic. Maina, 3, 32-37. Falace, A., Bressan, G., 2006. Seasonal variations of Cystoseira barbata (Stackhouse) C. Agardh frond architecture. Hydrobiologia, 555, 193-206.
Fernández, C., Gutiérrez, L.M., Rico, J.M., 1990. Ecology of Sargassum muticum on the North coast of Spain. Preliminary observations. Botanica Marina, 33, 423-428.
Gómez-Garreta, A., Barceló-Martí, M.C., Ribera-Siguan, M.A., Rull-Lluch, J., 2000. Cystoseiraceae. p. 89-166. In: Flora Phycologica Iberica Volume I, Fucales. Gómez-Garreta, (Eds). Universidad de Murcia, Murcia.
Hereu, B., Mangialajo, L., Ballesteros, E., Thibaut, T., 2008. On the occurrence, structure and distribution of deep-water Cystoseira populations in the Port-Cros National Park (Northwestern Mediterranean). European Journal of Phycology, 43, 263-273.
Lorimer, C.G., 1980. Age structure and disturbance history of a southern Appalachian virgin forest. Ecology, 61, 1169- 1184.
Mancuso, F.P., Strain, E.M.A., Piccioni, E., de Clerck, O., Sará, G. et al., 2018. Status of vulnerable Cystoseira populations along the Italian infralittoral fringe, and relationships with environmental and anthropogenic variables. Marine Pollution Bulletin, 129, 762-771.
Mangialajo, L., Chiantore, M., Cattaneo-Vietti, R., 2008. Loss of fucoid algae along a gradient of urbanisation, and structure of benthic assemblages. Marine Ecology Progress Series, 358, 63-74.
Mangialajo, L., Chiantore, M., Susini, M.L., Meinesz, A., Cattaneo-Vietti, R. et al., 2012. Zonation patterns and interspecific relationships of fucoids in microtidal environments. Journal of Experimental Marine Biology and Ecology, 412, 72-80.
Mariani, S., Cefalì, M.E., Terradas, M., Chappuis, E., Ballesteros, E., 2014. Using catenas for GIS-based mapping of NW Mediterranean littoral habitats. Estuarine, Coastal and Shelf Science, 147, 56-67.
Mariani, S., Cefalì, M.E., Chappuis, E., Terradas, M., Pinedo, S. et al., 2019. Past and present of Fucales from shallow and sheltered shores in Catalonia. Regional Studies in Marine Science, 32, 100824.
Medrano, A., Hereu, B., Cleminson, M., Pagès‐Escolà, M., Rovira, G.L. et al., 2020a. From marine deserts to algal beds: Treptacantha elegans revegetation to reverse stable degraded ecosystems inside and outside a No‐Take marine reserve. Restoration Ecology, 28, 632-644.
Medrano, A., Hereu, B., Mariani, S., Neiva, J., Pagès-Escolà, M. et al., 2020b. Ecological traits, genetic diversity and regional distribution of the macroalga Treptacantha elegans along the Catalan coast (NW Mediterranean Sea). Scientific Reports, 10, 19219.
Medrano, A., Linares, C., Aspillaga, E., Capdevila, P., Montero- Serra, I. et al., 2020c. Long-term monitoring of temperate macroalgal assemblages inside and outside a no-take marine reserve. Marine Environmental Research, 153, 104826.
Molinari-Novoa, E.A., Guiry, M.D., 2020. Reinstatement of the genera Gongolaria Boehmer and Ericaria Stackhouse (Sargassaceae, Phaeophyceae). Notulae Algarum, 172, 1-10.
Navarro, L., Ballesteros, E., Linares, C., Hereu, B., 2011. Spatial and temporal variability on deep-water algal assemblages in the Northwestern Mediterranean: insights into the effects of an exceptional storm. Estuarine, Coastal and Shelf Science, 95, 52-58.
Orellana, S., Hernández, M., Sansón, M., 2019. Diversity of Cystoseira sensu lato (Fucales, Phaeophyceae) in the eastern Atlantic and Mediterranean based on morphological and DNA evidence, including Carpodesmia gen. emend. and Treptacantha gen. emend. European Journal of Phycology, 54, 447-465.
Orfanidis, S., 1991. Temperature responses and distribution of macroalgae belonging to the warm-temperate Mediterranean- Atlantic distribution group. Botanica Marina, 34, 541-552.
Orfanidis, S., Rindi, F., Cebrian, E., Fraschetti, S., Nasto, I. et al., 2021. Effects of natural and anthropogenic stressors on fucalean brown seaweeds across different spatial scales in the Mediterranean Sea. Frontiers in Marine Science, 8, 658417.
Orlando-Bonaca, M., Pitacco, V., Slavinec, P., Šiško, M., Makovec, T. et al., 2021. First restoration experiment for Gongolaria barbata in Slovenian coastal waters. What can go wrong? Plants, 10, 239.
Perkol-Finkel, S., Airoldi, L., 2010. Loss and recovery potential of marine habitats: An experimental study of factors maintaining resilience in subtidal algal forests at the Adriatic Sea. PLoS ONE, 5, e10791.
Piazzi, L., Bonaviri, C., Castelli, A., Ceccherelli, G., Costa, G. et al., 2018. Biodiversity in canopy-forming algae: Structure and spatial variability of the Mediterranean Cystoseira assemblages. Estuarine, Coastal and Shelf Science, 207, 132-141.
Pinedo, S., García, M., Satta, M.P., De Torres, M., Ballesteros, E., 2007. Rocky-shore communities as indicators of water quality: a case study in the Northwestern Mediterranean. Marine Pollution Bulletin, 55, 126-135.
Pinnegar, J.K., Polunin, N.V., 2000. Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia, 122, 399-409.
R Core Team, 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL Rodríguez-Femenías, J.J., 1889. Algas de las Baleares. Anales de la Sociedad Española de Historia Natural, 18, 199-274.
Rodríguez-Prieto, C., Ballesteros, E., Boisset, F., Afonso-Carrillo, J., 2013. Guía de las macroalgas y fanerógamas marinas del Mediterráneo Occidental. Omega, Barcelona, 656 pp.
Russell, G., 1990. Age and stage in seaweed populations: a cautionary tale. British Phycological Journal, 25, 245-249.
Sala, E., Ballesteros, E., 1997. Partitioning of space and food resources by three fishes of the genus Diplodus (Sparidae) in a Mediterranean rocky infralittoral ecosystem. Marine Ecology Progress Series, 152, 273-283.
Sales, M., 2010. Cystoseira-dominated assemblages from sheltered areas in the Mediterranean Sea: Diversity, distribution and effects of pollution. PhD Thesis. Universitat de Girona, Spain, 261 pp. Sales, M., Ballesteros, E., 2009. Shallow Cystoseira (Fucales: Ochrophyta) assemblages thriving in sheltered areas from Menorca (NW Mediterranean): Relationships with environmental factors and anthropogenic pressures. Estuarine, Coastal and Shelf Science, 84, 476-482.
Sales, M., Ballesteros, E., 2012. Seasonal dynamics and annual production of Cystoseira crinita (Fucales: Ochrophyta)- dominated assemblages from the northwestern Mediterranean. Scientia Marina, 76, 391-401.
Sales, M., Cebrian, E., Tomas, F., Ballesteros, E., 2011. Pollution impacts and recovery potential in three species of the genus Cystoseira (Fucales, Heterokontophyta). Estuarine, Coastal and Shelf Science, 92, 347-357.
Sant, N., Chappuis, E., Rodríguez-Prieto, C., Real, M., Ballesteros, E., 2017. Cost-benefit of three different methods to study Mediterranean rocky assemblages. Scientia Marina, 81, 129-138.
Savonitto, G., de la Fuente, G., Tordoni, E., Ciriaco, S., Srijemsi, M. et al., 2021. Addressing reproductive stochasticity and grazing impacts in the restoration of a canopy‐forming brown alga by implementing mitigation solutions. Aquatic Conservation: Marine and Freshwater Ecosystems, 31, 1611-1623.
Schiel, D.R., Foster, M.S., 2006. The population biology of large brown seaweeds: Ecological consequences of multiphase life histories in dynamic coastal environments. Annual Review of Ecology, Evolution, and Systematics, 37, 343-372.
Sfriso, A., Facca, C., 2011. Macrophytes in the anthropic constructions of the Venice littorals and their ecological assessment by an integration of the “CARLIT” index. Ecological Indicators, 11, 772-781.
Tamburello, L., Papa, L., Guarnieri, G., Basconi, L., Zampardi, S. et al., 2019. Are we ready for scaling up restoration actions? An insight from Mediterranean macroalgal canopies. PloS ONE, 14, e0224477.
Teixidó, N., Gambi, M.C., Parravacini, V., Kroeker, K., Micheli, F. et al., 2018. Functional biodiversity loss along natural CO2 gradients. Nature Communications, 9, 5149.
Templado, J., Ballesteros, E., Galparsoro, I., Borja, A., Serrano, A. et al., 2012. Guía interpretativa: Inventario español de hábitats marinos. Inventario español de hábitats y especies marinos. Ministerio de Agricultura, Alimentación y Medio Ambiente, 229 pp.
Thibaut, T., Pinedo, S., Torras, X., Ballesteros, E., 2005. Longterm decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Marine Pollution Bulletin, 50, 1472-1489.
Thibaut, T., Blanfuné, A., Boudouresque, C.F., Verlaque, M., 2015. Decline and local extinction of Fucales in French Riviera: The harbinger of future extinctions? Mediterranean Marine Science, 16, 206-224.
Verdura, J., Sales, M., Ballesteros, E., Cefalì, M.E., Cebrian, E., 2018. Restoration of a canopy-forming alga based on recruitment enhancement: Methods and long-term success assessment. Frontiers in Plant Science, 9, 1832.
Most read articles by the same author(s)