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Rugulopteryx okamurae

Rugulopteryx okamurae is a species of multicellular algae belonging to the genus Rugulopteryx of the Dictyotaceae family, native to the coasts of the Far East (Japan, eastern China and Korea), but with a tendency to become an invasive species when it reaches temperate waters.

Description

R. okamurae is a species of brown algae native to the Pacific Ocean with a natural distribution along the coasts of Japan, China and Korea, and is one of the four known species of the genus Rugulopteryx. In its natural habitat it lives at depths of between 0.5 and 5 meters, occasionally reaching 15 meters in very transparent waters . The specific epipet pays homage to the Japanese botanist and phycologist Kintaro Okamura (1867-1935).

The stalk is yellowish-brown when the specimens are young, darkening as it ages to a dark brown . Morphologically the stalk is bifurcate (dichotomous), i.e. the stalk branches at the top into two equal branches. The stems are erect, growing preferentially on hard substrate at the bottom of the euphotic zone, reaching a height of around 15 centimeters in East Asia and a little less in the Mediterranean (only 5 centimeters in Étang de Thau). Two growth forms are described, a densely branched form and a sparsely branched form. The lenticular apical cell is prominent, about 55 μm long and 85 μm wide. The stalk has three cell layers, with a pith (medulla), surrounded by two layers of cortex. The pith is single-layered in the center, but with progressively multiple layers towards the edges, so that the stalk is thicker at the edge than in the middle section. Each cortical structure consists of two to three layers of cells. From the base of the thallus emanate creeping fibers that grow to develop new thalluses through vegetative propagation. The structure of the alga is anchored to the substrate by filamentous rhizoids. In addition to multiplication by creeping fibers, adventitious specimens can also be formed on the edge of vegetative stalks, forming normal stalks that detach and form rhizoids when in contact with the substrate. The sporangia of the asexual generation are formed on both surfaces of the flattened stalk. Each sporangium is a spherical structure at the end of a short stem formed by two cells, without an involucral layer (they are naked sporangia). Each sporangium produces either a single spore or four identical spores. The female gametophytes of the sexual generation form sori with 3 to 35 oogonia each, while the male gametophytes have 30 to 100 antheridia each.

Occurrence in the Mediterranean and Atlantic

Outside its natural habitat Rugulopteryx okamurae was first found in the Mediterranean Sea in the spring of 2002 in the lagoon known as Étang de Thau, on the western Mediterranean coast of southern France. The Étang de Thau has also long been known as an introduction point for other marine creatures from the Pacific, and these species are likely to have arrived as a result of contamination via oysters from Japan (Crassostrea gigas) for aquaculture. As the characteristic forked branching pattern (the same, for example, as the native species Dictyota dichotoma) only occurs in Pacific species, it quickly became clear that it must be an introduced species. In that lagoon, the algae grows on the rocky bottom to a depth of about two meters from April to September. As initially only vegetative propagation occurred, membership of the species was determined genetically . The species quickly spread to the Mediterranean.

Based on the principles of the European Union’s Blue Circular Economy, recent studies have evaluated the potential of R. okamurae as an ingredient in aquaculture feed, especially for European sea bass (Dicentrarchus labrax). The algae are rich in bioactive compounds, such as polyphenols, terpenes, and vitamins, and possess moderate protein (3-15%) and lipid (0.4-5%) content .

However, using the algae presents challenges, such as its high concentration of sulfuric acid and anti-herbivory compounds, which can affect feed palatability and fish health. Additionally, its fiber-rich cell wall hinders the bioavailability of nutrients, requiring treatments such as enzymatic hydrolysis and fermentation to improve its digestibility .

The species has spread rapidly throughout the Western Mediterranean since it first appeared. Around 2015, the species reached the Strait of Gibraltar and thus the Atlantic . Although it can apparently only spread vegetatively in this region and therefore does not complete its life cycle, the species tends to form dense populations, which can completely dominate the habitat. In addition, the species is well protected against attack by grazing herbivores by a chemical repellent, the diterpene known as dilkamural . In the Jbel Musa marine reserve, off the African coast of the Strait of Gibraltar, in a single year, the species became the dominant colonizer, sometimes covering up to 96% of the bottom at depths of up to 30 meters. As a result, the threatened coral species that used to be common here (with the exception of one species) have declined significantly .

The species was first detected in Portugal in 2019, near the main port of São Miguel Island in the Azores archipelago, in the Northeast Atlantic. Initially identified as Dictyota spp. due to its phenotypic similarity, it is believed to have been introduced via ballast water or ship hulls from the Mediterranean, where it colonizes the Strait of Gibraltar.

Proliferation and Ecological Impacts

After its arrival, R. okamurae rapidly proliferated, dominating well-lit and shaded rocky subtidal habitats along the southern coast of São Miguel. Within just two years, the species became dominant in much of the rocky seabed, with occupancy rates reaching almost 100% in some areas. Its invasion has resulted in biodiversity reduction, alterations in community structure and consequences to the ecosystem.

Additionally, in May 2021, reports indicated the accumulation of algae substrates on beaches of Faial Island. Large masses of R. okamurae detach from the seabed due to strong prevailing swells, accumulating in coastal recesses where their decomposition generates a strong stench, negatively impacting the coastal environment.

Socioeconomic Impacts

The invasion has also caused significant problems for human activities in the Azores. Large quantities of algae accumulating in coastal areas generate unpleasant odors, compromising the tourism appeal of bathing zones and the absence of local herbivores that utilize the algae as a food source suggests potential changes in trophic structure, with negative implications for regional fishing activities.

Studies and Monitoring

Research conducted at eight locations around São Miguel, using a Before-After Control-Impact (BACI) design, highlighted the severity of the situation. At impacted sites, R. okamurae coverage reached 97.6% in 2021, while control sites remained unaffected. The results showed that even protected areas are not immune to the devastating effects of the invasive alga.

The extraordinary colonization and competitive capacity of R. okamurae poses a serious threat to Azorean ecosystems, potentially leading to the extinction of native species and critical transformations of coastal ecosystems. Continuous monitoring and study of this species' impacts are essential for developing management strategies to mitigate damages and preserve the region's biodiversity.

The species has been on the European Union's Black List of Invasive Species since 2022, which implies the adoption of mandatory control and management measures for the species. Bringing in and taking out, transporting, keeping, multiplying and releasing are therefore prohibited .

Biology and life cycle

The species was first described in Japan, occurring in the Asian coastal waters of the northwest Pacific. In its natural distribution region in East Asia, especially along the coasts of the Korean Peninsula, Rugulopteryx okamurae is a common species in the subtidal shelf region, at depths of 0.5 to 5 meters, occasionally occurring up to 15 meters deep . The life cycle and reproductive strategies of R. okamurae are highly adaptable, contributing to its survival and proliferation across diverse environments.

R. okamurae employs a heteromorphic life cycle, alternating between a diploid sporophytic phase and a haploid gametophytic phase. This dual reproductive strategy allows the species to thrive under varying environmental conditions, ensuring both genetic diversity and efficient colonization of new habitats. For asexual reproduction the species reproduces vegetatively through fragmentation. Detached fragments of the thallus can establish themselves in new locations, especially in areas with strong currents or wave action. This mechanism makes R. okamurae highly effective at colonizing and dominating new environments.

In sexual reproduction the gametophytes produce male and female gametes that fuse to form zygotes, which subsequently develop into new sporophytes. This process of genetic mixing enhances the species’ adaptability to changing environmental conditions and stressors.

In its native range, R. okamurae demonstrates distinct seasonal growth cycles:

• Spring and Summer: The species experiences rapid growth, with new stalks sprouting from overwintering filaments attached to the substrate. Young stalks also develop during this period from spore germination. Sporophyte production peaks from June to October, with a maximum in September.
• Winter: Growth slows significantly, and the alga retreats to its basal state, leaving only filaments on the substrate. These filaments persist through adverse conditions, enabling regrowth in the following spring.

This seasonal adaptability, coupled with its reproductive versatility, underscores R. okamurae’s resilience and competitive dominance in both its native and introduced regions.

Toxicity

The invasive success of R. okamurae along the southwestern coasts of Europe has driven research into the possible role of its chemical defenses in explaining the macroalgae's spread in these new environments. A recent phytochemical analysis of R. okamurae collected from the Strait of Gibraltar identified six secondary metabolites (referred to as compounds 1–6). The chemical structures of these diterpenes were determined using nuclear magnetic resonance (NMR). Among these compounds, one in particular, dilkamural (compound 1), was suggested to play a key role in the macroalgae's deterrent and toxic effects on herbivores. This behavior appears to be linked to the notably high concentration of dilkamural compared to the other metabolites present in R. okamurae . This investigation highlighted the high content in dilkamural compound (4.21 ± 0.39% of the dry weight of algae) by R. okamurae, which may be responsible for the low preference of native consumers for the invasive species

Taxonomy and Systematics

The species name was introduced as Dilophus okamurai in 1950 by the American naturalist and algalogist Elmer Yale Dawson, and the specific epithet was later corrected to okamurae. Dawson paid homage to the Japanese phycologist Kintaro Okamura (1867-1935), who illustrated and described the species under the name Dictyota marginata in his work Iconography of Japanese Algae . Okamura's name is a younger homonym and therefore an illegitimate name, so a replacement name had to be found. Recent phylogenomic research, in which the relationship between species is examined by comparing homologous DNA sequences, subsequently revealed that the division of the Dictyotaceae family into genera would have to be revised. As a result, Il-Ki Hwang and colleagues placed the species in the genus Rugulopteryx in 2009, a solution that was widely accepted.

Subsequently, the genus Rugulopteryx was reorganized by Olivier de Clerck and Eric Coppejans in 2006 to include some species from the former genera Dictyota and Dilophus. In its current taxonomic circumscription, the genus Rugulopteryx has four described species:

• Rugulopteryx marginata (J.Agardh) De Clerck & Coppejans C
• Rugulopteryx okamurae (E.Y.Dawson) I.K.Hwang, W.J.Lee & H.S.Kim C
• Rugulopteryx radicans (Harvey) De Clerck & Coppejans C
• Rugulopteryx suhrii (Kützing) De Clerck & Coppejans C

References

1. https://www.algaebase.org/search/species/detail/?species_id=Tbe5484c5cd8b2be3 M.D. Guiry in Guiry, M.D. & Guiry, G.M. 01 February 2024. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway.
2. José Carlos García-Gómez et al. “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. Revista de Estudios Campogibraltareños, 49, diciembre 2018. Algeciras. Instituto de Estudios Campogibraltareños, pp. 97-113.
3. K. Hwang, W.J. Lee, H.-S. Kim and O. De Clerck. 2008. Taxonomic reappraisal of Dilophus okamurae (Dictyotales, Phaeophyta) from the western Pacific Ocean. Phycologia 48: 1–12. DOI: 10.2216/07-68.1
4. Verlaque, M., Steen, F., & De Clerck, O. (2009). Rugulopteryx (Dictyotales, Phaeophyceae), a genus recently introduced to the Mediterranean. Phycologia, 48(6), 536–542. https://doi.org/10.2216/08-103.1
5. Hwang, I. K., Lee, W. J., Kim, H. S., & De Clerck, O. (2009). Taxonomic reappraisal of Dilophus okamurae (Dictyotales, Phaeophyta) from the western Pacific Ocean. Phycologia, 48(1), 1–12. https://doi.org/10.2216/07-68.1
6. Verlaque, M., Steen, F., & De Clerck, O. (2009). Rugulopteryx (Dictyotales, Phaeophyceae), a genus recently introduced to the Mediterranean. Phycologia, 48(6), 536–542. https://doi.org/10.2216/08-103.1
7. Fonseca, F., Fuentes, J., Vizcaíno, A. J., Alarcón, F. J., Mancera, J. M., Martínez-Rodríguez, G., & Martos-Sitcha, J. A. (2023). From invasion to fish fodder: Inclusion of the brown algae Rugulopteryx okamurae in aquafeeds for European sea bass Dicentrarchus labrax (L., 1758). Aquaculture, 568. https://doi.org/10.1016/j.aquaculture.2023.739318
8. Fonseca, F., Fuentes, J., Vizcaíno, A. J., Alarcón, F. J., Mancera, J. M., Martínez-Rodríguez, G., & Martos-Sitcha, J. A. (2023). From invasion to fish fodder: Inclusion of the brown algae Rugulopteryx okamurae in aquafeeds for European sea bass Dicentrarchus labrax (L., 1758). Aquaculture, 568. https://doi.org/10.1016/j.aquaculture.2023.739318
9. García-Gómez, J. C., Florido, M., Olaya-Ponzone, L., Rey Díaz de Rada, J., Donázar-Aramendía, I., Chacón, M., Quintero, J. J., Magariño, S., & 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. Frontiers in Ecology and Evolution, 9. https://doi.org/10.3389/fevo.2021.639161
10. 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 and Shelf Science, 257. https://doi.org/10.1016/j.ecss.2021.107398
11. 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. https://doi.org/10.1016/j.ecolind.2020.107135
12. "L_2022186PT.01001001.XML".
13. Hwang, I. K., Lee, W. J., Kim, H. S., & De Clerck, O. (2009). Taxonomic reappraisal of Dilophus okamurae (Dictyotales, Phaeophyta) from the western Pacific Ocean. Phycologia, 48(1), 1–12. https://doi.org/10.2216/07-68.1
14. Fonseca, F., Fuentes, J., Vizcaíno, A. J., Alarcón, F. J., Mancera, J. M., Martínez-Rodríguez, G., & Martos-Sitcha, J. A. (2023). From invasion to fish fodder: Inclusion of the brown algae Rugulopteryx okamurae in aquafeeds for European sea bass Dicentrarchus labrax (L., 1758). Aquaculture, 568. https://doi.org/10.1016/j.aquaculture.2023.739318
15. García-Gómez, J. C., Florido, M., Olaya-Ponzone, L., Rey Díaz de Rada, J., Donázar-Aramendía, I., Chacón, M., Quintero, J. J., Magariño, S., & 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. Frontiers in Ecology and Evolution, 9. https://doi.org/10.3389/fevo.2021.639161
16. Dawson, E. Y., & Bulletin, S. : (1950). Torrey Botanical Society Notes on Some Pacific Mexican Dictyotaceae. In of the Torrey Botanical Club (Vol. 77, Issue 2). http://www.jstor.orgURL:http://www.jstor.org/stable/
17. Hwang, I. K., Lee, W. J., Kim, H. S., & De Clerck, O. (2009). Taxonomic reappraisal of Dilophus okamurae (Dictyotales, Phaeophyta) from the western Pacific Ocean. Phycologia, 48(1), 1–12. https://doi.org/10.2216/07-68.1

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