Epiphytic algal flora associated with habitat-forming brown seaweed in a central Mediterranean coastal area (Conero Riviera, Adriatic Sea): diversity and relationship with environmental variables


Published: Jun 4, 2024
Keywords:
Algal forests Cystoseira ecosystem engineers Gongolaria barbata macrophytobenthos microphytobenthos
GIULIA BELLANTI
TIZIANA ROMAGNOLI
STEFANO ACCORONI
ALESSANDRA CAMPANELLI
CECILIA TOTTI
FABIO RINDI
Abstract

The Cystoseira s.l. complex includes the most common macrophytes in shallow sublittoral habitats of Mediterranean rocky shores, where they form marine forests providing valuable ecosystem services. These communities are considered to be repositories of great marine biodiversity, but the epiphytic assemblages associated with them are still not fully known. In particular, extremely limited information is available about their microalgal epiphytes. We examined the microepiphytic and macroepiphytic communities associated with the brown alga Gongolaria barbata in a coastal area of the central Adriatic shore (Conero Riviera, Italy). We recorded 119 microalgal taxa and 60 macroalgal taxa growing as epiphytes on this species. Diatoms were the dominant microepiphytes, accounting for 83% of the total number of taxa, followed by Dinophyceae (9%), unidentified phytoflagellates (4%) and Cyanobacteria (3%). A slight negative and positive correlation was observed between phytoflagellate abundance and water temperature and DIN (Dissolved Inorganic Nitrogen). Red algae represented the majority of the macroepiphytes recorded, accounting for 60% of the total. Most of the macroalgal epiphytes were ephemeral species with filamentous morphology, and the non-indigenous red alga Melanothamnus japonicus was among the most common epiphytes. Our results confirm the role of the Cystoseira s.l. species as a major repository of marine biodiversity in the Mediterranean. However, they also suggest that our understanding of the diversity of their associated communities is probably still largely incomplete. New studies combining traditional taxonomy and DNA metabarcoding will be essential to advance our knowledge of them.

Article Details
  • Section
  • Research Article
Downloads
Download data is not yet available.
References
Accoroni, S., Romagnoli, T., Pichierri, S., Totti, C., 2016. Effects of the bloom of harmful benthic dinoflagellate Ostreopsis cf. ovata on the microphytobenthos community in the northern Adriatic Sea. Harmful Algae, 55, 179-190.
Afanasyev, D.F., Akatov, V.V., 2021. Effects of Cystoseira sensu lato (Fucales: Phaeophyceae) on species richness, composition, and biomass of Abrau Peninsula Shelf macrophytobenthic communities (Black Sea). Oceanology, 61 (2), 244-253.
Al-Harbi, S.M., Abu Affan, M.D., 2016. Seasonal dynamics of epiphytic microalgae and their host seaweeds Florideophyceae at Jeddah Coast, the Red Sea, Saudi Arabia. Pakistan Journal of Botany, 48 (3), 1289-1298. Arrontes, J., 1990.
Composition, distribution on host, and seasonality of epiphytes on three intertidal algae. Botanica Marina, 33 (2), 205-212.
Ballesteros, E., 1988. Estructura y dinámica de la comunidad de Cystoseira mediterranea Sauvageau en el Mediterráneo Noroccidental. Investigación Pesquera, 52 (3), 313-334.
Ballesteros, E., 1990a. Structure and dynamics of the community of Cystoseira zosteroides (Turner) C. Agardh (Fucales, Phaeophyceae) in the Northwestern Mediterranean. Scientia Marina, 54 (3), 217-229.
Ballesteros, E., 1990b. Structure and dynamics of the Cystoseira caespitosa Sauvageau (Fucales, Phaeophyceae) community in the North-Western Mediterranean. Scientia Marina, 54 (2), 155-168.
Belegratis, M.R., Bitis, I., Economou-Amilli, A., Ott, J.A., 1999. Epiphytic patterns of macroalgal assemblages on Cystoseira species (Fucales, Phaeophyta) in the East Coast of Attica (Aegean Sea, Greece). Hydrobiologia, 412, 67-80.
Casamajor, M.N., Lalanne, Y., Derrien-Courtel, S., Maria Gorostiaga, J., Le Gal, A. et al., 2019. Cystoseira baccata meadows along the French Basque coast (Bay of Biscay) as a reference for the implementation of the Water Framework and Marine Strategy EU directives. Continental Shelf Research, 182, 12-21.
Cibic, T., Blasutto, O., Falconi, C., Fonda Umani, S., 2007. Microphytobenthic biomass, species composition and nutrient availability in sublittoral sediments of the Gulf of Trieste (northern Adriatic Sea). Estuarine Coastal and Shelf Science, 75 (1-2), 50-62.
Cibic, T., Blasutto, O., Bettoso, N., 2009. Microalgal-meiofaunal interactions in a sublittoral site of the Gulf of Trieste (northern Adriatic Sea, Italy): A three-year study. Journal of Experimental Marine Biology and Ecology, 370, 144-154.
Coleman, V.L., Burkholder, J.A.M., 1994. Community structure and productivity of epiphytic microalgae on eelgrass (Zostera marina L.) under water-column nitrate enrichment. Journal of Experimental Marine Biology and Ecology, 179 (1), 29-48.
Coppejans, E., 1983. Iconographie d’algues méditerranéennes. Chlorophyta, Phaeophyta, Rhodophyta. Bibliotheca Phycologica, 63, 1-28.
Cormaci, M., Furnari, G., Catra, M., Alongi, G., Giaccone, G., 2012. Flora marina bentonica del Mediterraneo: Phaeophyceae. Bollettino dell’Accademia Gioenia di Scienze Naturali di Catania, 45, 1-508.
Cormaci, M., Furnari, G., Alongi, G., 2014. Flora marina bentonica del Mediterraneo: Chlorophyta. Bollettino dell’Accademia Gioenia di Scienze Naturali di Catania, 47, 11-436.
Cormaci, M., Furnari, G., Alongi, G., 2017. Flora marina bentonica del Mediterraneo: Rhodophyta (Rhodymeniophycidae escluse). Bollettino dell’Accademia Gioenia di Scienze Naturali di Catania, 50, 1-391.
Cormaci, M., Furnari, G., Alongi, G., 2020. Flora marina bentonica del Mediterraneo: Rhodophyta - Rhodymeniophycidae I. Acrosymphytales, Bonnemaisoniales, Gelidiales, Gigartinales, Gracilariales. Bollettino Accademia Gioenia di Scienze Naturali di Catania, 53, 11-346.
Cormaci, M., Furnari, G., Alongi, G., 2021. Flora marina bentonica del Mediterraneo: Rhodophyta - Rhodymeniophycidae II. Halymeniales, Nemastomatales, Peyssonneliales, Plocamiales, Rhodymeniales, Sebdeniales. Bollettino Accademia Gioenia di Scienze Naturali di Catania, 54, 9-342.
Cormaci, M., Furnari, G., Alongi, G., Serio, D., 2023. Flora marina bentonica del Mediterraneo: Rhodophyta – Rhodymeniophycidae III: Ceramiales I (Rhodomelaceae escluse). Bollettino Accademia Gioenia di Scienze Naturali di Catania, 56 (386), 81-621.
DeNicola, D.M., McIntire, D., 1990. Effects of substrate relief on the distribution of periphyton in laboratory streams. ii. interactions with irradiance. Journal of Phycology, 26 (4), 634-641.
Deyanova, D.A., Berov, D., Stoyneva, M., 2010. Pilot study of the composition of epiphyte communities on Cystoseira barbata (Stackhouse) C. Agardh in Sozopol Region. p. 7-10. In: Proceedings Youth Scientific Conference ’Kliment Ohridski. 22-23 November 2010.
Fabbrizzi, E., Scardi, M., Ballesteros, E., Benedetti-Cecchi, L., Cebrian, E. et al., 2020. Modeling macroalgal forest distribution at mediterranean scale: present status, drivers of changes and insights for conservation and management. Frontiers in Marine Science, 7, 20.
Facca, C., Sfriso, A., Socal, G., 2002. Changes in abundance and composition of phytoplankton and microphytobenthos due to increased sediment fluxes in the Venice Lagoon, Italy. Estuarine, Coastal and Shelf Science, 54 (5), 773-792.
Falace, A., Kaleb, S., de La Fuente, G., Asnaghi, V., Chiantore, M., 2018. Ex situ cultivation protocol for Cystoseira amentacea var. stricta (Fucales, Phaeophyceae) from a restoration perspective. PLOS ONE, 13 (2), e0193011.
Ferrario, F., Iveša, L., Jaklin, A., Perkol-Finkel, S., Airoldi, L., 2015. The overlooked role of biotic factors in controlling the ecological performance of artificial marine habitats. Journal of Applied Ecology, 653, 16-24.
Frankovich, T., Gaiser, E., Zieman, J., Wachnicka, A., 2006. Spatial and temporal distributions of epiphytic diatoms growing on Thalassia testudinum Banks ex König: relationships to water quality. Hydrobiologia, 569 (1), 259-271.
García-Fernández, A., Bárbara, I., 2016. Studies of Cystoseira assemblages in Northern Atlantic Iberia. Anales del Jardin Botanico de Madrid, 73 (1), e035.
Gómez Garreta, A., Ribera Siguán, M.A., Seoane Camba, J.A., 1982. Estudio fenologico de varias especies del genero Cystoseira en Mallorca. Collectanea Botanica, 13 (2), 841-855.
Guiry, M.D., Guiry, G.M., 2023. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org (accessed 19 May 2023).
Hasle, G.R., Syvertsen, E.E., 1996. Marine diatoms. pp. 5-385. In: identifying marine diatoms and dinoflagellates. Tomas C.R. (Ed.) Academic Press, San Diego.
Hillebrand, H., Sommer, U., 2000. Effect of continuous nutrient enrichment on microalgae colonizing hard substrates. Hydrobiologia, 426 (1), 185-192.
Hillebrand, H., Worm, B., Lotze, H.K., 2000. Marine microbenthic community structure regulated by nitrogen loading and grazing pressure. Marine Ecology Progress Series, 204, 27-38.
Hustedt, F., 1985. The Pennate Diatoms, a translation of Hustedt’s “Die Kieselalgen, 2 Teil”, with suppl. of N.H. Jensen. Koeltz Scientific Books, Koenigstein, 918 pp.
Irving, A.D., Balata, D., Colosio, F., Ferrando, G.A., Airoldi, L., 2009. Light, sediment, temperature, and the early life-history of the habitat-forming alga Cystoseira barbata. Marine Biology, 156, 1223-1231.
Karez, R., Engelbert, S., Kraufvelin, P., Pedersen, M.F., Sommer, U., 2004. Biomass response and changes in composition of ephemeral macroalgal assemblages along an experimental gradient of nutrient enrichment. Aquatic Botany, 78 (2), 103-117.
Kozak, A., Unal, D., Tuney-Kizilkaya, I., 2020. Seasonal variations of epiphytic flora, abscisic acid production and physiological response in the brown alga Cystoseira foeniculacea (Linnaeus) Greville. Cahiers de Biologie Marine, 61 (2), 169-179.
Lavery, P.S., Vanderklift, M.A., 2002. A comparison of spatial and temporal patterns in epiphytic macroalgal assemblages of the seagrasses Amphibolis griffithii and Posidonia coriacea. Marine Ecology Progress Series, 236, 99-112.
Lenzo, D., Pezzolesi, L., Samorì, C., Rindi, F., Pasteris, A. et al., 2022. Allelopathic interactions between phytobenthos and meiofaunal community in an Adriatic benthic ecosystem: understanding the role of aldheydes and macroalgal structural complexity. Science of the Total Environment, 807, 150827.
Lenzo, D., Colangelo, M.A., Pasteris, A., Rindi, F., Pistocchi, R. et al., 2023. Understanding the role of macroalgal complexity and allelochemicals prouction in invasive and non-invasive macroalgae in the North-Western Adriatic Sea: effect on the associated communities. Water, 15, 1697.
Lluch, J.R., Garreta, A., 1989. Distribución de las algas epífitas sobre los ejemplares de ‘Cystoseira mediterranea’ Sauv. Anales Del Jardín Botánico de Madrid, 46 (1), 99-106.
Mačic, V., Svirčev, Z., 2014. Macroepiphytes on Cystoseira species (Phaeophyceae) on the Coast of Montenegro. Fresenius Environmental Bulletin, 23 (1), 29-34.
Majewska, R., Gambi, M.C., Totti, M.C., Pennesi, C., De Stefano, M., 2013. Growth form analysis of epiphytic diatom communities of Terra Nova Bay (Ross Sea, Antarctica). Polar Biology, 36, 73-86.
Mannino, A.M., Micheli, C., 2020. Ecological function of phenolic compounds from Mediterranean fucoid algae and seagrasses: an overview on the genus Cystoseira sensu lato and Posidonia oceanica (L.) Delile. Journal of Marine Science and Engineering. 8 (1), 19.
Marks, J.C., Power, M.E., 2001. Nutrient induced changes in the species composition of epiphytes on Cladophora glomerata Kütz. (Chlorophyta). Hydrobiologia, 450, 187-196.
Medrano, A., Hereu, B., Cleminson, M., Pagès-Escolà, M., Rovira, G.L. et al., 2020. 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 (3), 632-644.
Méléder, V., Rincé, Y., Barillé, L., Gaudin, P., Rosa, P., 2007. Spatiotemporal changes in microphytobenthos assemblages in a macrotidal flat (Bourgneuf Bay, France). Journal of Phycology, 43 (6), 1177-1190.
Menden-Deuer, S., Lessard, E.J., 2000. Carbon to volume relationships for dino-flagellates, diatoms, and other protist plankton. Limnology and Oceanography, 45 (3), 569- 579.
Morales-Ayala, S., Viera-Rodríguez, M.A., 1989. Distribución de los epífitos en Cystoseira tamariscifolia (Hudson) Papenfuss (Fucales, Phaeophyta) en Punta de Gáldar (Gran Canaria, Islas Canarias). Anales Jardín Botánico de Madrid, 46 (1), 108-113.
Nelson, T.A., 1997. Epiphyte-grazer interactions on Zostera marina (Anthophyta: Monocotyledones): effects of density on community function. Journal of Phycology, 33 (5), 743-752.
Otero-Schmitt, J., Pérez-Cirera, J., 1996, Epiphytism on Cystoseira (Fucales, Phaeophyta) from the Atlantic Coast of Northwest Spain. Botanica Marina, 39, 445-465.
Otero-Schmitt, J., Sanjuan, A., 1992, Epibiotic seaweeds of the Cape Verde islands. Botanica Marina, 35, 379-390. Peragallo, H., Peragallo, M., 1897-1908. Diatomées marines de France et des districts maritimes voisins. Grez-sur Loing (S.-et-M.): J. Tempère, Micrographe-Editeur. pp. 491; I-XII: pp. 48, pl. 135.
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.
Prazukin, A.V., Firsov, Y.K., Kamenir, Y., 2020. The vertical structure of the vegetative canopy of the brown algae Cystoseira (Black Sea). Journal of Oceanology and Limnology, 38 (1), 124-132.
Rindi, F., Gavio, B., Díaz-Tapia, P., Di Camillo, C.G., Romagnoli, T., 2020. Long-term changes in the benthic macroalgal flora of a coastal area affected by urban impacts (Conero Riviera, Mediterranean Sea). Biodiversity and Conservation, 29, 2275-2295.
Rindi, F., Cinelli, F., 2000. Phenology and small-scale distribution of some rhodomelacean red algae on a western mediterranean rocky shore. European Journal of Phycology, 35 (2), 115-125.
Rindi, F., Vergés, A., Zuchegna, I., Bianchelli, S., de Caralt, S. et al., 2023. Standardized protocol for reproductive phenology monitoring of fucalean algae of the genus Cystoseira s.l. with potential for restoration. Frontiers in Marine Science, 10, 1250642.
Rodriguez-Prieto, C., Ballesteros, E., Boisset, F., Afonso-Carrillo, J., 2013. Guia de las macroalgas y fanerogamas marinas del Mediterraneo occidental. Ediciones Omega, S.A., Barcelona. 656 pp.
Romagnoli, T., Bavestrello, G., Cucchiari, E.M., De Stefano, M., Di Camillo, C.G. et al., 2007. Microalgal communities epibiontic on the marine hydroid Eudendrium racemosum in the Ligurian Sea during an annual cycle. Marine Biology, 151 (2), 537-552.
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 (4), 476-482.
Sales, M., Ballesteros, E., 2010. Long-term comparison of algal assemblages dominated by Cystoseira crinita (Fucales, Heterokontophyta) from Cap Corse (Corsica, North Western Mediterranean). European Journal of Phycology, 45 (4), 404-412.
Sales, M., Ballesteros, E., Anderson, M.J., Iveša, L., Cardona, E., 2012. Biogeographical patterns of algal communities in the Mediterranean Sea: Cystoseira crinita-dominated assemblages as a case study. Journal of Biogeography, 39 (1), 140-152.
Sauvageau, C., 1912. A propos des Cystoseira de Banyuls et Guéthary. Bulletin de la Station Biologique d’Arcachon, 14, 133-556.
Serio, D., 1994. On the structure, typology and periodism of Cystoseira spinosa Savageau community and of Cystoseira zosteroides C. Agardh community from Eastern Coast of Sicily (Mediterranean Sea). Giornale Botanico Italiano, 128 (6), 941-973.
Snoeijs, P., 1994. Distribution of epiphytic diatom species composition, diversity and biomass on different macroalgal hosts along seasonal and salinity gradients in the Baltic Sea. Diatom Research, 9 (1), 189-211.
Snoeijs, P., 2016. Effects of salinity on epiphytic diatom communities on Pilayella littoralis (Phaeophyceae) in the Baltic Sea. Écoscience, 2 (4), 382-394.
Steneck, R.S., Dethier, M.N., 1994. A functional group approach to the structure of algal-dominated communities. Oikos, 69 (3), 476-498.
Strain, E.M.A., van Belzen, J., van Dalen, J., Bouma, T.J., Airoldi, L., 2015. Management of local stressors can improve the resilience of marine canopy algae to global stressors. PLOS ONE, 10 (3), e0120837.
Strickland, J.D.H., Parsons, T.R. 1972. A practical handbook of seawater analysis. Fisheries Research Board of Canada, Ottawa, 310 pp. Tanaka, N., 1986. Adhesive strength of epiphytic diatoms on various seaweeds. Bulletin of the Japanese Society of Scientific Fisheries, 52 (2), 817-821.
Thomas, D.P., Jiang, J., 1986. Epiphytic diatoms of the inshore marine area near Davis Station. Hydrobiologia, 140 (3), 193-198.
Totti, C., 2003. Influence of the plume of the river Po on the distribution of subtidal microphytobenthos in the Northern Adriatic Sea. Botanica Marina, 46, 161-178.
Totti, C., Cucchiari, E., De Stefano, M., Pennesi, C., Romagnoli, T. et al., 2007. Seasonal variations of epilithic diatoms on different hard substrates, in the northern Adriatic Sea. Journal of the Marine Biological Association of the United Kingdom, 87 (3), 649-658.
Totti, C., Poulin, M., Romagnoli, T., Perrone, C., Pennesi, C. et al., 2009. Epiphytic diatom communities on intertidal seaweeds from Iceland. Polar Biology, 32 (11), 1681-1691.
Tuji, A., 2000. The effect of irradiance on the growth of different forms of freshwater diatoms: implications for succession in attached diatom communities. Journal of Phycology, 36 (4), 659-661.
Van Heurck, H., 1880-1885. Synopsis des Diatomées de Belgique. 132 (Suppl. A, B, C). Anvers, Ducaju et Cie. pp. 235.
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.
Wear, D.J., Sullivan, M.J., Moore, A.D., Millie, D.F., 1999. Effects of water-column enrichment on the production dynamics of three seagrass species and their epiphytic algae. Marine Ecology Progress Series, 179, 201-213.
Welker, C., Sdrigotti, E., Covelli, S., Faganeli, J., 2002. Microphytobenthos in the Gulf of Trieste (Northern Adriatic Sea): relationship with labile sedimentary organic matter and nutrients. Estuarine, Coastal and Shelf Science, 55 (2), 259-273.
Wellnitz, T.A., Ward, J.V., 2000. Herbivory and irradiance shape periphytic architecture in a Swiss alpine stream. Limnology and Oceanography, 45 (1), 64-75.
Worm, B., Sommer, U., 2000. Rapid direct and indirect effects of a single nutrient pulse in a seaweed-epiphyte-grazer system. Marine Ecology Progress Series, 202, 283-288.
Most read articles by the same author(s)