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Occurrence of the invasive brown seaweed Rugulopteryx okamurae in Morocco (Mediterranean Sea)

  • Instituto Universitario de Sanidad Animal y Seguridad Alimentaria
  • National Institute of Fisheries Research

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Rugulopteryx okamurae, a brown alga native to the temperate western Pacific Ocean, was discovered for the first time in the Mediterranean Sea in 2002, in the Thau Lagoon (France). A new population of R. okamuraewas discovered in Belyounech Beach with the observation of some specimens fixed near the harbour of Tanger (Strait of Gibraltar-Morocco). As well as, the remarkable record of this alga stranded in M’diq beach (Alboran Sea-Morocco).Since its introduction R. okamurae has established in the Thau Lagoon (France), self-sustaining populations without displaying an invasive behaviour. On the contrary,the newly discovered population in Morocco would be classified as invasive. This new record gives the range extension of this invasive alga, from the southwest of Alboran Sea to the southwestern limit of Gibraltar.The presence of this invasive seaweed in the area may affect the native alga, seagrass and native fauna including fish community negatively (PDF) Occurrence of the invasive brown seaweed Rugulopteryx okamurae in Morocco (Mediterranean Sea). Available from: [accessed Mar 18 2019].
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... This brown macroalga, originated from the northwest of Asia (Hwang et al., 2009), has been systematically reported on the coasts of the Strait of Gibraltar since 2015 (see Altamirano-Jeschke et al., 2016), when more than 5,000 tons of wracks were extracted from the beaches of its south coasts, in the city of Ceuta (North-Africa) (Ocaña et al., 2016). The rocky bottoms of The Jbel Moussa Site of Biological and Ecological Interest (SIBE) (El Aamri et al., 2018) and the eastern littoral of El Estrecho Natural Park (PNE) firstly represented the northern and southern scenarios of R. okamurae expansion in the Strait of Gibraltar. Until date, these areas constitute the most intensely affected by the brown alga, which continues its westward and eastward directionality of expansion Figueroa et al., 2020) with trend to monopolize the sea rocky bottom in detriment of the photophilous resident biota (García-Gómez et al., 2020b). ...
... It is urgent to carry out studies on the distribution, ecology and impacts of R. okamurae in the Mediterranean and the Atlantic coasts, as well as the implementation of management measures. However, few studies have been carried out on R. okamurae distribution (e.g., Altamirano-Jeschke et al., 2016;Ocaña et al., 2016;El Aamri et al., 2018;Altamirano et al., 2019) and its derived impacts on the recipient sessile , 2020bSempere-Valverde et al., 2020) and mobile associated biota (Navarro-Barranco et al., 2019). In this regard, there is only one published study monitoring the temporal dynamic of the invasion since the first apparition of the species in the Strait waters (see García-Gómez et al., 2020b) by the utilization of Sessile Bioindicators in Permanent Quadrats (SBPQ). ...
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The invasive macroalga Rugulopteryx okamurae represents an unprecedented case of bioinvasion by marine macroalgae facing the European coasts. Since the first apparition of the species in the Strait of Gibraltar in 2015, its fast dispersion along the introduced habitats constitutes a real challenge to develop monitoring strategies that ahead of its impacts. The present study uses three different approaches to address impacts on the benthic ecosystems, at the same time offers relevant data for future management actions in El Estrecho Natural Park (PNE). Information obtained by monitoring permanent sentinel stations revealed a significant loss in resident species coverage after the moment of maximum growth in 2017. Thus, despite coverage of R. okamurae did not strongly varied in the latter years, impacts generated remain high in the habitats studied. Estimations of the invasive species coverage by combining cartographic image analysis and in situ data predicted a major occupation (over 85% coverage) between 10 and 30 m, coinciding with the maximum rocky surface areas (m 2) mapped on the PNE. Furthermore, a Citizen Science research collaboration evidenced impacts on the benthic seascape through an ad hoc exploration of images that allowed a "before" and "after" comparison of the invasion process in the same geographic locations. This has made it possible to graphically demonstrate severe changes in the underwater seascape and, therefore, the general impact of this new biological invasion. The spatial colonization estimations combined with the impacts reported by both scientific [Sessile Bioindicators in Permanent Quadrats (SBPQ) sentinel stations] and civilian (Citizen Science) monitoring methodologies claim the urgent development of further studies that allow the design of monitoring strategies against R. okamurae expansion across the Mediterranean and Atlantic waters.
... The Belyounech region, Tangier, and Mdiq on the Mediterranean coast and in the Strait of Gibraltar [6] Spartina densiflora(Herbaceous plants) ...
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Following a scientific prospecting mission, a direct observation of the crab Callinectes sapidus Rathbun, 1896 was recorded. This observation confirms the expansion of this species in the Atlantic fringe, including the Merja Zerga Biological Reserve.
... Rugulopteryx okamurae has proliferated on the Atlantic and Mediterranean coast in a short time displacing the local biota and generating an unprecedented ecological impact, causing a great concern for the sea-dependent local activities in the aforementioned geographical enclave (El Aamri et al. 2018;Navarro-Barranco et al 2019;García-Gómez et al. 2020;Sempere-Valverde et al. 2021). The high content of spatane type diterpenes, with herbivorous deterrent activity, of this species has allowed its high and rapid propagation and production. ...
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The biomass valorisation of the invasive brown alga Rugulopteryx okamurae (Dictyotales, Phaeophyceae) is key to curbing the expansion of this invasive macroalga which is generating tonnes of biomass on southern Spain beaches. As a feasible alternative for the biomass management, anaerobic co-digestion is proposed in this study. Although the anaerobic digestion of macroalgae barely produced 177 mL of CH 4 g ⁻¹ VS, the co-digestion with a C-rich substrate, such as the olive mill solid waste (OMSW, the main waste derived from the two-phase olive oil manufacturing process), improved the anaerobic digestion process. The mixture improved not only the methane yield, but also its biodegradability. The highest biodegradability was found in the mixture 1 R. okamurae— 1 OMSW, which improved the biodegradability of the macroalgae by 12.9% and 38.1% for the OMSW. The highest methane yield was observed for the mixture 1 R. okamurae —3 OMSW, improving the methane production of macroalgae alone by 157% and the OMSW methane production by 8.6%. Two mathematical models were used to fit the experimental data of methane production time with the aim of assessing the processes and obtaining the kinetic constants of the anaerobic co-digestion of different combination of R. okamurae and OMSW and both substrates independently. First-order kinetic and the transference function models allowed for appropriately fitting the experimental results of methane production with digestion time. The specific rate constant, k (first-order model) for the mixture 1 R. okamurae - 1.5 OMSW, was 5.1 and 1.3 times higher than that obtained for the mono-digestion of single OMSW and the macroalga, respectively. In the same way, the transference function model revealed that the maximum methane production rate ( R max ) was also found for the mixture 1 R. okamurae —1.5 OMSW (30.4 mL CH 4 g ⁻¹ VS day ⁻¹ ), which was 1.6 and 2.2 times higher than the corresponding to the mono-digestions of the single OMSW and sole R. okamurae (18.9 and 13.6 mL CH 4 g ⁻¹ VS day ⁻¹ ), respectively.
... Nevertheless, in Thau lagoon, this species did not show a critical invasive behavior as it happened in the Strait coasts (Verlaque et al., 2009;García-Gómez et al., 2018). During 2015-2016, R. okamurae quickly colonized most of the shoreline of this Strait, requiring municipal cleaning machines to remove more than 5,000 tons of detached biomass from the touristic beaches of Ceuta, North Africa (Ocaña et al., 2016;El Aamri et al., 2018). The massive algal wracks detected ( Supplementary Figure 1), together with the huge coverages identified when the species is attached to the rocky bottoms (García-Gómez et al., 2018, 2020, suggest that this case is worryingly unusual because of the large amounts of biomass produced in such a small geographical area. ...
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The present study constitutes the first evaluation of the space colonization strategies performed by Rugulopteryx okamurae when co-occurring with the resident macroalgal community in the introduced areas. Since the first apparition of the nonindigenous macroalga in the Strait of Gibraltar, its high propagation capacity together with its colonization ability has enhanced the establishment success of the species in detriment of the resident biota. In this study, we carried out observational surveys during 2017-2020 in order to assess the coverage levels of R. okamurae on different lighting conditions, surface orientations, and substrata types (artificial and natural). Results revealed that, beyond the high percent coverages already reported at illuminated and semi-illuminated natural rocky habitats, R. okamurae is able to settle on a wide variety of artificial substrata. The settlement performance of the species was also investigated and different mechanisms underlying the space colonization were proposed. Thus, R. okamurae was observed interacting with 43 resident macroalgal species at generally illuminated rocky habitats of the northern Strait coasts. Six colonization mechanisms were proposed for spatial growth scenarios. Overall, results pointed out that, in most of the cases where the invasive species co-occur with the resident community, R. okamurae would be favored as regards spatial growth success. Competitive interactions and environmental factors which influence results obtained must be addressed in order to fully predict impacts on resident communities. Moreover, together with previous scientific works, overall data provided in this study highlight the need to urgent implement management measures focused on habitats susceptible to be invaded, as well as studies on the ecology and dispersal vectors of R. okamurae in the Strait of Gibraltar and adjacent areas.
... In 2017 an alert about this invasive seaweed was published in Quercus (Altamirano et al., 2017). Also in August 2017 this seaweed was observed in the south of Alboran, first in the Moroccan part of Gibraltar Strait and extending along the Moroccan Mediterranean coast in 2018 (El AAmri et al., 2018;García-Gómez et al., 2018). ...
Technical Report
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We report the findings of a pilot project on the interactions between bottlenose dolphin and other cetaceans and artisanal fisheries using nets in the northern Alboran Sea, the GSA 01 of the GFCM. Based on most of the ports of the region, the SSF is generally affected in their activity and revenues by depredation of captures. The situation was wrong from 2016 when al alien algae species, Rugulopterix okamurae, extended through the whole region affecting the ecosystem and the fishing activity.
The southwestern coasts of Europe (Strait of Gibraltar) are experiencing a severe invasion of the brown alga Rugulopteryx okamurae, original from the northwestern Pacific ocean. Currently there is no clue regarding to the reasons of such huge invasive potential, although the involvement of chemical defenses has recently been suggested. In this context, this study was aimed to investigate the presence and potential role of chemical defenses in the invasive success of R. okamurae. The chemical study of R. okamurae from the Strait of Gibraltar led to the isolation of six secondary metabolites, among which the compound dilkamural stands out because of its high concentration. Later, in a set of feeding deterrent assays, the generalist native herbivore Paracentrotus lividus showed a higher consumption over the native alga Ulva sp. than over the non-native R. okamurae. This low consumption was tracked down to dilkamural, which displayed not only deterrent properties but also caused harmful and even lethal effects over the sea urchins. These results are consistent with the novel weapons hypothesis, since dilkamural was not described previously in the invaded area and has a defensive role against generalist herbivores in the new range, thus helping to explain the great expansion of R. okamurae in the Strait of Gibraltar.
Invasive alien species (IAS) is a scourge that gnaws away at biodiversity, the environment as a whole, and the socioeconomic fabric of countries. In Morocco, nearly 150 IAS have been inventoried and argued, and it is sincerely believed that this number is well below the actual total number of IAS introduced into the country, which suggests other scientific investigations, both on the ground and in the laboratory, to be able to identify them. These IAS cause damage, sometimes catastrophic. Virtually all environments suffer: ecosystems, landscapes, the agro‐ecosystem, the forest ecosystem, wetlands, and the marine and coastal environment. The country's economy, its social stability, as well as human and animal health are also concerned. In agriculture and aquaculture, vital and strategic (food security, jobs, rural economy), IAS pose a real threat to grain farming, arboriculture, seaweed farming, and so on, and almost all species of food interest are threatened by IAS, accidentally or deliberately introduced to the point where yield, of cereal for example, has dropped by 98% in some areas of the country. The reduction in yield concerns not only cultivated plants but also farmed animals (sheep flocks, goats, birds, bees, etc.) because of their toxicity, their aggressiveness, or their competitiveness. The Moroccan forest, which is strategic for the country's overall ecological balance and for its rural economy, also suffers from IAS, in particular its heritage species such as the Atlas cedar. Wetlands that have experienced fish introductions since the beginning of the last century have been greatly affected by these exotic species to the point that, in the early years of introduction, native forms such as pallary trout have been exterminated. The marine and coastal environment, despite its buffering capacity, is beginning to feel the weight of the threat of IAS introduced mainly for aquaculture reasons. The information concerning this environment remains very fragmentary given the insufficient human and material resources available for exploration of this area, particularly for ballast water and bio‐soiling. The little information that exists, however, shows a negative effect of introduced species on native ones. Silverleaf nightshade (in Morocco, morelle jaune) and the pine processionary are also the origin of respiratory or allergic diseases, and the tiger mosquito could be the origin of many more serious diseases. The fight against IAS remains punctual, often mechanical, without a targeted strategy; and the main monitoring instrument remains the establishment of the National Office for the Health Security of Food Products (ONSSA), whose main task is the control of transit, at each point of entry into the national territory, of plants, seeds, animals, and biological material potentially harmful to the environment or health in the country.
La macroalga parda de origen asiático Rugulopteryx okamurae, está invadiendo las costas de Ceuta, norte de Marruecos y Andalucía (especialmente las de las provincias de Cádiz y Málaga). Desde su detección en Ceuta en el año 2015, no ha dejado de colonizar fondos marinos desde zonas intermareales hasta 40 m de profundidad y, de acuerdo con modelos de favorabilidad ambiental, podría colonizar todo el Mediterráneo y parte de la costa Atlántica Noroeste de Marruecos. La rápida expansión de esta especie exótica hace que sea urgente tener más conocimiento de la biología y bioquímica de la especie y de los factores autoecológicos y ambientales que favorecen la proliferación y dispersión. En este artículo se presentan características fotosintéticas de la especie, demostrando que es un alga muy productiva y con una gran plasticidad fisiológica, ya que es capaz de mantener una alta capacidad fotosintética a lo largo del año, tanto en talos fijados al sustrato como talos sueltos que flotan en la columna de agua. La identificación de los factores ambientales que expliquen la proliferación del alga en nuestras costas requiere de un buen conocimiento de su ciclo biológico, fisiología, composición bioquímica e interacciones con otras comunidades, tanto de macrófitos como de potenciales depredadores. Sólo con este conocimiento es posible diseñar planes efectivos para prevenir su expansión y acciones de remediación
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The Mediterranean is one of the most biodiverse and anthropogenically impacted seas and the coralligenous is one of its most diverse habitats. Its presence is indicative of well-preserved areas and its associated species are considered among the best bioindicators for monitoring nearshore rocky habitats. This study aims to report the temporal fluctuations of the coralligenous community in the marine protected area of Jbel Moussa (Strait of Gibraltar) in a period concomitant with the rapid expansion of the non-indigenous species Rugulopteryx okamurae (E.Y.Dawson) I.K.Hwang, W.J.Lee & H.S.Kim in the area. From year 2015 to 2019, an area covering 36 m 2 of the coralligenous habitat was monitored across three sites, including temperature logs from 2017 to 2019. After its first record in the area in 2017, R. okamurae became the most abundant species in only one year, followed by a change in the coralligenous community structure and a regression of the bioindicator species Paramuricea clavata (Risso, 1826) and Mesophyllum expansum (Philippi) Cabioch & M.L.Mendoza. These species are sensitive to increases in water temperature and were already under a gradual regression due to anthropogenic disturbances and previous biological invasions, all of which could have reduced niche competition in the area and favoured the impacts caused by R. okamurae in the area. Results highlight the need of a rapid administrative response to increase mitigation efforts on this protected habitat. Due the potential expansion of this non-indigenous invasive species to the Mediterranean Sea, the present study could provide valuable information for future monitoring, conservation and management actions.
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Se resumen los aspectos tratados en la mesa redonda desarrollada en el Workshop de especies invasoras marinas.
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Dilophus okamurae, a common species of brown alga in the warm temperate western Pacific Ocean (Philippines, Taiwan, China, Korea and Japan), is characterized by a typical vegetative morphology that would support its traditional placement in the genus Dilophus. The species has a unilayered cortex, and the medulla is multilayered at least near the margins of the tahllus. Sporangia on a two-celled stalk, without an involucrum, however, indicate a close relationship with the recently described genus Rugulopteryx. Molecular phylogenetic analyses, based on three separate loci, large subunit rDNA (LSU), rbcL and psbA confirm the close phylogenetic relationship between D. okamurae and R. radicans, and R. marginatus and R. suhrii. A transfer of D.okamurae to the genus Rugulopteryx is therefore proposed. Contrary to the expected diplobiontic life cycle, typically encountered in Dictyotales, the species exhibits an asexual life cycle consisting of sporophytes only in the populations studied on the east and south coast of Korea. Gametophytes were only obtained by culturing field collected specimens.
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Although invasive species are widely recognized as a major threat to marine biodiversity, there has been no quantitative global assessment of their impacts and routes of introduction. Here, we report initial results from the first such global assessment. Drawing from over 350 databases and other sources, we synthesized information on 329 marine invasive species, including their distribution, impacts on biodiversity, and introduction pathways. Initial analyses show that only 16% of marine ecoregions have no reported marine invasions, and even that figure may be inflated due to under-reporting. International shipping, followed by aquaculture, represent the major means of introduction. Our geographically referenced and publicly available database provides a framework that can be used to highlight the invasive taxa that are most threatening, as well as to prioritize the invasion pathways that pose the greatest threat. *** FYI You can access the paper and associated database here:
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Although invasive species can negatively impact communities via processes such as resource competition, they may also add new resources that facilitate the distribution and/or abundance of other organisms. In rocky intertidal systems, many benthic macroalgae compete for primary substrate, while providing secondary substrata to which sessile organisms can attach. Using field surveys and laboratory experiments, we investigated algal host-epiphyte dynamics in a New England rocky intertidal system. First, we compared the composition, abundance, richness, and diversity of epiphytes on 2 invasive macroalgal species, Codium fragile ssp. tomentosoides and Grateloupia turuturu, to 2 native macroalgal species, Chondrus crispus and Fucus vesiculosus. We found significant differences among epiphyte communities, as all macroalgal hosts supported different assemblages of species. While epiphyte richness and diversity were generally low on F. vesiculosus and G. turuturu year-round, they were low on C. crispus during the winter only, In contrast, epiphyte richness and diversity on C. fragile remained high throughout the year, suggesting that C. fragile plays an important role for supporting epiphytes during the cooler months. Second, we examined the relationship between epiphytes and a common herbivorous snail, Lacuna vincta. The abundance of juvenile L. vincta was positively correlated with 1 of the 2 most common epiphyte species, Neosiphonia harveyi. However, L. vincta showed a significant consumption preference for the other abundant epiphyte, Ceramium virgatum, in laboratory assays. Our results suggest that epiphyte facilitation by these invasive algal hosts is not only seasonally important for maintaining species richness and diversity, but may also provide both food and habitat for higher trophic levels.
The life cycle of Dilophus okamurae and the associated benthic invertebrate fauna were studied monthly or bimonthly from June 1998 to September 1999 at a depth of 4–7 m in Onagawa Bay along the Pacific coast of north-eastern Honshu, Japan (38°28′N, 149°29′E). Dry biomass ranged from 230 g/m2 in June to 10 g/m2 in October. Sporophytes with tetrasporangia appeared during July to September 1998. Gametophytes with oogonia or antheridia were observed for the first time in May 1999 during observation. The absence of mature sporophytes in 1999 suggests that the life cycle is completed over two years. The sympatric gastropods Lirularia iridescens, Homalopoma sangrarense, Conotalopia minima and Cantharidus callichroa synchronized with seasonal changes in biomass of this algae. In contrast, Barleeia angustata and B. trifasciata fluctuated independently. The juvenile sea urchin Strongylocentrotus nudus appeared in the algal population starting in October at 0.7 mm mean test diameter at high density, and disappeared after March.
Dictyota is a genus of tropical to warm temperate brown algae characterized by parenchymatous, flattened thalli that grow from a single, transversely oriented apical cell. Dictyota is currently distinguished from allied genera of the tribe Dictyoteae (Dilophus, Glossophora, Glossophorella, and Pachydictyon) by the structure of the cortical and medullary layers, as well as the relative abundance of surface proliferations. Even though the traditional classification of the Dictyoteae has repeatedly been criticized in the past, the absence of sound molecular data has so far discouraged any new taxonomic proposals apart from a merger of Dilophus with Dictyota, which has been accepted by only part of the phycological community. Phylogenetic analysis of rbcL gene, partial 26S rDNA sequence, and combined data sets, including four of five generitypes, demonstrates that the traditional classification does not accurately reflect the evolutionary history of the group. None of the genera are resolved as a monophyletic clade. Hence, a merger of Glossophora, Glossophorella, and Pachydictyon in Dictyota is proposed. Two new genera, Canistrocarpus (incorporating D. cervicornis, D. crispata, and D. magneana) and Rugulopteryx (accommodating D. radicans, Dil. suhrii, and Dil. marginata), are proposed. Both genera are supported by molecular indications and a combination of reproductive and vegetative characters. The position of Dil. fastigiatus as a clade sister to Dictyota s.l. and the absence of Dil. gunnianus, the generitype of Dilophus, from the analyses, prevented us from making a more definite statement on the status of the latter genus.
Invasive alien marine species threaten biodiversity, marine industries (including fishing and tourism) and human health, and unlike oil spills only get worse with time. While some progress is being made internationally on the 10,000 species estimated to be in transit around the world in the ballast water, effective solutions are a long way off; meanwhile the majority of vectors is being ignored. A systematic approach to invasive alien marine species is required to target the means and location of the most effective management actions. Cooperation among regional trading partners will be essential to effectively manage the threat.
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Marine bioinvasions: conservation hazards and vehicles for ecological understanding
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