Rapid invasion of the non-indigenous brown alga Stypopodium schimperi in the Adriatic Sea

PDF
Published: Jul 8, 2025
DOI: https://doi.org/10.12681/mms.38412
Keywords:
invasive algae Adriatic Sea Stypopodium schimperi
PETRA LUCIC JELIĆ
Institute of Oceanography and Fisheries, Šetalište I. Meštrovića 63, 21 000 Split, Croatia
IVAN CVITKOVIĆ
Institute of Oceanography and Fisheries, Šetalište I. Meštrovića 63, 21 000 Split, Croatia
JELENA NEJAŠMIĆ
Institute of Oceanography and Fisheries, Šetalište I. Meštrovića 63, 21 000 Split, Croatia
SVJETLANA CVJETAN
Institute of Oceanography and Fisheries, Šetalište I. Meštrovića 63, 21 000 Split, Croatia
MARIJA DESPALATOVIĆ
Institute of Oceanography and Fisheries, Šetalište I. Meštrovića 63, 21 000 Split, Croatia
MAJA MUCKO
University of Zagreb, Faculty of Science, Biology Department, Marulićev trg 20, 10000 Zagreb, Croatia
MARIJA KVESIĆ IVANKOVIĆ
Institute of Oceanography and Fisheries, Šetalište I. Meštrovića 63, 21 000 Split, Croatia
ANTE ŽULJEVIĆ
Institute of Oceanography and Fisheries, Šetalište I. Meštrovića 63, 21 000 Split, Croatia
Abstract

In this study, we report the first record of the brown alga Stypopodium schimperi in the Adriatic Sea, which also represents the northernmost occurrence of this Lessepsian species within the Mediterranean. Species identification was confirmed through morphological examination and molecular analyses based on genotyping of the chloroplast genes rbcL, psbA, and psaA. During a 3-year observation period, S. schimperi demonstrated a vigorous increase in both coverage and spatial distribution. Starting from a few observed thalli in autumn 2020, coverage reached 100% over a large area. Consequently, this resulted in a drastic reduction of native macroalgae on rocky bottoms, mostly at depths of 5-20 m, which we quantified via photo-quadrat analyses along a gradient of its coverage. In conclusion, this non-indigenous species has the potential to become one of the most invasive in the Adriatic Sea, with a high likelihood of spreading further into the northwestern Mediterranean.

Article Details
  • Section
  • Research Article

Authors who publish with this journal agree to the following terms:

  1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
  2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
  3. Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Downloads
Download data is not yet available.
References
Bardamaskos, G., Tsiamis, K., Panayotidis, P., Megalofonou, P., 2009. New records and range expansion of alien fish and macroalgae in Greek waters (south-east Ionian Sea). Marine Biodiversity Records, 2, 9.
Baza pokazatelja, 2025. Baza podataka i pokazatelja stanja morskog okoliša, marikulture i ribarstva. https://vrtlac.izor. hr/ords/bazapokpub/bindex (Accessed on 20 May 2025).
Bianchi, C.N., Pronzato, R., Cattaneo-Vietti, R., Benedetti Cecchi, L., Morri, C. et al., 2003. Hard bottoms. p. 185-216. In: Mediterranean marine benthos: a manual of methods for its sampling and study. Gambi, M.C., Dappiano, M. (Eds). Biologia Marina Mediterranea, Genova.
Bitar, G., Harmelin, J.G., Verlaque, M., Zibrowius, H., 2000. Sur la flore marine benthique suppose lessepsienne de la côte libanaise. Cas particulier de Stypopodium schimperi. p. 97-100. In: Proceedings of the first Mediterranean symposium on marine vegetation, Ajaccio, 3-4 October 2000. Regional Activity Centre for Specially Protected Areas (RAC/ SPA), Tunis.
Bitar, G., Ramos-Espla, A.A., Ocana, O., Sghaier, Y.R., Forcada, A. et al., 2017. The introduced marine macroflora of Lebanon and its distribution on the Levantine coast. Mediterranean Marine Science, 18 (1), 138-155.
Bittner, L., Payri, C.E., Couloux, A., Cruaud, C., de Reviers, B. et al., 2008. Molecular phylogeny of the Dictyotales and their position within the Phaeophyceae, based on nuclear, plastid and mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution, 49 (1), 211-226.
Bottalico, A., Tursi, A., Mastrototaro, F., Chimienti, G., Mincuzzi, A., 2024. Eastward spreading of the invasive Rugulopteryx okamurae (Heterokontophyta, Dictyotales) in the Mediterranean: first record in the Adriatic Sea. Mediterranean Marine Science, 25 (3), 698-708.
Borriglione, M., Ruitton, S., Boyer, F., Thibault, D., Blanfuné, A. et al., 2024. Impact of the invasive brown alga Rugulopteryx okamurae on the benthic communities in the Northwestern Mediterranean Sea. Estuarine Coastal and Shelf Science, 310 (1-2), 109010.
Boudouresque, C.F., Verlaque M., 2012. An overview of species introduction and invasion processes in marine and coastal lagoon habitats. Cahiers de Biologie Marine, 53 (3), 309-317.
Boudouresque, C.F., Verlaque, M., 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin, 44 (1), 32-38.
Burrowes, R., Rousseau, F., Müller, D.G., de Reviers, B., 2003. Taxonomic placement of Microzonia (Phaeophyceae) in the Syringodermatales based on the rbcL and 28S nrDNA sequences. Cryptogamie Algologie, 24 (1), 63-73.
Çinar, M.E., Bilecenoglu, M., Yokes, M.B., Öztürk, B., Taskin, E. et al., 2021. Current status (as of end of 2020) of marine alien species in Turkey. Plos One, 16 (5).
Civitarese, G., Gačić, M., Lipizer, M., Eusebi Borzelli, G.L., 2010. On the impact of the Bimodal Oscillating System (BiOS) on the biogeochemistry and biology of the Adriatic and Ionian Seas (Eastern Mediterranean). Biogeosciences, 7 (12), 3987-3997.
Davidson, A.D., Campbell, M.L., Hewitt, C.L., Schaffelke, B., 2015. Assessing the impacts of nonindigenous marine macroalgae: an update of current knowledge. Botanica Marina, 58 (2), 55-79.
Dimitriadis, C., Fournari-Konstantinidou, I., Sourbès, L., Koutsoubas, D., Katsanevakis, S., 2021. Long Term Interactions of Native and Invasive Species in a Marine Protected Area Suggest Complex Cascading Effects Challenging Conservation Outcomes. Diversity, 13 (2), 71.
Dragičević, B., Ugarković, P., Krželj, M., Zurub, D., Dulčić, J., 2021. New record of Pterois cf. miles (Actinopterygii: Scorpaeniformes: Scorpaenidae) from the eastern middle Adriatic Sea (Croatian waters): Northward expansion. Acta Ichthyologica Et Piscatoria, 51(4), 379-383.
Draisma, S.G.A., Prud’Homme van Reine, W.F., Stam, W.T., Olsen, J.L., 2001. A Reassessment of Phylogenetic Relationships within the Phaeophyceae Based on Rubisco Large Subunit and Ribosomal DNA Sequences. Journal of Phycology, 37 (4), 586-603.
Elton C.S., 1958. The ecology of invasions by animals and plants. Methuen publ. Reprinted 2000 by University of Chicago Press, 196 pp.
Fridley, J.D., Stachowicz, J.J., Naeem, S., Sax, D.F., Seabloom, E.W. et al., 2007. The invasion paradox: Reconciling pattern and process in species invasions. Ecology, 88, 3-17.
Gačić, M., Eusebi Borzelli, G.L., Civitarese, G., Cardin, V., Yari, S., 2010. Can internal processes sustain reversals of the ocean upper circulation? The Ionian Sea example. Geophysical Research Letters, 37(9).
Galanidi, M., Aissi, M., Ali, M., Bakalem, A., Bariche, M. et al., 2023. Validated Inventories of Non-Indigenous Species (NIS) for the Mediterranean Sea as Tools for Regional Policy and Patterns of NIS Spread. Diversity, 15 (9).
García-Gómez, J.C., Sempere-Valverde, J., González, A.R., Martínez-Chacón, M., Olaya-Ponzone, L. et al., 2020. From exotic to invasive in record time: The extreme impact of Rugulopteryx okamurae (Dictyotales, Ochrophyta) in the strait of Gibraltar. Science of the Total Environment, 704.
Gerwick, W.H., Fenical, W., Fritsch, N., Clardy, J., 1979. Stypotriol and stypoldione; ichthyotoxins of mixed biogenesis from the marine alga Stypopodium zonale. Tetrahedron Letters, 20 (2), 145-148.
Gerwick, W.H., Fenical, W., 1981. Ichthyotoxic and cytotoxic metabolites of the tropical brown alga Stypopodium zonale (Lamouroux) Papenfuss. The Journal of Organic Chemistry, 46 (1), 22-27.
Guiry, M.D., Guiry, G.M., 2025. AlgaeBase. World-wide electronic publication, University of Galway. https://www.algaebase. org (Accessed on 20 May 2025).
Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q., Vinh, L.S., 2018. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution, 35 (2), 518-522.
Hoffman, R., 2014. Alien Benthic Algae and Seagrasses in the Mediterranean Sea and Their Connection to Global Warming p. 159-181. In: The Mediterranean Sea: Its history and present challenges. Goffredo, S., Dubinsky, Z. (Eds). Springer Science+Business Media, Dordrecht.
Hoffman, R., Dubinsky, Z., 2010. Invasive and Alien Rhodophyta in the Mediterranean and along the Israeli Shores p. 45-60. In: Red Algae in the Genomic Age. Seckbach, J., Chapman, D.J. (Eds). Springer Science+Business Media, Dordrecht.
Hoffman, R., Shemesh, E., Ramot, M., Dubinsky, Z., Pinchasov- Grinblat, Y. et al., 2011. First record of the Indo-Pacific seaweed Codium arabicum Kutz. (Bryopsidales, Chlorophyta) in the Mediterranean Sea. Botanica Marina, 54 (5), 487-495.
Inkscape, 2020. Inkscape. https://inkscape.org
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A., Jermiin, L.S., 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14 (6), 587-589.
Katsanevakis, S., Zenetos, A., Macic, V., Beqiraj, S., Poursanidis, D. et al., 2011. Invading the Adriatic: spatial patterns of marine alien species across the Ionian-Adriatic boundary. Aquatic Biology, 13 (2), 107-118.
Katsanevakis, S., Zenetos, A., Corsini-Foka, M., Tsiamis, K., 2020. Biological Invasions in the Aegean Sea: Temporal Trends, Pathways, and Impacts p. 1-34. In: The Handbook of Environmental Chemistry. Anagnostou, C.L., A.G., Kostianoy, I.D., Mariolakos, P., Panayotidis, M., Soilemezidou et al. (Eds). Springer, Berlin, Heidelberg.
Kleitou, P., Agius, D., Akalin, S., Albano, M., Ammar, I. A. et al., 2025. New records of introduced species in the Mediterranean Sea (February 2025). Mediterranean Marine Science, 26 (1), 175-198.
La Rivière M., Michez N., Delavenne J., Andres S., Fréjefond C. et al., 2021. Fiches descriptives des biocénoses benthiques de Méditerranée. Ref. UMS PatriNat (OFB-CNRSMNHN), Paris, 660 pp.
Lejeusne, C., Chevaldonné, P., Pergent-Martini, C., Boudouresque, C.F., Pérez, T., 2010. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends in Ecology & Evolution, 25 (4), 250-260.
Lipej, L., Kovačić, M., Dulčić, J., 2022. An analysis of Adriatic ichthyofauna-ecology, zoogeography, and conservation status. Fishes, 7 (2), 58.
Lučić, P., Nejašmić, J., Cvjetan, S., Despalatović, M., Cvitković, I. et al., 2022. First record of the non-indigenous brown alga Stypopodium schimperi in the Adriatic Sea. p. 103-104. In: Proceedings of the 2nd Mediterranean Symposium on the Non-Indigenous Species, Genova, Italy, 22-23 September. 2022. Bouafif C., Ouerghi Α. (Eds). SPA/RAC publi., Tunis, 133 p.
Lundberg, B., Payiatas, G., Argyrou, M., 2013. Notes on the diet of the Lessepsian migrant herbivorous fishes, Siganus luridus and S. rivulatus, in Cyprus. Israel Journal of Zoology, 45 (1), 127-134.
Marchini A., Ferrario J., Sfriso A., Occhipinti-Ambroggi A., 2015. Current status and trends of biological invasions in the Lagoon of Venice, a hotspot of marine NIS introductions in the Mediterranean Sea. Biological Invasions, 17, 2943-2962.
Mayhoub, H., Billard, C., 1991. Contribution à la connaissance d’un Stypopodium (Dictyotales, Phaeophyceae) installé récemment sur les côtes syriennes. Cryptogamie Algologie, 12 (2), 125-136.
Meusnier, I., Valero, M., Olsen, J.L., Stam, W.T., 2004. Analysis of rDNA ITS1 indels in Caulerpa taxifolia (Chlorophyta) supports a derived, incipient species status for the invasive strain. European Journal of Phycology, 39 (1), 83-92.
Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D. et al., 2020. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Molecular Biology and Evolution, 37 (5), 1530-1534.
Nejašmić, J., Lučić, P., Cvitković, I., Despalatović, M., Žužul, I. et al., 2021. Spreading of non-indigenous crab Percnon gibbesi (H. Milne Edwards, 1853) in the Croatian part of the Adriatic Sea p. 88-88. In: 4th Croatian Symposium on Invasive Species, Croatian Ecological Society, Zagreb.
Occhipinti Ambrogi, A., 2000. Biotic invasions in a Mediterranean lagoon. Biological Invasions, 2, 165-176. Pastor, F., Valiente, J.A., Palau, J.L., 2018. Sea Surface Temperature in the Mediterranean: Trends and Spatial Patterns (1982-2016). Pure and Applied Geophysics, 175 (11), 4017-4029.
Pećarević, M., Mikuš, J., Bratoš Cetinić, A., Dulčić, J., Čalić, M., 2013. Introduced marine species in Croatian waters (Eastern Adriatic Sea). Mediterranean Marine Science, 14 (1), 224-237.
Poulain, P.M., 2001. Adriatic Sea surface circulation as derived from drifter data between 1990 and 1999. Journal of Marine Systems, 29 (1-4), 3-32. Rambaut, A., 2018. Molecular Evolution, Phylogenetics and Epidemiology. FigTree v.1.4.4., Software, http://tree.bio. ed.ac.uk/software/figtree
Ruitton, S., Blanfune, A., Boudouresque, C.F., Guillemain, D., Michotey, V. et al., 2021. Rapid Spread of the Invasive Brown Alga Rugulopteryx okamurae in a National Park in Provence (France, Mediterranean Sea). Water, 13 (16).
Sansón, M., Reyes, J., Afonso-Carrillo, J., Muñoz, E., 2002. Sublittoral and deep-water red and brown algae new from the Canary Islands. Botanica Marina, 45 (1), 35-49.
Sfriso A., Wolf M.A., Buosi A., Sciuto K., Sfriso A.A., 2023. Alien macroalgal rearrangement in the soft substrata of the Venice Lagoon (Italy): Impacts, threats, time and future trends. Sustainability, 1 (8256), 1-15.
Shaltout, M., 2019. Recent sea surface temperature trends and future scenarios for the Red Sea. Oceanologia, 61 (4), 484-504.
Shan, T.F., Pang, S.J., Zhang, Y.R., Yakovleva, I.M., Skriptsova, A.V., 2011. An AFLP-based survey of genetic diversity and relationships of major farmed cultivars and geographically isolated wild populations of Saccharina japonica (Phaeophyta) along the northwest coasts of the Pacific. Journal of Applied Phycology, 23 (1), 35-45.
SOMLIT, 2021. Service d′Observation en Milieu Littoral. https://www.somlit.fr (Accessed on 20 May 2025).
Spanier, E., Galil, B.S., 1991. Lessepsian migration - a continuous biogeographical process. Endeavour, 15 (3), 102-106.
Streftaris, N., Zenetos, A., 2006. Alien Marine Species in the Mediterranean - the 100 ‘Worst Invasives’ and their Impact. Mediterranean Marine Science, 7 (1), 87-118.
Tsiamis, K., Montesanto, B., Panayotidis, P., Katsaros, C., Verlaque, M., 2010. Updated records and range expansion of alien marine macrophytes in Greece (2009). Mediterranean Marine Science, 11 (1), 61-80.
Tsiamis, K., Palialexis, A., Stefanova, K., Gladan, Ž.N., Skejić, S. et al., 2019. Non-indigenous species refined national baseline inventories: A synthesis in the context of the European Union’s Marine Strategy Framework Directive. Marine Pollution Bulletin, 145, 429-435.
van der Loos, L.M., Bafort, Q., Bosch, S., Ballesteros, E., Barbara, I. et al., 2024. Non-indigenous seaweeds in the Northeast Atlantic Ocean, the Mediterranean Sea and Macaronesia: a critical synthesis of diversity, spatial and temporal patterns. European Journal of Phycology, 59 (2), 127-156.
Verlaque, M., Boudouresque, C.F., 1991. Stypopodium schimperi (Buchinger ex Kützing) Verlaque et Boudouresque comb. nov. (Dictyotales, Fucophyceae), algue de mer Rouge récemment apparue en Méditerranée. Cryptogamie Algologie, 12 (3), 195-211.
Verlaque, M., Ruitton, S., Mineur, F., Boudouresque, C.F., 2015. CIESM Atlas of Exotic Species in the Mediterranean Vol.4. Macrophytes. CIESM, Monaco, 364 pp.
Vieira, C., Steen, F., D’Hondt, S., Bafort, Q., Tyberghein, L. et al., 2021. Global biogeography and diversification of a group of brown seaweeds (Phaeophyceae) driven by clade-specific evolutionary processes. Journal of Biogeography, 48 (4), 703-715.
Yoon, H.S., Hackett, J.D., Bhattacharya, D., 2002. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proceedings of the National Academy of Sciences, 99 (18), 11724-11729.
Zenetos, A., Albano, P.G., Garcia, E.L., Stern, N., Tsiamis, K. et al., 2022. Established non-indigenous species increased by 40% in 11 years in the Mediterranean Sea. Mediterranean Marine Science, 23 (1), 196-212.
Žuljević, A., Antolić, B., Despalatović, M., Onofri, V., 2004. The spread of the invasive variety of Caulerpa racemosa in the Adriatic Sea p. 574. In: Rapport du 37 Congres de la Commission internationale pour l’exploration scientifique de la Mer Méditerranée, CIESM.
Žuljević, A., Despalatović M., Antolić B., Cvitković I., Nikolić V. et. al., 2009. Morska bioraznolikost otoka Biševa i jugoistočne strane otoka Visa - Stručna podloga za održivo upravljanje. GEF/UNDP COAST, Project report (in Croatian), 60 pp.
Žuljević, A., Cvitković, I., Despalatović, M., Lučić, P., Žunec, A., 2019. Decline of Caulerpa taxifolia in the Adriatic Sea. p. 82-87. In: Proceedings of the 1st Mediterranean Symposium on the Non-Indigenous Species, Antalya, Turkey, 17- 18 January 2019. Langar H., Ouerghi A., (Eds)., SPA/RAC publi., Tunis, 116 p.
Most read articles by the same author(s)