Healthy thalli of the invasive seaweed Rugulopteryx okamurae (Phaeophyceae) being massively dragged into deep-sea bottoms by the Mediterranean Outflow Water

REFERENCES

• Altamirano M., De la Rosa J., Carmona R., Zanolla M. & Muñoz A.-R. 2019. Macroalgas invasoras en las costas andaluzas. Algas 55e: 10–13. ISSN:1695-8160.
   Google Scholar
• Altamirano M., De la Rosa J., Kawai H., Hanyuda T., Carmona R., Zanolla M. & Muñoz A.-R. 2021. Cryptic introduction and invasion of Rugulopteryx okamurae (Dictyotales, Ochrophyta) at the Strait of Gibraltar: a real threat to the Mediterranean ecosystems. 12th International Phycological Congress (IPC2021), Chile 22–26 March 2021, abstract, p. 17.
   Google Scholar
• Anton A., Geraldi N., Lovelock C., Apostololaki E.T., Bennett S., Cebrian J., Krause-Jensen D., Marbà N., Martinetto P., Pandolfi M.J. et al. 2019. Global ecological impacts of marine exotic species. Nature Ecology & Evoution 3: 787–800. DOI: 10.1038/s41559-019-0851-0.
   PubMed Web of Science ®Google Scholar
• Babb I., Conroy C., Govert N., Schneeberger C., Walton O., Auster P. & Zajac T. 2021. Preliminary map products from an ecological characterization of Eastern Long Island sound and Fishers Island sound regions: Long Island sound cable fund phase II survey area. Technical Report. 42 pp. DOI: 10.13140/RG.2.2.16488.60166.
   Google Scholar
• Bellanco M.J. & Sánchez-Leal R. 2016. Spatial distribution and intra-annual variability of water masses on the Eastern Gulf of Cadiz seabed. Continental Shelf Research 128: 26–35. DOI: 10.1016/j.csr.2016.09.001.
   Web of Science ®Google Scholar
• Bogaert K., Beeckman T. & De Clerck O. 2016. Abiotic regulation of growth and fertility in the sporophyte of Dictyota dichotoma (Hudson) J.V. Lamouroux (Dictyotales, Phaeophyceae). Journal of Applied Phycology 28: 2915–2924. DOI: 10.1007/s10811-016-0801-z.
   Web of Science ®Google Scholar
• Borum J., Pedersen M., Krause-Jensen D., Christensen P.B. & Nielsen K. 2002. Biomass, photosynthesis and growth of Laminaria saccharina in a high-arctic fjord, NE Greenland. Marine Biology 141: 11–19−.
   Web of Science ®Google Scholar
• CAGPDS 2019. Programa de gestión sostenible del medio marino. Consejeria de Agricultura, Ganaderia, Pesca y Desarrollo Sostenible, Informe Regional 2019, Sevilla, Spain. 151 pp. https://www.juntadeandalucia.es/medioambiente/portal/documents/20151/3227240/informe_anual_medio_marino_2019.pdf/eed625c9-1488-292b-c607-bb282a2ee83e?t=1606215965664
   Google Scholar
• Casal-Porras I., Zubía E. & Brun F.G. 2021. Dilkamural: a novel chemical weapon involved in the invasive capacity of the alga Rugulopteryx okamurae in the Strait of Gibraltar. Estuarine, Coastal & Shelf Science 257: Article 107398. DOI: 10.1016/j.ecss.2021.107398.
   Web of Science ®Google Scholar
• Ceccherelli G. & Cinelli F. 1999. The role of vegetative fragmentation in dispersal of the invasive alga Caulerpa taxifolia in the Mediterranean. Marine Ecology Progress Series 182: 299–303. DOI: 10.3354/meps182299.
   Web of Science ®Google Scholar
• Cecere E., Petrocelli A. & Verlaque M. 2011. Vegetative reproduction by multicellular propagules in Rhodophyta: an overview. Marine Ecology 32: 419–437. DOI: 10.1111/j.1439-0485.2011.00448.x.
   Web of Science ®Google Scholar
• Celis-Plá P.S.M., Hall-Spencer J.M., Horta P.A., Milazzo M., Korbee N., Cornwall C.E. & Figueroa F.L. 2015. Macroalgal responses to ocean acidification depend on nutrient and light levels. Frontiers in Marine Science 2: Article 26.
   Google Scholar
• de la Torriente A., Serrano A., Fernández-Salas L.M., García M. & Aguilar R. 2018. Identifying epibenthic habitats on the Seco de los Olivos Seamount: species assemblages and environmental characteristics. Deep-Sea Research I 135: 9–22. DOI: 10.1016/j.dsr.2018.03.01.
   Google Scholar
• Dunton K.H. & Schell D.M. 1986. Seasonal carbon budget and growth of Laminaria solidungula in the Alaskan High Arctic. Marine Ecology Progress Series 31: 57–66−.
   Web of Science ®Google Scholar
• Eilers P.H.C. & Peeters J.C.H. 1988. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Model 42: 199–215. DOI:10.1016/0304-3800(88)90057-9.
   Web of Science ®Google Scholar
• El Aamri F., Idhalla M. & Tamsouri M.N. 2018. Occurrence of the invasive brown seaweed Rugulopteryx okamurae (E.Y.Dawson) I.K.Hwang, W.J.Lee & H.S.Kim (Dictyotales, Phaeophyta) in Morocco (Mediterranean Sea). Mediterranean Fisheries and Aquaculture Research 1: 92–96.
   Google Scholar
• Faria J., Prestes A.C.L., Moreu I., Martins G.M., Neto A.I. & Cacabelos E. 2022. Arrival and proliferation of the invasive seaweed Rugulopteryx okamurae in NE Atlantic islands. Botanica Marina 65: 45–50. DOI: 10.1515/bot-2021-0060.
   Web of Science ®Google Scholar
• Figueroa F., Vega J., Gómez-Valderrama M., Korbee N., Mercado J.M., Bañares E. & Flores A. 2020. Invasión de la especie exótica Rugulopteryx okamurae en Andalucía I: estudios preliminares de la actividad fotosintética. Algas 56: 35–46. ISSN: 1695-8160.
   Google Scholar
• García Lafuente J. & Ruiz J. 2007. The Gulf of Cádiz pelagic ecosystem: a review. Progress in Oceanography 74: 228–251. .
   Web of Science ®Google Scholar
• García-Gómez J.C., Sempere-Valverde J., Ostalé-Valriberas E., Martínez M., Olaya-Ponzone L., Roi A., Espinosa F., Sánchez-Moyano E., Megina C. & Parada J.A. 2018. Rugulopteryx okamurae (E.Y. Dawson) I.K. Hwang, W.J. Lee & H.S. Kim (Dictyotales, Ochrophyta), alga exótica “explosiva” en el estrecho de Gibraltar. Observaciones preliminares de su distribución e impacto. Almoraima 49: 97–113.
   Google Scholar
• García-Gómez J.C., Sempere-Valverde J., Roi A., Martínez-Chacón M., Oloya-Ponzone L., Sánchez-Moyano E., Ostalé-Valriberas E. & Megina C. 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: Article 135408. DOI: 10.1016/j.scitotenv.2019.135408.
   PubMed Web of Science ®Google Scholar
• Iñiguez C., Carmona R., Lorenzo M.R., Niell F.X., Wiencke C. & Gordillo F.J.L. 2016a. Increased CO2 modifies the carbon balance and the photosynthetic yield of two common Arctic brown seaweeds: Desmarestia aculeata and Alaria esculenta. Polar Biology 39: 1979–1991. DOI: 10.1007/s00300-015-1724-x.
   Web of Science ®Google Scholar
• Iñiguez C., Carmona R., Lorenzo M.R., Niell F.X., Wiencke C. & Gordillo F.J.L. 2016b. Increased temperature, rather than elevated CO2, modulates the carbon assimilation of the Arctic kelps Saccharina latissima and Laminaria solidungula. Marine Biology 163: Article 248. DOI: 10.1007/s00227-016-3024-6.
   Web of Science ®Google Scholar
• Kain J.M. & Destombe C. 1995. A review of the life history, reproduction and phenology of Gracilaria. Journal of Applied Phycology 7: 269–281.
   Web of Science ®Google Scholar
• Klein J. & Verlaque M. 2008. The Caulerpa racemosa invasion: a critical review. Marine Pollution Bulletin 56: 205–225. DOI: 10.1016/j.marpolbul.2007.09.043.
   PubMed Web of Science ®Google Scholar
• Krause-Jemsen D. & Duarte M.C. 2016. Substantial role of macroalgae in marine carbon sequestration. Nature Geoscience 9: 737–742. DOI: 10.1038/NGEO2790.
   Web of Science ®Google Scholar
• Krueger-Hadfield S.A., Kollars N.M., Byers J.E., Greig T.W., Hammann M., Murray D.C., Murren C.J., Strand A.E., Terada R., Weinberger F. et al. 2016. Invasion of novel habitats uncouples haplo-diplontic life cycles. Molecular Ecology 25: 3801–3816. DOI: 10.1111/mec.13718.
   PubMed Web of Science ®Google Scholar
• Kurata K., Taniguchi K., Shiraishi K. & Suzuki M. 1989. Structures of secospatane-type diterpenes with feeding-deterrent activity from the brown alga Dilophus okamurai. Tetrahedron Letters 30: 1567–1570. DOI: 10.1016/S0040-4039(00)99521.
   Web of Science ®Google Scholar
• Lee I.K. & Kang J.A. 1986. A check list of marine algae in Korea. Korean Journal of Phycology 1: 311–325.
   Google Scholar
• Li H., Scheschonk L., Heinrich S., Valentin K., Harms L., Glöckner G., Corre E. & Bischof K. 2020. Transcriptomic responses to darkness and the survival strategy of the kelp Saccharina latissima in the early polar night. Frontiers in Marine Sciences 7: Article 592033.
   Web of Science ®Google Scholar
• Llave E., Hernández-Molina F.J., García M., Ercilla G., Roque C., Juan C., Mena A., Preu B., Van Rooij D., Rebesco M. et al. 2019. Contourites along the Iberian continental margins: conceptual and economic implications. Geological Society Special Publication 476: 403–436. DOI: 10.1144/SP476-2017-46.
   Google Scholar
• Lüning K. 1990. Seaweeds: their environment, biogeography, and ecophysiology. Wiley. WileyInterscience, New York, USA. xiii + 527 pp.
   Google Scholar
• MITECO 2021. EU non-native organism risk assessment scheme: Rugulopteryx okamurae (E.Y. Dawson) I.K. Hwang, W.J. Lee & H.S. Kim 2009. Ministerio para transición ecológica y reto demográfico, Spain, and CIRCABC, European Union. https://circabc.europa.eu/sd/a/3ea80df2-56d7-4c1f-80f7-ee8d3e91bb8a/Rugulopteryx_okamurae_final_20210413.pdf
   Google Scholar
• Muñoz A.R., Martin-Taboada A., De la Rosa J., Carmona R., Zanolla M. & Altamirano M. 2019. La modelación de la distribución de especies como herramienta en la gestión de invasiones biológicas en el medio marino: el caso de Rugulopteryx okamurae (Dictyotaceae, Ochrophyta) en el Mediterráneo. Algas 55: 37–40.
   Google Scholar
• Navarro G., Ruiz J., Huertas I.E., García C.M., Criado Aldeanueva F. & Echevarría F. 2006. Basin scale structures governing the position of the deep fluorescence maximum in the Gulf of Cádiz. Deep Sea Research II 53: 1261–1281. DOI: 10.1016/j.dsr2.2006.04.013
   Web of Science ®Google Scholar
• Ocaña Ó., Afonso-Carrillo J. & Ballesteros E. 2016. Massive proliferation of a dictyotalean species (Phaeophyceae, Ochrophyta) through the Strait of Gibraltar (research note). Revista de la Academia Canaria de Ciencias 28: 165–170.
   Google Scholar
• Peters E. & Thomas D.N. 1996. Prolonged darkness and diatom mortality I: marine Antarctic species. Journal of Experimental Marine Biology and Ecology 207: 25–41.
   Web of Science ®Google Scholar
• Ramirez-Llodra E., Rinde E., Hege Gundersen H., Christie H., Fagerli C.W., Fredriksen S., Gitmark J.K., Norling K., Walday M.G. & Norderhaug K.M. 2016. A snap shot of the short-term response of crustaceans to macrophyte detritus in the deep Oslofjord. Scientific Reports 6: Article 23800. DOI: 10.1038/srep23800.
   PubMed Web of Science ®Google Scholar
• R Core Team 2020. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
   Google Scholar
• Rosas-Guerrero J., Meco Y.E. & Altamirano M. 2018. Could Rugulopteryx okamurae (Dictyotales, Ochrophyta) have been introduced by ballast waters? Algas 54: 52.
   Google Scholar
• Sánchez-Leal R., Bellanco M.J., Fernández-Salas L.M., García-Lafuente J., Gasser-Rubinat M., González-Pola C., Hernández-Molina F.J., Pelegrí J.L., Peliz A., Relvas P. et al. 2017. The Mediterranean overflow in the Gulf of Cadiz: a rugged journey. Science Advances 3: Article eaao0609. DOI: 10.1126/sciadv.aao0609.
   Google Scholar
• Schneider C.A., Rasband W.S. & Eliceiri K.W. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675.
   PubMed Web of Science ®Google Scholar
• Schreiber U., Schliwa U. & Bilger W. 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10: 51–62. DOI: 10.1007/BF00024185.
   PubMed Web of Science ®Google Scholar
• Sempere-Valverde J., Ostalé-Valriberas E., Maestre M., González-Aranda R., Bazairi H. & Espinosa F. 2021. Impacts of the non-indigenous seaweed Rugulopteryx okamurae on a Mediterranean coralligenous community (Strait of Gibraltar): the role of long-term monitoring. Ecological Indicators 121: Article 107135. DOI: 10.1016/j.ecolind.2020.107135.
   Web of Science ®Google Scholar
• Silva P.C., Meñez E.G. & Moe R.L. 1987. Catalogue of the benthic marine algae of the Philippines. Smithsonian Contributions to Marine Sciences 27: 1–179. DOI: 10.5479/si.1943667X.27.1.
   Google Scholar
• Suchanek T.H., Williams S.L., Ogden J.O., Hubbard D.K. & Gill P. 1985. Utilization of shallow-water seagrass detritus by Caribbean deep-sea macrofauna: δ13C evidence. Deep-Sea Research Part A 35: 201–214 . DOI:10.1016/0198-0149(85)90028-7.
   Google Scholar
• Suzuki M., Yamada H. & Kurata K. 2002. Dictyterpenoids A and B, two novel diterpenoids with feeding-deterrent activity from the brown alga Dilophus okamurae. Journal of Natural Products 65: 121–125. DOI: 10.1021/np010234b.
   PubMed Web of Science ®Google Scholar
• Thomsen M.S. 2020. Indiscriminate data aggregation in ecological meta-analysis underestimates impacts of invasive species. Nature Ecology & Evolution 4: 312–314. DOI: 10.1038/s41559-020-1117-6.
   PubMed Web of Science ®Google Scholar
• Trevathan-Tackett S., Kelleway J., Macreadie P.I., Beardall J., Ralph P. & Bellgrove A. 2015. Comparison of marine macrophytes for their contributions to blue carbon sequestration. Ecology 96: 3043–3057. DOI: 10.1890/15-0149.1.
   PubMed Web of Science ®Google Scholar
• Tsiamis K., Azzurro E., Bariche M., Çinar M.E., Crocetta F., De Clerck O., Galil B., Gómez F., Hoffman R., Jensen K.R. et al. 2020. Prioritizing marine invasive alien species in the European Union through horizon scanning. Aquatic Conservation: Marine and Freshwater Ecosystems 30: 794–845. DOI: 10.1002/aqc.3267.
   Web of Science ®Google Scholar
• Urra J., Palomino D., Lozano P., González-García E., Farias C., Mateo-Ramírez Á., Fernández-Salas L.M., López-González N., Vila Y., Orejas C. et al. 2021. Deep-sea habitat characterization using acoustic data and underwater imagery in Gazul mud volcano (Gulf of Cádiz, NE Atlantic). Deep Sea Research Part I 169: Article 103458. DOI: 10.1016/j.dsr.2020.103458.
   Web of Science ®Google Scholar
• Watanabe S., Metaxas A. & Scheibling R.E. 2009. Dispersal potential of the invasive green alga Codium fragile ssp. fragile. Journal of Experimental Marine Biology and Ecology 381: 114–125. DOI:10.1016/j.jembe.2009.09.012.
   Web of Science ®Google Scholar
• Winters G., Beer S., Willette D.A., Viana I.G., Chiquillo K.L., Beca-Carretero P., Villamayor B., Azcárate-García T., Shem-Tov R., Mwabvu B. et al. 2020. The tropical seagrass Halophila stipulacea: reviewing what we know from its native and invasive habitats, alongside identifying knowledge gaps. Frontiers in Marine Science 7: Article 300. DOI: 10.3389/fmars.2020.00300.
   Web of Science ®Google Scholar
• Wolff T. 1976. Utilization of seagrass in the deep sea. Aquatic Botany 2: 161–174. DOI:10.1016/0304-3770(76)90017-6.
   Google Scholar
• Yoshida T. 1998. Marine algae of Japan. Uchida Rokakuho, Tokyo, Japan. 1222 pp.
   Google Scholar
• Zenetos A. & Galandi M. 2020. Mediterranean non-indigenous species at the start of the 2020s: recent changes. Marine Biodiversity Records 13: Article 10. DOI:10.1186/s41200-020-00191-4.
   Google Scholar