Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter November 4, 2021

Arrival and proliferation of the invasive seaweed Rugulopteryx okamurae in NE Atlantic islands

  • João Faria

    João Faria holds a PhD in biology from the University of Lisbon and has been accumulating considerable knowledge on coastal habitats. He has proven to be skillful in applying experimental ecology designs and molecular and genetic tools to better understand how biological diversity is generated. His main research interests lie in the field of marine conservation and resilience of marine organisms to natural and/or anthropogenic-derived disturbances (i.e. biological invasions, fisheries, ocean warming and ocean acidification).

    ORCID logo EMAIL logo
    , Afonso C.L. Prestes

    Afonso C.L. Prestes is a PhD student of biology of the 3CBIO in the University of the Azores, studying the impact of invasive algae in the Azorean algal community. He has a research grant in the MIMAR + project for monitoring, control and mitigation of proliferations of marine organisms associated with human disturbances and climate change in the Macaronesian Region. He has participated in several research projects involving for instance the implementation of the European Water Framework in the Azores archipelago.

    , Ignacio Moreu , Gustavo M. Martins

    Gustavo M. Martins is currently head of the LAB-Algae lab at AQUAZOR where he coordinates the experimental laboratory for cultivation of marine macroalgae at off-shore structures. He was a post-doctoral researcher between 2010 and 2018. He has broad research interests that include the community ecology of intertidal rocky shores, the population and community level effects of harvesting, the importance of biodiversity for ecosystem processes, the impact of man-made structures on coastal ecosystems and the effects of climate change on species interactions.

    , Ana I. Neto

    Ana I. Neto passed away in May 2021. She was a professor at the University of Azores and since 1988 investigated marine botany and coastal ecology, using macroalgae as model organisms and the Azorean littoral communities as model systems. She was the lead scientist of the Island Aquatic Ecology SubGroup of the Azorean Biodiversity Group, and she coordinated the Herbarium AZB Ruy Telles Palhinha of DB/UAc.

    and Eva Cacabelos

    Eva Cacabelos is a post-doctoral researcher and has extensive experience in the analysis of factors affecting littoral communities. She has participated in projects investigating the effects of invasions, climate change or anthropogenic perturbations in benthic communities, as well as related to valorization of marine resources. She is well acquainted with the methods of investigating effects of non-indigenous species in littoral systems.

    ORCID logo
From the journal Botanica Marina

Abstract

The present study reports the recent occurrence and expansion of Rugulopteryx okamurae in the Azores archipelago (NE Atlantic). Morphological and molecular characters confirmed the species identification. Quick surveys around the island of São Miguel showed that it has successfully colonized the island and is quickly expanding. In some locations, R. okamurae is currently the dominant organism smothering all other benthic biota and posing a serious threat to the benthic ecosystems across the region. The species first record dates from 2019 near the main harbour of the island, suggesting that its introduction was driven by human-assisted transport, via boat ballast waters or adhered to ship hulls and likely originating from the Mediterranean populations that have been proliferating in recent years across the Strait of Gibraltar.


Corresponding author: João Faria, Department of Biology, Faculty of Sciences and Technology, cE3c - Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group; University of Azores, Ponta Delgada 9501-801, São Miguel, Azores, Portugal, E-mail:
Ana I. Neto unfortunately deceased prior to the publication of this article.

Funding source: FCT Fundao para a Cincia e Tecnologia

Award Identifier / Grant number: UID/BIA/00329/20152019 and UID/BIA/00329/2020

About the authors

João Faria

João Faria holds a PhD in biology from the University of Lisbon and has been accumulating considerable knowledge on coastal habitats. He has proven to be skillful in applying experimental ecology designs and molecular and genetic tools to better understand how biological diversity is generated. His main research interests lie in the field of marine conservation and resilience of marine organisms to natural and/or anthropogenic-derived disturbances (i.e. biological invasions, fisheries, ocean warming and ocean acidification).

Afonso C.L. Prestes

Afonso C.L. Prestes is a PhD student of biology of the 3CBIO in the University of the Azores, studying the impact of invasive algae in the Azorean algal community. He has a research grant in the MIMAR + project for monitoring, control and mitigation of proliferations of marine organisms associated with human disturbances and climate change in the Macaronesian Region. He has participated in several research projects involving for instance the implementation of the European Water Framework in the Azores archipelago.

Gustavo M. Martins

Gustavo M. Martins is currently head of the LAB-Algae lab at AQUAZOR where he coordinates the experimental laboratory for cultivation of marine macroalgae at off-shore structures. He was a post-doctoral researcher between 2010 and 2018. He has broad research interests that include the community ecology of intertidal rocky shores, the population and community level effects of harvesting, the importance of biodiversity for ecosystem processes, the impact of man-made structures on coastal ecosystems and the effects of climate change on species interactions.

Ana I. Neto

Ana I. Neto passed away in May 2021. She was a professor at the University of Azores and since 1988 investigated marine botany and coastal ecology, using macroalgae as model organisms and the Azorean littoral communities as model systems. She was the lead scientist of the Island Aquatic Ecology SubGroup of the Azorean Biodiversity Group, and she coordinated the Herbarium AZB Ruy Telles Palhinha of DB/UAc.

Eva Cacabelos

Eva Cacabelos is a post-doctoral researcher and has extensive experience in the analysis of factors affecting littoral communities. She has participated in projects investigating the effects of invasions, climate change or anthropogenic perturbations in benthic communities, as well as related to valorization of marine resources. She is well acquainted with the methods of investigating effects of non-indigenous species in littoral systems.

Acknowledgments

We thank the editor and reviewers for their helpful comments on the manuscript. In loving memory of Ana Neto.

  1. Author contribution: The authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: Funding was provided by National Funds through FCT – Fundação para a Ciência e Tecnologia, within the projects UID/BIA/00329/2015–2019 and UID/BIA/00329/2020–2023. ACLP was supported by a PhD grant awarded by FRCT- Fundo Regional da Ciência e Tecnologia (M3.1.a/F/083/2015).

  3. Conflict of interest statement: The author declare no conflicts of interest regarding this article.

References

Altamirano, M., De La Rosa, J., and Martínez, F.J. (2016). Arribazones de la especie exótica Rugulopteryx okamurae (E.Y. Dawson) I.K. Hwang, W.J. Lee and H.S. Kim (Dictyotales, Orchrophyta) en el Estrecho de Gibraltar: primera cita para el Atlántico y España. Algas 52: 20.Search in Google Scholar

Altamirano, M., De La Rosa, J., Martínez, F.J.G., and Muñoz, A.R.G. (2017). Prolifera en el Estrecho un alga nunca citada en nuestro litoral de origen asiático. Quercus 374: 32–33.Search in Google Scholar

Baptista, L., Santos, A.M., Melo, C.S., Rebelo, A.C., Madeira, P., Cordeiro, R., Botelho, A.Z., Hipólito, A., Pombo, J., Voelker, A.H.L., et al.. (2021). Untangling the origin of the newcomer Phorcus sauciatus (Mollusca: Gastropoda) in a remote Atlantic archipelago. Mar. Biol. 168: 9. https://doi.org/10.1007/s00227-020-03808-5.Search in Google Scholar

Bridsen, D. and Forman, L. (Eds.) (2010). The herbarium handbook, 3rd ed. Kew: Royal Botanic Gardens.Search in Google Scholar

De Clerck, O., Leliaert, F., Verbruggen, H., Lane, C.E., De Paula, J.C., Payo, D.I., and Coppejans, E. (2006). A revised classification of the Dictyoteae (Dictyotales, Phaeophyceae) based on rbcL and 26S ribosomal DNA sequence data analyses. J. Phycol. 42: 1271–1288. https://doi.org/10.1111/j.1529-8817.2006.00279.x.Search in Google Scholar

Draisma, S.G.A., Prud’homme van Reine, W.F., Stam, W.T., and Olsen, J.L. (2001). A reassessment of phylogenetic relationships within the Phaeophyceae based on Rubisco large subunit and ribosomal DNA sequences. J. Phycol. 37: 586–603. https://doi.org/10.1046/j.1529-8817.2001.037004586.x.Search in Google Scholar

García-Gómez, J.C., Sempere-Valverde, J., Ostalé-Valriberas, E., Martínez, M., Olaya-Ponzone, L., González, A.R., Espinosa, F., Sánchez-Moyano, E., Megina, C., et al. (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 48: 97–113.Search in Google Scholar

García-Gómez, J.C., Sempere-Valverde, J., González, A.R., Martínez-Chacón, M., Olaya-Ponzone, L., Sánchez-Moyano, E., Ostalé-Varriberas, E., and Megina, C. (2020). From exotic to invasive in record time: the extreme impact of Rugulopteryx okamurae (Dictyotales, Ochrophyta) in the strait of Gibraltar. Sci. Total Environ. 704: 135408. https://doi.org/10.1016/j.scitotenv.2019.135408.Search in Google Scholar PubMed

García-Gómez, J.C., Florido, M., Olaya-Ponzone, L., Rey Díaz de Rada, J., Donázar-Aramendía, I., Chacón, M., Quintero, J.J., Magariño, S., and Megina, C. (2021). Monitoring extreme impacts of Rugulopteryx okamurae (Dictyotales, Ochrophyta) in El Estrecho Natural Park (Biosphere Reserve). Showing radical changes in the underwater seascape. Front. Ecol. Evol. 9: 639161. https://doi.org/10.3389/fevo.2021.639161.Search in Google Scholar

Gayral, P. (1986). Connaitre et reconnaitre les algues marines. Éditions Ouest-France, Rennes.Search in Google Scholar

Hawkins, S.J., and Jones, H.D. (1992). Marine field course guide. 1. Rocky shores. marine conservation society. Immel Publishing Ltd, London.Search in Google Scholar

Hewitt, C.L., Gollasch, S., and Minchin, D. (2009). The vessel as a vector – bio-fouling, ballast water and sediments. In: Rilov, G. and Crooks, J.A. (Eds.). Biological invasions in marine ecosystems: ecological, management, and geographic perspectives. Springer-Verlag Berlin, Germany, pp. 117–131. https://doi.org/10.1007/978-3-540-79236-9_6.Search in Google Scholar

Hwang, I.K., Lee, W.J., Kim, H.S., and De Clerck, O. (2009). Taxonomic reappraisal of Dilophus okamurae (Dictyotales, Phaeophyta) from the western Pacific Ocean. Phycologia 48: 1–12. https://doi.org/10.2216/07-68.1.Search in Google Scholar

Lee, I.K. and Kang, J.A. (1986). A check list of marine algae in Korea. Korean J. of Phycol. 1: 311–325.Search in Google Scholar

Martins, G.M., Wallenstein, F.F.M.M., Álvaro, N.V., Neto, A.I., and Costa, A.C. (2005). Sampling strategies for biotope definition: minimal sampling area for selected groups of macroinvertebrates in the rocky subtidal of São Miguel, Azores. Helgol. Mar. Res. 59: 219–223. https://doi.org/10.1007/s10152-005-0222-x.Search in Google Scholar

Martins, G.M., Cacabelos, E., Faria, J., Álvaro, N.M., Prestes, A.C.L., and Neto, A.I. (2019). Patterns of distribution of the invasive alga Asparagopsis armata Harvey: a multi-scaled approach. Aquat. Invasions 14: 582–593. https://doi.org/10.3391/ai.2019.14.4.02.Search in Google Scholar

Martins, G.M., Patarra, R.F., Álvaro, N.V., Prestes, A.C.L., and Neto, A.I. (2013). Effects of coastal orientation and depth on the distribution of subtidal benthic assemblages. Mar. Ecol. 34: 289–297. https://doi.org/10.1111/maec.12014.Search in Google Scholar

Ocaña, O., Afonso-Carrillo, J., and Ballesteros, E. (2016). Massive proliferation of a dictyotalean species (Phaeophyceae, Ochrophyta) through the Strait of Gibraltar (Research note). Rev. Acad. Canar. Cienc. 28: 165–170.Search in Google Scholar

Rosas-Guerrero, J., Meco, Y.E., and Altamirano, M. (2018). Could Rugulopteryx okamurae (Dictyotales, Ochrophyta) have been introduced by ballast waters? Algas 54: 52.Search in Google Scholar

Saunders, G.W. and Moore, T.E. (2013). Refinements for the amplification and sequencing of red algal DNA barcode and RedToL phylogenetic markers: a summary of current primers, profiles and strategies. ALGAE 28: 31–43. https://doi.org/10.4490/algae.2013.28.1.031.Search in Google Scholar

Sempere-Valverde, J.J., Carlos García, J., Ostalé-Valriberas, E., Martínez, M., Olaya-Ponzone, L., González, A.R., Sánchez-Moyano, E., Megina, C., Parada, J.A., and Espinosa, F. (2019). Expansion of the exotic brown algae Rugulopteryx okamurae (e.y. Dawson) I.K. Hwang, W.J. Lee & H.S. Kim in the strait of Gibraltar. In: Proceedings of the 1st Mediterranean symposium on the non-indigenous species (Antalya, Turkey, 18 January 2019). SPA/RAC, Tunis, p. 116.Search in Google Scholar

Sempere-Valverde, J., Ostalé, E., Maestre, M., González, R., Bazairi, H., and 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. Ecol. Indicat. 121: 107135. https://doi.org/10.1016/j.ecolind.2020.107135.Search in Google Scholar

Silva, P.C., Menez, E.G., and Moe, R.L. (1987). Catalog of the benthic marine algae of the Philippines. Smithsonian Contrib. Mar. Sci. 27: 1–179. https://doi.org/10.5479/si.1943667x.27.1.Search in Google Scholar

Sun, Z., Hasegawa, K., and Tanaka, J. (2006). A morphological study of Dilophus okamurae (Dyctiotales, Phaeophyceae) in Japan. J. Jpn. Bot. 81: 235–244.Search in Google Scholar

Verlaque, M., Steen, F., and De Clerck, O. (2009). Rugulopteryx (Dictyotales, Phaeophyceae), a genus recently introduced to the Mediterranean. Phycologia 48: 536–542. https://doi.org/10.2216/08-103.1.Search in Google Scholar

Wallenstein, F.M., Neto, A.I., Álvaro, N.V., and Santos, C.I. (2008). Algae-based biotopes of the Azores (Portugal): spatial and seasonal variation. Aquat. Ecol. 42: 547–559. https://doi.org/10.1007/s10452-007-9134-y.Search in Google Scholar

Womersley, H.B.S. (1987). The marine benthic flora of southern Australia. Part II. South Australian Government Printing Division, Adelaide, Australia.Search in Google Scholar

Yoshida, T. (1998). Marine Algae of Japan. Uchida Rokakuho Publication, Tokyo.Search in Google Scholar


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2021-0060).


Received: 2021-06-15
Revised: 2021-08-08
Accepted: 2021-09-02
Published Online: 2021-11-04
Published in Print: 2022-02-23

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 6.12.2023 from https://www.degruyter.com/document/doi/10.1515/bot-2021-0060/html?lang=en
Scroll to top button