Abstract
The Gongolaria barbata forest inhabiting Šćuza lagoon on the southern Istrian coast (northern Adriatic) represents the last significant refuge for this species among the shallow waters of the Istrian Coast. The lagoon is characterised by extreme winter and summer temperatures. Moreover, the absence of certain grazers could be one of the main factors favouring the development and growth of G. barbata forest. Two morphologically distinct forms of G. barbata inhabit the lagoon: attached and detached. Abundance and morphological characteristics of each form were analysed in randomly sampled thalli. The wet weight, thallus length, number of cauloids and total cauloid length were significantly higher in the detached than in the attached form. Although the main cauloid was highly branched in both forms, its total length was up to three times higher in the detached than in the attached form. Our study suggests that this population of G. barbata can thrive in the extreme conditions found in the lagoon, while also exhibiting two distinct forms. Furthermore, this large population could serve as a donor for future restoration attempts on the western Istrian Coast where a decline of G. barbata has been confirmed in recent years.
Funding source: Hrvatska Zaklada za Znanost
Award Identifier / Grant number: IP-2019-04-6984
About the authors
Ljiljana Iveša is a senior research associate at the Center for Marine Research in Rovinj, Ruđer Bošković Institute, Croatia. Her field of research includes taxonomy and ecology of macrophytobenthos (seaweeds and seagrasses), ecology of coastal habitats of the natural rocky shore and artificial hard surfaces and assessment of the ecological status of coastal waters using macroalgal assemblages. Her current research is focused on ecology of canopy-forming species of the order Fucales and distribution patterns of non-indigenous species.
Andrea Bilajac is an assistant at the Center for Marine Research in Rovinj, Ruđer Bošković Institute, Croatia, and a PhD candidate. His field of interest is the ecology of canopy and forest forming fucalean macroalgae. As part of the project HabCys, his current work is focused on assessing the impact of local and global stressors on fucalean macroalgae, mapping of fucalean species along the west Istrian Coast and building a scientific basis for the restoration of degraded marine forests.
Edi Gljušćić is an assistant at the Center for Marine Research in Rovinj, Ruđer Bošković Institute, Croatia. His field includes marine conservation biology as well as marine ecology. Currently, his work is focused on the ecology and restoration of canopy-forming fucalean species habitats, especially in the mediolitoral zone and tidepools. He also collects terrestrial and freshwater biodiversity data of Istria mainly on butterflies, dragonflies, amphibians and reptiles.
Mirjana Najdek is a senior scientist at the Center for Marine Research in Rovinj, Ruđer Bošković Institute, Croatia. Her field of research includes the origin and processes of organic matter in marine ecosystem studied by lipid biomarkers: fatty acids, hydrocarbons and sterols. Her current research is focused on physiology and ecology of macroalgae and seagrasses.
Acknowledgements
We are grateful to the editor and two anonymous reviewers for their suggestions and constructive criticism.
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Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Research funding: The study was supported by Croatian Science Foundation project: The responses of habitat-forming brown macroalgae of the genus Cystoseira on local and global stressors (grant no. IP-2019-04-6984).
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Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Airoldi, L. and Beck, M.W. (2007). Loss, status and trends for coastal marine habitats of Europe. Oceanogr. Mar. Biol. 45: 345–405.10.1201/9781420050943.ch7Search in Google Scholar
Airoldi, L., Ballesteros, E., Buonuomo, R., van Belzen, J., Bouma, T.J., Cebrian, E., De Clerk, O., Engelen, A.H., Ferrario, F., Fraschetti, S., et al.. (2014). Marine forests at risk: solutions to halt the loss and promote the recovery of Mediterranean canopy-forming seaweeds. In: Langar, H., Bouafif, C., and Ouerghi, A. (Eds.), Proceedings of the 5th Mediterranean Symposium on Marine Vegetation. Slovenia: Portorož, pp. 28–33.Search in Google Scholar
Ballesteros, E. (1990). Structure and dynamics of the Cystoseira caespitosa Sauvageau (Fucales, Phaeophyceae) community in the North-Western Mediterranean. Sci. Mar. 54: 155–168.Search in Google Scholar
Ballesteros, E., Sala, E., Garrabou, J., and Zabala, M. (1998). Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean. Eur. J. Phycol. 3: 121–128. https://doi.org/10.1080/09670269810001736613.Search in Google Scholar
Battelli, C. and Catra, M. (2021). First report of Cystoseira aurantia (Sargassaceae, Fucophyceae) from the lagoon of Strunjan (Gulf of Trieste, northern Adriatic). Ann. Ser. Hist. Nat. 31: 139–146.Search in Google Scholar
Bellan-Santini, D. (1968). Influence da la pollution sur les peuplements benthiques. Rev. Int. Oceanogr. Med. 10: 27–53.Search in Google Scholar
Bennett, S., Wernberg, T., de Bettignies, T., Kendrick, G.A., Anderson, R.J., Bolton, J.J., Rodgers, K.L., Shears, N.T., Leclerc, J.C., Leveque, L., et al.. (2015). Canopy interactions and physical stress gradients in subtidal communities. Ecol. Lett. 18: 677–686. https://doi.org/10.1111/ele.12446.Search in Google Scholar
Bianchi, C.N. and Morri, C. (2000). Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Mar. Pollut. Bull. 40: 367–376. https://doi.org/10.1016/s0025-326x(00)00027-8.Search in Google Scholar
Blanfuné, A., Boudouresque, C.F., Verlaque, M., and Thibaut, T. (2019). The ups and downs of a canopy-forming seaweed over a span of more than one century. Sci. Rep. 9: 5250. https://doi.org/10.1038/s41598-019-41676-2.Search in Google Scholar PubMed PubMed Central
Bologa, A.S. and Sava, D. (2006). Progressive decline and present trend of the Romanian Black Sea macroalgal flora. Cercetari Marine 36: 31–60.Search in Google Scholar
Catra, M., Alongi, G., Leonardi, R., Negri, M.P., Sanfilippo, R., Serio, D., Viola, A., and Rosso, A. (2019). Degradation of a photophilic algal community and its associated fauna from eastern Sicily (Mediterranean Sea). Mediterr. Mar. Sci. 20: 74–89. https://doi.org/10.12681/mms.17765.Search in Google Scholar
Cebrian, E., Uriz, M.J., Garrabou, J., and Ballesteros, E. (2011). Sponge mass mortalities in a warming Mediterranean Sea: are cyanobacteria-harboring species worse off? PLoS One 6: e20211. https://doi.org/10.1371/journal.pone.0020211.Search in Google Scholar PubMed PubMed Central
Clark, J.S., Poore, A.G.B., Coleman, M.A., and Doblin, M.A. (2020). Local scale thermal environment and limited gene flow indicates vulnerability of warm edge populations in a habitat forming macroalga. Front. Mar. Sci. 7: 711, doi:https://dx.doi.org/10.3389/fmars.2020.00711.10.3389/fmars.2020.00711Search in Google Scholar
Coleman, M.A. and Wernberg, T. (2017). Forgotten underwater forests: the key role of fucoids on Australian temperate reefs. Ecol. Evol. 7: 8406–8418. https://doi.org/10.1002/ece3.3279.Search in Google Scholar PubMed PubMed Central
Connell, S.D., Russell, B.D., Turner, D.J., Shepherd, S.A., Kildea, T., Miller, D., Airoldi, L., and Cheshire, A. (2008). Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar. Ecol. Prog. Ser. 360: 63–72. https://doi.org/10.3354/meps07526.Search in Google Scholar
Cormaci, M., Furnari, G., Catra, M., Alongi, G., and Giaccone, G. (2012). Flora marina bentonica del Mediterraneo: Phaeophyceae. Boll. Accad. Gioenia Sci. Nat. Catania 45: 1–508.Search in Google Scholar
Draisma, S.G.A., Ballesteros, E., Rousseau, F., and Thibaut, T. (2010). DNA sequence data demonstrate the polyphyly of the genus Cystoseira and other Sargassaceae genera (Phaeophyceae). J. Phycol. 46: 1329–1345. https://doi.org/10.1111/j.1529-8817.2010.00891.x.Search in Google Scholar
Ercegović, A. (1952). Jadranske cistozire. Njihova morfologija, ekologija i razvitak. – Sur les Cystoseira adriatiques. Leur morphologie, écologie et évolution. Fauna et Flora Adriatica. Split: Institut za Oceanografiju i Ribarstvo.Search in Google Scholar
Fabrizzi, E., Scardi, M., Ballesteros, E., Benedetti-Cecchi, L., Cebrian, E., Ceccherelli, G., De Leo, F., Deidun, A., Guarnieri, G., Falace, A., et al.. (2020). Modeling macroalgal forest distribution at Mediterranean scale: present status, drivers of changes and insights for conservation and management. Front. Mar. Sci. 7: 20. https://doi.org/10.3389/fmars.2020.00020.Search in Google Scholar
Falace, A. and Bressan, G. (2006). Seasonal variations of Cystoseira barbata (Stackhouse) C. Agardh frond architecture. Hydrobiologia 555: 193–206. https://doi.org/10.1007/s10750-005-1116-2.Search in Google Scholar
Garrabou, J., Coma, R., Bensoussan, N., Bally, M., Chevaldonne, P., Cigliano, M., Diaz, D., Harmelin, J.G., Gambi, M.C., Kersting, D.K., et al.. (2009). Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob. Change Biol. 15: 1090–1103. https://doi.org/10.1111/j.1365-2486.2008.01823.x.Search in Google Scholar
Gómez Garreta, A., Barceló Martí, M.C., Ribera Siguan, M.A., and Rull LLuch, J. (2001). Cystoseira C. Agardh. In: Gómez-Garreta, A. (Ed.), Flora Phycologica Iberica, Fucales, Vol. 1. Murcia: Universidad de Murcia, pp. 99–166.Search in Google Scholar
Guidetti, P. and Sala, E. (2007). Community-wide effects of marine reserves in the Mediterranean Sea. Mar. Ecol. Prog. Ser. 335: 43–56. https://doi.org/10.3354/meps335043.Search in Google Scholar
Guiry, M.D., Guiry, M.D., and Guiry, G.M. (2022). AlgaeBase. World-wide electronic publication. Galway: National University of Ireland, Available at https://www.algaebase.org (Accessed 27 May 2022).Search in Google Scholar
Hereu, B., Mangialajo, L., Ballesteros, E., and Thibaut, T. (2008). On occurrence, structure and distribution of deep-water Cystoseira (Phaeophyceae) populations in the Port-Cros National Park (north-western Mediterranean). Eur. J. Phycol. 43: 263–273. https://doi.org/10.1080/09670260801930330.Search in Google Scholar
Hrs-Brenko, M. (1977). Oyster larvae and spat in Pomer Bay. Rapp. Comm. Int. Mer. Médit. 24: 155–157.Search in Google Scholar
Iveša, Lj. and Devescovi, M. (2014). Distribution and composition of stands along the west Istrian coast (northern Adriatic, Croatia) and comparison with historical data. In: Langar, H., Bouafif, C., and Ouerghi, A. (Eds.), Proceedings of the 5th Mediterranean Symposium on Marine Vegetation. Slovenia: Portorož, pp. 102–107.10.1016/j.marenvres.2015.03.008Search in Google Scholar
Iveša, Lj., Djakovac, T., and Devescovi, M. (2016). Long-term fluctuation in Cystoseira population along the west Istrian Coast (Croatia) related to eutrophication patterns in the northern Adriatic Sea. Mar. Pollut. Bull. 106: 162–173. https://doi.org/10.1016/j.marpolbul.2016.03.010.Search in Google Scholar PubMed
Khailov, K.M. (1979). Ontogenetic trends in morphogenetic parameters of Cystoseira barbata thalli. Bot. Mar. 22: 299–311. https://doi.org/10.1515/botm.1979.22.5.299.Search in Google Scholar
Khailov, K.M. and Firsov, Y.K. (1979). Morphophysiological analysis of the hierarchical structure of Cystoseira barbata thalli. Bot. Mar. 22: 333–345. https://doi.org/10.1515/botm.1979.22.5.299.Search in Google Scholar
Lüning, K. (1990). Seaweeds: their environment, biogeography, and ecophysiology. Wiley.Search in Google Scholar
Mačić, V., Antolić, B., Thibaut, T., and Svircev, Z. (2010). Distribution of the most common Cystoseira C. Agardh species (Heterokontophyta, Fucales) on the coast of Montenegro (South-east Adriatic Sea). Fresenius Environ. Bull. 19: 1191–1198.Search in Google Scholar
Mangialajo, L., Chiantore, M., and Cattaneo-Vietti, R. (2008). Loss of fucoid algae along a gradient of urbanisation, and structure of benthic assemblages. Mar. Ecol. Prog. Ser. 358: 63–74. https://doi.org/10.3354/meps07400.Search in Google Scholar
Mariani, S., Cefalì, M.E., Chappuis, E., Terradas, M., Pinedo, S., Torras, X., Jordana, E., Medrano, A., Verdura, J., and Ballesteros, E. (2019). Past and present of Fucales from shallow and sheltered shores in Catalonia. Reg. Stud. Mar. Sci. 32: 100824. https://doi.org/10.1016/j.rsma.2019.100824.Search in Google Scholar
Munda, I.M. (1979). Some Fucacean associations from the vicinity of Rovinj, Istrian coast, Northern Adriatic. Nova Hedwigia 31: 607–664.Search in Google Scholar
Munda, I.M. (1982). The effects of organic pollution on the distribution of fucoid algae from the Istrian coast (vicinity of Rovinj). Acta Adriat. 23: 329–337.Search in Google Scholar
Munda, I.M. (1993). Changes and degradation of seaweed stands in the Northern Adriatic. Hydrobiologia 260/261: 239–253. https://doi.org/10.1007/bf00049025.Search in Google Scholar
Munda, I.M. (2000). Long-term marine floristic changes around Rovinj (Istrian coast, North Adriatic) estimated on the basis of historical data from Paul Kuckuck’s field diaries from the end of the 19th century. Nova Hedwigia 71: 1–36. https://doi.org/10.1127/nova/71/2000/1.Search in Google Scholar
Oliver, E.C.J., Donat, M.G., Burrows, M.T., Moore, P.J., Smale, D.A., Alexander, L.V., Benthuysen, J.A., Feng, M., Gupta, A.S., Hobday, A.J., et al.. (2018). Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9: 1324. https://doi.org/10.1038/s41467-018-03732-9.Search in Google Scholar PubMed PubMed Central
Orfanidis, S. (1991). Temperature responses and distribution of macroalgae belonging to the warm-temperate Mediterranean-Atlantic distribution group. Bot. Mar. 34: 541–552. https://doi.org/10.1515/botm.1991.34.6.541.Search in Google Scholar
Orlando-Bonaca, M., Lipej, L., and Orfanidis, S. (2008). Benthic macrophytes as a tool for delineating, monitoring and assessing ecological status: the case of Slovenian coastal waters. Mar. Pollut. Bull. 56: 666–676. https://doi.org/10.1016/j.marpolbul.2007.12.018.Search in Google Scholar PubMed
Pećarević, M., Mikuš, J., Bratoš Cetinić, A., Dulčić, J., and Čalić, M. (2013). Introduced marine species in Croatian waters (Eastern Adriatic Sea). Mediterr. Mar. Sci. 14: 224–237. https://doi.org/10.12681/mms.383.Search in Google Scholar
Pecl, G.T., Araújo, M.B., Bell, J.D., Blanchard, J., Bonebrake, T.C., Chen, I.C., Clark, T.D., Colwell, R.K., Danielsen, F., Evengård, B., et al.. (2017). Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355: eaai9214.10.1126/science.aai9214Search in Google Scholar PubMed
Perkol-Finkel, S., Ferrario, F., Nicotera, V., and Airoldi, L. (2012). Conservation challenges in urban seascapes: promoting the growth of threatened species on coastal infrastructures. J. Appl. Ecol. 49: 1457–1466. https://doi.org/10.1111/j.1365-2664.2012.02204.x.Search in Google Scholar
Ribera, M.A., Gómez Garreta, A., Gallardo, T., Cormaci, M., Furnari, G., and Giaccone, G. (1992). Check-list of Mediterranean Seaweeds. I. Fucophyceae (Warming, 1884). Bot. Mar. 35: 109–130. https://doi.org/10.1515/botm.1992.35.2.109.Search in Google Scholar
Sadogurska, S.S. (2021). Unattached Cystoseira S. L. in the Black Sea: taxonomy of Gongolaria barbata f. repens comb. nov. Int. J. Algae 23: 293–304. https://doi.org/10.1615/interjalgae.v23.i3.80.Search in Google Scholar
Sadogurska, S.S., Neiva, J., Falace, A., Serrao, E.A., and Israel, A. (2021). The genus Cystoseira s.l. (Ochrophyta, Fucales, Sargassaceae) in the Black Sea: morphological variability and molecular taxonomy of Gongolaria barbata and endemic Ericaria crinita f. bosphorica comb. nov. Phytotaxa 480: 1–21. https://doi.org/10.11646/phytotaxa.480.1.1.Search in Google Scholar
Sala, E., Boudouresque, C.F., and Hamerlin-Vivien, M. (1998). Fishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82: 425–482. https://doi.org/10.2307/3546364.Search in Google Scholar
Sala, E., Kizilkaya, Z., Yildirim, D., and Ballesteros, E. (2011). Alien marine fishes deplete algal biomass in the Eastern Mediterranean. PLoS One 6: e17356. https://doi.org/10.1371/journal.pone.0017356.Search in Google Scholar PubMed PubMed Central
Sales, M. and Ballesteros, E. (2009). Shallow Cystoseira (Fucales: Ochrophyta) assemblages thriving in sheltered areas from Menorca (NW Mediterranean): relationships with environmental factors and anthropogenic pressures. Estuar. Coast Shelf Sci. 84: 476–482. https://doi.org/10.1016/j.ecss.2009.07.013.Search in Google Scholar
Serio, D. (1994). On the structure, typology and periodism of Cystoseira spinosa Sauvageau community and Cystoseira zosteroides C. Agardh community from Eastern coast of Sicily (Mediterranean Sea). Giorn. Bot. Ital. 128: 941–973. https://doi.org/10.1080/11263509409436463.Search in Google Scholar
Smale, D.A. and Wernberg, T. (2013). Extreme climatic event drives range contraction of a habitat-forming species. Proc. R. Soc. B 280: 20122829. https://doi.org/10.1098/rspb.2012.2829.Search in Google Scholar PubMed PubMed Central
Steneck, R.S., Graham, M.H., Bourque, B.J., Corbett, D., Erlandson, J.M., Estes, J.A., and Tegner, M.J. (2002). Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ. Conserv. 29: 436–459. https://doi.org/10.1017/S0376892902000322.Search in Google Scholar
Tamburello, L., Chiarore, A., Fabbrizzi, E., Colletti, A., Franzitta, G., Grech, D., Rindi, F., Rizzo, L., Savinelli, B., and Fraschetti, S. (2022). Can we preserve and restore overlooked macroalgal forests? Sci. Total Environ. 806. https://doi.org/10.1016/j.scitotenv.2021.150855.Search in Google Scholar PubMed
Thibaut, T., Blanfuné, A., Boudouresque, C.F., and Verlaque, M. (2015). Decline and local extinction of Fucales in the French Riviera: the harbinger of future extinction? Mediterr. Mar. Sci. 16: 206–224.10.12681/mms.1032Search in Google Scholar
Thibaut, T., Blanfuné, A., Boudouresque, C.-F., Cottalorda, J.-M., Hereu, B., Susini, M.-L., and Verlaque, M. (2016). Unexpected temporal stability of Cystoseira and Sargassum forests in Port-Cros, one of the oldest Mediterranean Marine National Parks. Cryptogam. Algol. 37: 61–90.10.7872/crya/v37.iss1.2016.61Search in Google Scholar
Verdura, J., Sales, M., Ballesteros, E., Cefalì, M.E., and Cebrian, E. (2018). Restoration of a canopy-forming alga based on recruitment enhancement: methods and long-term success assessment. Front. Plant Sci. 9: 1832. https://doi.org/10.3389/fpls.2018.01832.Search in Google Scholar PubMed PubMed Central
Verdura, J., Santamaria, J., Ballesteros, E., Smale, D.A., Cefali, M.E., Golo, R., de Caralt, S., Verges, A., and Cebrian, E. (2021). Local-scale climatic refugia offer sanctuary for a habitat-forming species during a marine heatwave. J. Ecol. 109: 1758–1773. https://doi.org/10.1111/1365-2745.13599.Search in Google Scholar
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