Journal Pre-proofs

From exotic to invasive in record time: the extreme impact of rugulopteryx oka-
murae (dictyotales, ochrophyta) in the strait of gibraltar

José Carlos García-Gómez, Juan Sempere-Valverde, Alexandre Roi González,

Manuel Martínez-Chacón, Liliana Olaya-Ponzone, Emilio Sánchez-Moyano,
Enrique Ostalé-Valriberas, César Megina

PII: S0048-9697(19)35401-4
DOI: https://doi.org/10.1016/j.scitotenv.2019.135408
Reference: STOTEN 135408

To appear in: Science of the Total Environment

Received Date: 14 August 2019

Revised Date: 29 October 2019
Accepted Date: 5 November 2019

Please cite this article as: J.C. García-Gómez, J. Sempere-Valverde, A.R. González, M. Martínez-Chacón, L. Olaya-
Ponzone, E. Sánchez-Moyano, E. Ostalé-Valriberas, C. Megina, 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 (2019), doi: https://doi.org/10.1016/j.scitotenv.2019.135408

This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover
page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will
undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing
this version to give early visibility of the article. Please note that, during the production process, errors may be
discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

© 2019 Elsevier B.V. All rights reserved.

FROM EXOTIC TO INVASIVE IN RECORD TIME: THE EXTREME

IMPACT OF RUGULOPTERYX OKAMURAE (DICTYOTALES,

OCHROPHYTA) IN THE STRAIT OF GIBRALTAR

José Carlos García-Gómez*,1, Juan Sempere-Valverde1, Alexandre Roi

González1, Manuel Martínez-Chacón3, Liliana Olaya-Ponzone1, Emilio

Sánchez-Moyano1, Enrique Ostalé-Valriberas1

, César Megina#,2

1Laboratorio de Biología Marina de la Universidad de Sevilla (LBMUS)/ Área

de Investigación I+D+i del Acuario de Sevilla/ Estación de Biología Marina del

Estrecho (Ceuta)

2Biodiversidad y Ecología de Invertebrados Marinos, Universidad de Sevilla/

Área de Investigación I+D+i del Acuario de Sevilla

3Club de buceo CIES-ALGECIRAS

* First author: jcgarcia@us.es, ORCID: 0000-0002-6913-1215

# Corresponding author: cmegina@us.es

ABSTRACT

In 2015, the exotic seaweed Rugulopteryx okamurae was detected for the first

time on the south side of the Strait of Gibraltar, in Ceuta (northern Africa). This
highly sensitive area is ideal for monitoring local environmental impacts arising

from global warming, as well as the intrusion of alien species. Within one year,

R. okamurae became an invasive species with an overflowing competitive

capacity and growth. In 2015, more than 5,000 tons of upstream biomass was

extracted from beaches in Ceuta, and it has since spread irrepressibly on rocky

illuminated bottoms of the subtidal zone to a maximum observed depth of 40 m.

The highest coverage (80–90%) of R. okamurae in Ceuta was observed between

10–20 m depth in illuminated habitats, where it was having a severe impact on

local benthic communities which were displaced. Between 5–30 m depth,

coverage of R. okamurae exceeded 70% over a wide variety of substrate types. A

submarine sentinel sessile bioindicators permanent quadrats (SBPQ) station

installed in 2013 on poorly lit, vertical, and shady substrate in the El Estrecho

Natural Park, on the north side of the Strait of Gibraltar (Tarifa), detected the

presence of R. okamurae in July 2016 and recorded the subsequent increase in

coverage. These findings reveal the useful role of this type of monitoring SBPQ

sentinel station for the detection of impacts and exotic species in marine protected

areas, and for the monitoring of global warming based on indicator species. We

conclude that the catastrophic bloom of R. okamurae exhibited an initial

geographical expansion (2015–2017) to the northern coastal area of the Strait of

Gibraltar (Tarifa-Gibraltar) and subsequent extension (2018–2019) to the south-

eastern and southern Mediterranean coastlines of the Iberian Peninsula. This

bloom could have been associated with the temperature peak in July 2015 and

was thus possibly linked to global warming.

Keywords: Bioinvasion, Rugulopteryx, SBPQ method, global warming, Strait of

Gibraltar, ecological impact

1. Introduction

The global phenomenon of NIS (non-indigenous species) is considered one of the

greatest threats to native biodiversity and the value of resources in the world's

oceans (Molnar et al., 2008). NIS may cause severe ecological impacts by

modifying the invaded habitat, its food webs, and community structure, as well

as by displacing native species (Viard and Comtet, 2015). Despite global climate

change being hypothesised to lead to the increased invasion of communities by

NIS (Dukes and Mooney, 1999), climate change and invasive species are most

commonly treated as independent issues (Pyke, 2007). Some empirical studies

have however specifically linked climate change to increasing abundances of

non-native species, especially in marine systems (e.g., Sorte, 2010). Previous

studies indicate that temperature increases similar to those predicted by climate

change models will have a strong impact on marine species (Sanford, 1999;
Harley, 2006; Wethey and Woodin, 2008), but less is known about the responses

of marine invaders relative to native species (Carlton, 2010).

The Strait of Gibraltar is a biodiversity hotspot, where the Lusitanian,

Mauritanian, and Mediterranean provinces converge within the Atlantic-

Mediterranean biogeographic subregion (Ekman, 1953; Briggs, 1974; García-

Gómez, 2002). Furthermore, it is one of the enclaves with the highest maritime

traffic in the world (Endrina, 2018), and has been subject to increasing water

temperatures. In the north of the strait, the coastal water temperature rose during

the period 2000–2017, reaching a maximum monthly mean of 23.9°C in July

2015 (Consejería de Agricultura, Ganadería, Pesca y Desarrollo Sostenible,

2019). This area is thus exposed to multiple local, regional, and global

environmental changes, making it able to provide valuable information about

alterations driven by climate change, as well as the intrusion of potentially

invasive species. In this context, five invasive species have previously been

recorded in southern Spain (Andalusian coast): Asparagopsis armata Harvey, A.

taxiformis (Delile) Trevisan de Saint-Léon, Caulerpa cylindracea Sonder,

Sargassum muticum (Yendo) Fensholt, and Codium fragile (Suringar) Hariot

(e.g., Figs. 1E to G; Altamirano et al., 2010).

Rugulopteryx okamurae (E.Y.Dawson) I.K.Hwang, W.J.Lee and H.S.Kim

(Dictyotales, Ochrophyta) is a common phaeophyceae in the temperate areas of

the Northwest Pacific (e.g., Philippines, Taiwan, China, Korea, and Japan - see
Huang, 1994) but it ranges from tropical areas to the Gulf of California (see also

Norris, 2010). In the Mediterranean, it is an exotic seaweed that has been recorded

since 2002 in the northwestern zone where it was accidentally introduced in the

Thau lagoon of the French coast through seed importation for Japanese oyster

(Crassostrea gigas [Thunberg]) culturing (Verlaque, 2009). In 2015, R.

okamurae was detected off the coast of Ceuta (North Africa), and one year later

it covered most of the area’s illuminated rocky bottoms, resulting in the municipal

cleaning machines removing more than 5,000 tons of algal biomass from Ceuta’s

beaches (Ocaña et al., 2016; Figs. 1A and B). Between 2015 and 2016, R.

okamurae colonised most of the rocky bottoms of the shoreline of the Strait of

Gibraltar (García-Gómez et al., 2018). Preliminary observations of R. okamurae

in the Strait of Gibraltar (Altamirano-Jeschke et al., 2016; Altamirano-Jeschke et

al., 2017; El Aamri, 2018; García-Gómez et al., 2018) indicate that the aggressive

invasion process, and the ecological and landscape impacts provoked by this alga,

is unprecedented in European waters.

INSERT FIG. 1 (COLOR PLATE)

A preliminary distribution map of R. okamurae in the Strait of Gibraltar has been

constructed by García-Gómez et al. (2018). Within the limits indicated in this

map, it was the dominant seaweed in the macrophytobenthos, while it seems to

be completely absent outside of those limits except as wrack deposits on coasts.

Particularly concerning are its effects on the El Estrecho Natural Park, which is
integrated into the Intercontinental Reserve of the Biosphere of Andalusia (Spain)

and Morocco. Other algal invasions, such as Lophocladia lallemandi (Montagne)

F. Schmitz, 1893 in the Balearic Islands (Patzner, 1998; Ballesteros et al., 2007),

or Undaria pinnatifida (Harvey) Suringar, 1873 in the United Kingdom (Epstein

and Smale, 2017), have occurred in the western Mediterranean or eastern

Atlantic. However, none with such expansive virulence and restricted to such

very close limits, especially when these limits do not seem to constitute a strict

barrier for any of the other native species that live within the Strait including the

abovementioned invasive species (García-Gómez et al., 2018).

One of the main actions for the prevention and management of biological

invasions of NIS is early detection (Galil et al., 2018), which can be done through

the monitoring of representative taxons as substitutive of the whole community

(Puente and Juanes, 2008). In this respect, García-Gómez (2015) proposed the

sessile bioindicators permanent quadrats (SBPQ) monitoring methodology,

implemented in submarine sentinel stations. This methodology focuses on

bioindicator species and their periodic photographic monitoring through

revisiting fixed quadrats. This approach may also facilitate the early detection of

benthic NIS species.

This study aimed to evaluate the potential impact of the NIS R. okamurae on local

biodiversity. Specifically, the main objectives were to: (1) describe a process of

sudden invasion that threatens to expand uncontrollably; (2) provide information

about the bathymetric distribution of R. okamurae; (3) update the information on

its geographical distribution in the Strait of Gibraltar, establishing the present

state of this biological invasion (i.e., whether it is in expansion, regression, or

equilibrium); and (4) to validate the SBPQ method (García-Gómez, 2015) for the

monitoring and early detection of allochthonous benthic species.

2. Material and methods

2.1. Geographical distribution: progress in the new area of invasion

Field surveys to measure the distribution of R. okamurae along the coasts of the

Strait of Gibraltar and nearby areas were carried out by SCUBA between August

2018 and July 2019. The survey area included the Marine Protected Areas

(MPAs) of the Andalusian Intercontinental Biosphere Reserve (Spain-Morocco),

the Site of Community Importance (SCI) of Monte Hacho, as well as

Calamocarro-Benzú in Ceuta, and the Jbel Moussa Site of Biological and

Ecological Interest (SIBE). Both the southern European coast, from Chipiona

(36°44'19.06"N, 6°25'59.51"W; southern Atlantic coast of Andalusia) to

Benalmádena (36°36'1.75"N, 4°30'55.75"W; southern Mediterranean coast of

Andalusia), and the North-African coast, from Oued el Marsa, Morocco

(35°54’22.9”N, 5°26’32.9”W) to Ceuta Sur (35°52’30.3”N, 5°19’56.2”W) were

surveyed. Within these shorelines, R. okamurae presence/absence was sampled

every 10–20 km. During the dives, the occurrence of the species was checked, as

well as whether it was attached to the substrate or detached (i.e. floating in the
water column, forming rugs of loose specimens on the sea bottom, or as supra-

littoral wrack deposits). Absence was inferred deeper than 15 m if R. okamurae

was not present in rocky areas shallower than 15 m.

2.2.Bathymetric study

To test the invasive capacity of space colonisation of R. okamurae across different

depths in the Strait of Gibraltar, we selected the Ceuta coastline (North Bay). To

obtain more detailed data on algal coverage, three transects perpendicular to the

shoreline were established in August on natural substrate along the northern coast

of the Monte Hacho SCI in Ceuta (Fig. 2A). Transects ran from the shallow

Ciclón beach (35°54’05.1”N, 5°17’53.9”W) to the deeper Ciclón de Más Afuera

submerged natural reef (35°55’34.5”N, 5°20’62.1”W). For each transect, five 50

× 50 cm quadrats were placed randomly and photographed at six depths (0, 5, 10,

20, 30, and 40 m) over horizontal rocky surfaces (Dumas et al., 2009). Species

percent coverage was obtained from images by superposing a 10 × 10 grid over

the photo-quadrats and counting species occurrence in each cell of the grid

(García-Gómez, 2015). This methodology overestimates the cover of each

individual species, and so the total cover in each quadrat may exceed 100%.

One-way ANOVA and Tukey HSD post-hoc tests were carried out to test

differences in the R. okamurae coverage across the six different depths.

Homogeneity of dispersions were tested using the Levene’s test. IBM SPSS

Statistics 25.0 software was used for the analyses.

2.3.Submarine sentinel station and SBPQ monitoring study

The sentinel SBPQ method for sessile and sensitive indicator species monitoring

has been proposed in previous work (Chapter 9 in García-Gómez, 2015). The

Island of Tarifa SBPQ submarine sentinel station (36°00’15.5”N, 5°36’56”W) is

located within the maximum protection area of the “El Estrecho” MPA (Fig. 2B).

This SBPQ sentinel station is composed of three 1 × 1 m fixed quadrats, separated

5–10 m from each other and located on partially shaded vertical walls of the

precoralligenous habitat at 15 m depth. To monitor coverage of NIS (mainly A.

armata and Caulerpa cylindracea Sonder) and bioindicator species (i.e.,

Paramuricea clavata [Risso] and Astroides calycularis [Pallas] - see all

bioindicator species for the studied area in García-Gómez, 2015), the station was

photographed several times each year between 2013 and 2017 to account for

intra-annual and seasonal variability. Species coverage (percent) was obtained as

in section 2.2.

A Bray–Curtis similarity matrix was obtained from the square root transformed

coverage data. For an overall visualisation of the spatial distribution of replicates

among years, a non-metric Multi-Dimensional Scaling (nMDS) ordination was

carried out in which samples were grouped by year (five levels; 2013–2017). This

resemblance matrix was used to perform a PERMANOVA analysis using a nested

design, with the sampling times as a random factor nested within the year. Type

II sum of squares was utilised to exclude season variability before testing the
effect of year as a factor. This analysis was repeated, excluding R. okamurae from

the data to identify the variation caused by this species. For both PERMANOVA

tests, PERMDISP analyses were also carried out to test the homogeneity of the

data dispersion among years (Anderson, 2006). The analysis was carried out

using PRIMER-e v6 PERMANOVA+ software (Clarke and Gorley, 2006;

Anderson et al., 2008).

3. Results

3.1.Geographical distribution: progress in the new area of invasion

The updated geographical distribution map of R. okamurae on the coasts of the

Strait of Gibraltar and nearby areas is shown in Fig. 2. The alga is not found

attached in sandy coastal stretches, but the frequent presence rocky outcrops, even

in sandy zones, appear to have facilitated its expansion. In relation to a previous

publication (García-Gómez et al., 2018) in which the invasive species was

registered exclusively in 2015–2016 between Tarifa (36° 0'10.24"N,

5°36'32.87"W) and Gibraltar (36° 6'50.41"N, 5°20'38.77"W) (including the bay

of Algeciras), we show that in 2017–2018 it advanced from Tarifa to Trafalgar-

Caños de Meca (36°10'55.9”N, 6°02’04.4”W - southern Atlantic coast of

Andalusia). By July 2019, it had advanced from Trafalgar to Cape Roche

(36º17’46.4”N, 6º08’33.1”W - southern Atlantic coast of Andalusia) and from

Gibraltar to Marbella (36º29’58.0”N, 4º55’34.2”W - southern Mediterranean

coast of Andalusia) (Fig. 2).

INSERT FIG. 2

3.2.Bathymetric study

In the North Bay of Ceuta, R. okamurae was present from 0–40 m depth. High

coverage (i.e. from 70–100% - see landscape picture in Fig. 1D), were recorded

within a wide bathymetrical range, from 5–30 m depth (Fig. 3). Besides its

overwhelming growth at the subtidal levels, it was also observed in the shadowed

areas of intertidal pools (e.g., Fig. 1).

INSERT FIG. 3

3.3.Submarine sentinel station and SBPQ monitoring study

At the SBPQ monitoring station (with fixed quadrats located on a vertical rocky

wall partially shaded with sciaphilic species) on the Island of Tarifa, the first

record of R. okamurae was in 2016. Soon after in 2017, exponential growth of up

to 65% average cover was recorded, much to the detriment of the coverage of

Mesophyllum sp. and Astroides calycularis (threatened species), clearly reflecting

the impact within partially shaded areas (Supplementary Table 1; Fig. 4). These

findings demonstrate the effectiveness of SBPQ sentinel stations in the early

detection of sessile exotic species with invasive potential in specific habitats, as

well as for the environmental monitoring of threatened sessile species. Species

with less than 10% coverage (Alcyonium sp., Aplidium sp., Asparagopsis armata

Harvey, Crambe sp., Ircinia sp., and Polycitor adriaticus [Drasche]) were

grouped under ‘Other species’. The increase in R. okamurae coverage has driven

a large change in a short time in community composition one year after the first

recordings of this species on the Island of Tarifa sentinel stations (Table 1; Fig.

5).

INSERT FIG. 4

INSERT FIG. 5

4. Discussion

4.1.A cryptic invasion?

According to Morais and Reichard (2017), “Cryptic invasions are defined as the

introduction and spread of non-native lineages within the species' native range

(intra-specific cryptic invasion) or the invasion of non-native species that goes

unnoticed due to misidentification as a native or another invasive species (inter-

specific cryptic invasion)”. In this sense, R. okamurae was initially confused (in

2015) with Dictyota pinnatifida. Although it may be common for an introduced

exotic species to be cryptic (due to its low abundance or being confused with

other native species) until environmental conditions allow it to become invasive,

R. okamurae was not detected between 2013 and 2015 at the underwater sentinel

SBPQ station of the Island of Tarifa. It should be mentioned here that this station
was not in the best possible environment for this alga, because it was partially

shaded, with the presence of the sciaphilic orange coral Astroides calycularis. R.

okamurae started appearing in 2016, and then expanded exponentially at the

expense of native species. On the other hand, the sudden appearance and

demographic bloom in the opposite side of the Strait of Gibraltar (i.e., in Ceuta,

2015), suggests that the species had previously established on the North African

coast of the strait before that time, but it was probably unnoticed due to its

similarity to some local species (i.e. Dictyota dichotoma [Hudson]

J.V.Lamouroux)(see Supplementary Fig. 1 for some diagnostic characters to

distinguish R. okamurae from other dyctiotaceans in the Strait of Gibraltar).

4.2.Bathymetry and geographical distribution

The confinement of R. okamurae near the limits of the Strait of Gibraltar, and the

environmental impact detected in this area (relevant on a wider scale because of

the coalescence of the Mauritanian, Lusitanian, and Mediterranean

biogeographical regions - Ekman, 1953; Briggs, 1974; García-Gómez, 2002), are

of great concern given that this species may progressively expand to both the

Mediterranean and the Atlantic. With the information available (we do not have

additional information about any possible progress in Moroccan coasts) the

updated distribution within the northern coast of the Strait of Gibraltar shows a

substantial expansion both westwards and eastwards.

In the Pacific, R. okamurae grows in areas shallower than 15 metres and is present

throughout the year, though it is more abundant during the summer months as the

thallus is reduced to a basal system of perennial rhizoids in winter (Kajimura,

1992; Hwang et al., 2009). This situation is similar to that observed in the waters

of the Strait of Gibraltar (García-Gómez et al., 2018), although here, R. okamurae

were found from the intertidal pools down to 40 metres depth. The highest

densities, occurring between five and 30 metres, were associated with well-lit

horizontal surfaces (see Fig. 3).

4.3.Competitiveness against native biodiversity, other invasive algae, and

threatened animal species

The results highlight the high competitiveness of the invasive species R.

okamurae (i.e., over 90% coverage between ten and 20 metres depth), resulting

in a severe impact on sessile native macrobiota. Navarro-Barranco et al. (2019)

have established that despite the high similarity between Dictyota dichotoma and

R. okamurae, both habitat-forming species hosted different macrofaunal

assemblages, but the assemblages in D. dichotoma showed lower number of

species, abundance of individuals, and diversity values than the introduced

macroalga.

In relation to other invasive macroalgae species in the Strait of Gibraltar,

halogenated compounds have been identified in Asparagopsis taxiformis and A.

armata (Burreson et al., 1976; McConnell and Fenical, 1977; Woolard et al.,
1979), with strong antifungal and antibiotic activity (Genovese et al., 2012; Greff,

2017a). On the other hand, Caulerpa cylindracea, which is strongly defended by

the toxin caulerpenyne, indirectly causes coral mortality by enhancing microbial

activity via the release of dissolved compounds. This creates a positive feedback

loop whereby compounds released by algae enhance the microbial activity on live

coral surfaces, subsequently causing mortality of coral tissue and supporting

further algal growth (Smith et al., 2006). However, although A. armata, A.

taxiformis, and C. cylindracea exhibit a strong invasive behaviour and are

included in the list of the '100 Worst Invasives in the Mediterranean Sea'

(Streftaris and Zenetos, 2006), in the Strait of Gibraltar, R. okamurae is more

competitive than these three invasive species and displaces all three when they

interact (García-Gómez et al., 2018; J.C. García-Gómez personal observation). In

this regard, R. okamurae is strongly defended by sesquiterpenes and other anti-

herbivory bioactive compounds (Paula et al., 2011), which could have influenced

its invasive behaviour and the displacement of previously established algae in

shallow well-lit areas of the strait. On the other hand, a recent study has shown

that the interaction between the invasive alga A. taxiformis and the threatened

species Astroides calycularis (orange coral) induces changes in the microbiome

and metabolomic fingerprints of the latter, an induction related to the expression

of bioactive metabolites on the macroalgal surface (Greff et al., 2017b). This

phenomenon might represent an immediate defensive response of the macroalga,

or an allelopathic offense against the coral. In the future, it should be checked

whether R. okamurae outcompetes A. calycularis for space as described above

inducing changes in the microbiome and metabolomic fingerprints of the latter.

4.4.Possible introduction vectors and environmental variables that may have

favoured the expansion of R. okamurae in the Strait of Gibraltar

In the Mediterranean, R. okamurae was reported by (Verlaque et al., 2009) on the

French coast, probably introduced through the importation of the Japanese oyster

for aquaculture. From the area it was first recorded (in the coastal lagoon of

Thau), the species did not manage to expand in an invasive way. However, by a

hitherto unknown vector, presumably the ballast waters of the Asian vessels

anchored in the Bay of Algeciras or Tanger Med (in the northern and southern

coasts of the strait, respectively), the alga landed in the Strait of Gibraltar with an

overflowing invasive potential. Notably, importation associated to oyster

aquaculture cannot be discarded as also being responsible in this area, as it is a

common activity in southern Spain (Ministerio de Agricultura Pesca y

Alimentación, 2019). Pulido and Altamirano (2017) pointed out that R. okamurae

is fertile in the Strait of Gibraltar throughout the year, but only by vegetative

spores, as its sexual reproduction has not yet been observed. However, the sexual

reproductive structures and maximum growth of this species occur in the natural

environment at temperatures above 15°C, thus restricting reproduction to be

exclusively asexual at the limits of its distribution at high latitudes (Hwang et al.,

2009).
Rugulopteryx okamurae is a temperate to subtropical species (Verlaque et al.,

2009) and the sea temperature in the Strait of Gibraltar is ideal for it (El Aamri et

al., 2018): in this area, monthly mean temperature almost never fall below 15ºC

all along the year and the maintained temperature peaks in summer may be a key

factor for the explosivity (blooming) of the species. The explosive growth of R.

okamurae documented in a very short time in Ceuta also coincided with the

maximum SST in the Strait of Gibraltar and nearby areas in the period between

2000–2017, peaking at 23.9°C in July 2015 (Fig. 6). This also coincides with a

decrease of other abundant Laminariales macroalgae in the area, such as

Laminaria ochroleuca Bachelot de la Pylaie, and Saccorhiza polyschides

(Lightfoot) Batters (García-Gómez and Magariño personal observations), which

have colder thermal demands as the upper limit for the reproduction of the

gametophyte for both species is 21°C (Lüning, 1990) and <17°C (Norton, 1970),

respectively.

INSERT FIG. 6

Based on the temperature tolerance and survival predicted by Sorte et al. (2010)

for marine fouling, as the ocean temperature increases, native species will

decrease in abundance (they are expected to move poleward; Occhipinti-

Ambrogi and Galil, 2010), whereas introduced species more tolerant of higher

temperatures are likely to increase. In this regard, the greatest effects of climate

change on benthic communities may be due to changes in the maximum and

minimum temperatures rather than the annual means (Stachowicz et al., 2002).

Sorte et al. (2010) suggest that by giving introduced species an earlier start and

increasing the magnitude of their growth and recruitment relative to natives,

global warming may facilitate a shift to dominance by NIS, accelerating the

homogenisation of the global biota. The explained scenario is consistent with

the process illustrated by Occhipinti-Ambrogi (2007), in which a NIS

population established in a new environment (stage 3 – i.e., in North Africa

before the local bloom in 2015 when R. okamurae was still unnoticed), and then

become locally dominant (stage 4b), facilitated by some favourable physical-

chemical factors (it was coincident with the July 2015 temperature peak of

23.9ºC). The posterior catastrophic expansion between 2015 and 2017 (stage 5;

Occhipinti-Ambrogi, 2007) could have been facilitated by the propagule

pressure generated after the local bloom in Ceuta in 2015. Therefore, we

hypothesised that it was first installed in the southern coast of the Strait of

Gibraltar and after that in its northern coast, where the submarine sentinel

station on the Island of Tarifa detected it despite being in partially shaded

habitats (vertical rocky surfaces of the precoralligenous habitats) in July 2016.

However, R. okamurae could have been established prior to this date on the

coast of Tarifa on illuminated horizontal rocky surfaces, much more suitable for

its establishment and uncontrolled expansion, as has been observed. According

to the available data, it is plausible to consider that the primary vector for the

species could be the Port of Tangier, or an area close to it, by colonising the
species first south of the Strait of Gibraltar and then crossing it by means of its

propagules. Regardless of the Western Alboran Gyre, which expands from the

south to the north in the eastern area of the Strait of Gibraltar (Rodríguez et al.,

1982; Periañez, 2007), it has also been shown that in the central part of the

strait, the commonest westward currents flux from the coast of Africa to the

Atlantic and can cross to the north shore with tide coefficients higher than 0.93

(Bustamante, 1979). This information would support the aforementioned

hypothesis. On the other hand, modelling studies with particle injection in the

western part of the Strait of Gibraltar (García-Lafuente et al., 2013) allow us to

infer the viability, in some circumstances, of connections from the south to the

north (despite the powerful central surface current from the Atlantic to the

Mediterranean, which may impede the connectivity between the Atlantic coasts

of the Strait of Gibraltar). Furthermore, the northern and southern coasts of the

Strait of Gibraltar are very frequently connected, with about 20,000 ferries per

year (Port Authority of Algeciras Bay, 2019).

This invasive bloom of the benthic R. okamurae only seems to be comparable to

the blooms of pelagic Sargassum spp. in the western Atlantic (Sargassum fluitans

[Børgesen] Børgesen and Sargassum natans [Linnaeus] Gaillon according to

Franks et al. [2011] and Smetacek and Zingone [2013]), detected for the first time

in 2011 in the Caribbean and in 2013 on the coasts of Africa (Langin, 2018). The

great difference of the case of Sargassum spp. with that of R. okamurae is that
this last species is exotic and comes from Asia, while S. fluitans and S. natans are

native species of the Western Atlantic. According to van Tussenbroek et al.

(2017), the latter species had been reported previously in the Caribbean Sea, but

with low abundance and at irregular intervals, and their arrival was possibly due

to seasonal export from the Sargasso Sea in the northwestern mid-Atlantic;

known as the Sargasso Loop System (Frazier, 2014). Subsequently, other authors

(van Tussenbroek et al., 2017) suggested that a new ocean scale accumulation of

drifting Sargassum spp. in 2012 extended throughout the North Atlantic

Recirculation Region (NARR - Johnson et al., 2013; Smetacek and Zingone,

2013; Oyesiku and Egunyomi, 2014), and was probably related to an area off the

coast of Brazil fed by the Sargassum spp. that had bloomed in the NARR

(Johnson et al., 2013; Franks et al., 2016). In this sense, a recurrent great Atlantic

Sargassum belt has been observed in satellite imagery since 2011, often

extending from West Africa to the Gulf of Mexico, and containing >20 million

metric tons (June 2018) of Sargassum biomass. This suggests that recent

increases and interannual variability after 2011 appear to be driven by upwelling

off West Africa during boreal winter, and by Amazon River discharge during

spring and summer (Wung et al., 2019). Unlike these two species of Sargassum,

the introduction and subsequent expansion of R. okamurae have only been related

to aquaculture and ballast water of large merchant ships. Finally, the comparison

with the pelagic Sargassum suggests that the intervention of an additional source

of nutrients could also be involved in the observed explosive biomass production.

The Strait of Gibraltar and nearly areas represent an environmentally and socially

complex scenario where potential sources of additional nutrients have been

described (e.g., wind driven upwelling on the African coast of the Strait -

Stanichny et al., 2005; increasing human-mediated eutrophication - Powley et al.,

2018), but a link between this invasion and an additional source of nutrients is

not yet clear.

The factors favouring invasive behaviour of NIS are the increase in genetic

variation, decrease or absence of natural enemies, biotic regulation, purge or

purification, adaptive mutations, and epigenetic changes (Pérez et al., 2010).

None of these factors have yet been assessed for R. okamurae, but these results

indicate that its competitive potential is unrivalled, even by the rest of the invasive

species of the area.

Acknowledgments

We are deeply grateful to the CEPSA Foundation for its initiative to support and

finance scientific research related to the environmental impact of the invasive

species R. okamurae on the marine autochthonous biodiversity of the Bay of

Algeciras, Strait of Gibraltar and nearby areas. Also, this work has benefitted

from the scientific equipment acquired in project number 1889, related to the

estuary of the Guadalquivir River, co-financed by the Port Authority of Seville,

the Seville Aquarium and the University of Seville, as well as related

environmental campaigns and controls in the areas near the mouth of the
mentioned river. Thanks to the Diving Club Campo de Gibraltar, La Linea, and

to the CIES Club, Algeciras for their logistic support in the development of the

campaigns on the North Coast of the Strait. We also thank “El Estrecho” Natural

Park and its director, Jorge Serradilla, as well as Verdemar -Ecologistas en

Acción, Agaden Ecologistas and Asociación de Alumnas “Algas del Estrecho”

(special mention: Antonio Vegara). We also express our gratitude to Stephen

Warr and Clive Crisp (Department of Environment and Climate Change,

Gibraltar), as well as Darren Fa (University of Gibraltar) for providing

information about R. okamurae in Gibraltar. From the Marine Biology Station of

the Strait (Ceuta) we would also like to thank Watergames Gran Azul diving club,

Marina Hércules S.A. and OBIMASA, Consejería de Medio Ambiente y

Sostenibilidad, Autonomous City of Ceuta.

References

Altamirano, M., de la Rosa, J., Dana, E.D., Fernández, E., 2010. Algas invasoras

en las costas andaluzas. Quercus. 293.

Altamirano-Jeschke, M., de la Rosa Álamos, J., Martínez Medina, F.J., 2016.

Arribazones de la especie exótica Rugulopteryx okamurae (EY Dawson) en el

Estrecho de Gibraltar. RIUMA. Available from:

http://hdl.handle.net/10630/12433/ (accessed on August 2019).

Altamirano-Jeschke, M., de la Rosa, J., Gil, F.J.M., Gallego, A.R.M., 2017.

Prolifera en el Estrecho un alga nunca citada en nuestro litoral de origen asiático,

"Rugulopteryx okamurae" ocupa ya una gran extensión. Quercus. 374, 32-33.

Amade, P., Lemée, R., 1998. Chemical defence of the Mediterranean alga

Caulerpa taxifolia: variations in caulerpenyne production. Aquat Toxicol. 43,

287-300.

Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA for PRIMER:

Guide to Software and Statistical Methods. PRIMER-E, Plymouth.

Anderson, M.J., 2006. Distance-based tests for homogeneity of multivariate

dispersions. Biometrics. 62, 245–253.

Ballesteros, E., Cebrian, E., Alcoverro, T., 2007. Mortality of shoots of Posidonia

oceanica following meadow invasion by the red alga Lophocladia lallemandii.

Botanica Marina. 50, 8-13.

Briggs, J.C., 1974. Marine Zoogeography. McGraw-Hill Book Company.

Burreson, B.J., Moore, R.E., Roller, P.P., 1976. Volatile halogen compounds in

the alga Asparagopsis taxiformis (Rhodophyta). J. Agric Food Chem. 24, 856–

861.

Bustamante, J.M., 1979. Corrientes en el Estrecho de Gibraltar. Boletín del

Instituto Español de Oceanografía. 5, 1-191.

Carlton, J.T., 2000. Global change and biological invasions in the oceans.

Invasive species in a changing world. 31-53.

Clarke, K.R., Gorley, R.N., 2006. Plymouth: Primer-E. PRIMER v6: User

manual/tutorial.

Consejería de Agricultura, Ganadería, Pesca y Desarrollo Sostenible, 2019.

Environmental Information Network of Andalusia.

http://laboratoriorediam.cica.es/geonetwork (accessed on August 2019).

Dumas, P., Bertaud, A., Peignon, C., Leopold, M., Pelletier, D., 2009. A “quick

and clean” photographic method for the description of coral reef habitats. J Exp

Mar Biol Ecol. 368, 161-168.

Dukes, J.S., Mooney, H.A., 1999. Does global change increase the success of

biological invaders?. Trends Ecol Evol. 14, 135–139.

Ekman, S., 1953. Zoogeography of the sea. 1-417. Sidgwick & Jackson, London.

El Aamri, F., Idhalla, M., Tamsouri, M.N., 2018. Occurrence of the invasive

brown seaweed Rugulopteryx okamurae (EY Dawson) IK Hwang, WJ Lee & HS

Kim (Dictyotales, Phaeophyta) in Morocco (Mediterranean Sea). MedFAR. 1,

92-96.

Endrina, N., Rasero, J.C., Konovessis, D., 2018. Risk analysis for RoPax vessels:

A case of study for the Strait of Gibraltar. Ocean Eng. 151, 141-151.

Epstein, G., Smale, D.A., 2017. Environmental and ecological factors influencing

the spillover of the non-native kelp, Undaria pinnatifida, from marinas into

natural rocky reef communities. Biol Invasions. 20, 1049-1072.

Franks, J., Johnson, D., Ko, D-S., Sanchez-Rubio, G., Hendon, R., Lay, M., 2011.

Unprecedented Influx of Pelagic Sargassum Along Caribbean Island Coastlines

During 2011. 64. Gulf and Caribbean Fisheries Institute. 6–8.

Franks, J., Johnson, D., Ko, D-S., 2016. Pelagic Sargassum in the tropical North

Atlantic. Gulf and Caribbean Research. 27, SC6–SC11.

Frazier, J., 2014. Advanced Prediction of the Intra-Americas Sargassum Season

Through Analysis of the Sargassum Loop System Using Remote Sensing

Technology. (Doctoral dissertation) A & M University, Texas.

Galil, B.S., Marchini, A., Occhipinti-Ambrogi, A., 2018. East is east and West is

west? Management of marine bioinvasions in the Mediterranean Sea. Est Coast

Shelf Sci. 201, 7-16.

García-Gómez, J.C., 2002. Paradigmas de una fauna insólita. Los Moluscos

Opistobranquios del Estrecho de Gibraltar. Serie Ciencias, 20 IECG. 1-397.

García-Gómez, J.C., 2015. A guide on environmental monitoring of rocky

seabeds in Mediterranean Marine Protected Areas and surrounding zones.

RAC/SPA-MedMPAnet Project, Tunis. 1-491.

García-Gómez, J.C., Sempere-Valverde, J., Ostalé-Valriberas, E., Martínez, M.,

Olaya-Ponzone, L., González, A.R., Espinosa, F., Sánchez-Moyano, J.E.,

Megina, C., Parada, J.A., 2018. Rugulopteryx okamurae (EY Dawson) IK

Hwang, WJ Lee & HS Kim (Dictyotales, Ochrophyta), alga exótica “explosiva”

en el estrecho de Gibraltar. Observaciones preliminares de su distribución e

impacto. Almoraima. 49. (http://institutoecg.es/wp-

content/uploads/2019/03/Almoraima49-97-114.pdf)

García-Lafuente, J., Bruque Pozas, E., Sánchez-Garrido, J.C., Sannino, G.,

Sammartino, S., 2013. The interface mixing layer and the tidal dynamics at the

eastern part of the Strait of Gibraltar. J Mar Syst. 117, 31–42.

Genovese, G., Faggio, C., Gugliandolo, C.., Torre, A., Spanò, A., Morabito, M.,

Maugeri, T.L., 2012. In vitro evaluation of antibacterial activity of Asparagopsis

taxiformis from the Straits of Messina against pathogens relevant in aquaculture.

Mar Environ Res. 73, 1–6.

Greff, S., Zubia, M., Payri, C., Thomas, O.P., Perez, T., 2017a. Chemogeography

of the red macroalgae Asparagopsis: metabolomics, bioactivity, and relation to

invasiveness. Metabolomics. 13, 33.

Greff, S., Aires, T., Serrão, E.A., Engelen, A.H., Thomas, O.P., Pérez, T., 2017b.

The interaction between the proliferating macroalga Asparagopsis taxiformis and

the coral Astroides calycularis induces changes in microbiome and metabolomic

fingerprints. Sci Rep. 7, 42625.

Harley, C.D., Randall Hughes, A., Hultgren, K.M., Miner, B.G., Sorte, C.J., 2006.

Thornber CS, et al. The impacts of climate change in coastal marine systems.

Ecol Lett. 9, 228–241.

Huang, Z.G., 1994. Marine Species and their distributions in China’s Seas. China

Ocean Press. Beijing.

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, 1-12.

Johnson, D.R., Ko, D.S., Franks, J.S., Moreno, P., Sanchez-Rubio, G., 2013. The

Sargassum Invasion of the Eastern Caribbean and Dynamics of the Equatorial

North Atlantic. 65. GCFI. 102–103.

Kajimura, M., 1992. Vegetative propagation in Dilophus okamurae and Zonaria

flabellata (Dictyotaceae, Phaeophyta). Shimane University. 26, 95-106.

Langin, K., 2018. Seaweed masses assault Caribbean islands. Science. 360, 1157-

1158.
McConnell, O., Fenical, W., 1977. Halogen chemistry of the red alga

Asparagopsis. Phytochemistry. 16, 367–374.

Lüning, K., 1990. Seaweeds: their environment, biogeography, and

ecophysiology. John Wiley & Sons. New York.

Ministerio de Agricultura Pesca y Alimentación, 2019. Directorio de

Instalaciones; Acuicultura; Andalucía.

http://www.mapa.gob.es/app/instalaciones/listado_instalaciones.asp?CCAA=1

(accessed on August 2019).

Molnar, J.L., Gamboa, R.L., Revenga, C., Spalding, M.D., 2008. Assessing the

global threat of invasive species to marine biodiversity. Front Ecol Environ. 6,

485–492.

Morais, P., Reichard, M., 2017. Cryptic invasions: A review. Science of the Total

Environment. 613, 1438-1448.

Navarro-Barranco, C., Muñoz-Gómez, B., Saiz, D., Ros, M., Guerra-García,

J.M., Altamirano, M., Ostalé-Valriberas, E., Moreira, J., 2019. Can invasive

habitat-forming species play the same role as native ones? The case of the exotic
marine macroalga Rugulopteryx okamurae in the Strait of Gibraltar. Biol

Invasions. 1-16.

Norris, J.N., 2010. Marine Algae of the Northern Gulf of California: Chlorophyta

and Phaeophyceae. Smithsonian Contributions to Botany.

Norton, T.A., 1970. Synopsis of biological data on Saccorhiza polyschides. FAO

Fisheries Synopsis. 83, 1-35.

Ocaña, O., Alfonso-Carrillo, J.M., Ballesteros, E., 2016. Massive proliferation of

a dictyotalean species (Phacophyccae, Ochriohyta) througn the strait of Gibraltar.

Rev Acad Canaria Cien. 28, 165-169.

Oyesiku, O.O., Egunyomi, A., 2014. Identification and chemical studies of

pelagic masses of Sargassum natans (Linnaeus) Gaillon and S. fluitans

(Borgesen) Borgesen (brown algae), found offshore in Ondo State, Nigeria. Afr.

J. Biotechnol. 13, 1188–1193.

Patzner, R.A., 1998. The invasion of Lophocladia (Rhodomelaceae,

Lophotalieae) at the northern coast of Ibiza (Baleares, western Mediterranean

Sea). SHNB. 41, 75-80.

Pérez, J.E., Gómez, J.A., Alfonsi, C., Nirchio, M., Muñoz, C., 2010. ¿Cómo una

especie exótica se convierte en invasora? Tecnociencia. 12, 103-118.

Periañez, R., 2007. Chemical and oil spill rapid response modelling in the Strait

of Gibraltar–Alboran Sea. Ecol modell. 207, 210–222.

Port Authority of Algeciras Bay, 2019. Stats. https://www.apba.es/en/stats/

(accessed on August 2019).

Puente, A., Juanes, J.A., 2008. Testing taxonomic resolution, data transformation

and selection of species for monitoring macroalgae communities. Estuar Coast

Shelf Sci. 78, 327-340.

Paula, J.C.D., Vallim, M.A., Teixeira, V.L., 2011. What are and where are the

bioactive terpenoids metabolites from Dictyotaceae (Phaeophyceae). Rev Bras

Farmacogn. 21, 216-228.

Pulido, L.C., Altamirano, J.A., 2017. Rugulopteryx okamurae (Dyctiotales,

Ochrophyta): una posible invasión críptica en el Estrecho de Gibraltar. Rivas,

ML, López-Martínez S, editors. Libro de resúmenes del II Congreso de

biodiversidad y conservación de la naturaleza: Divulgación y transferencia del

conocimiento entre los distintos sectores de la sociedad. Almería, España. 1-50.

Pyke, C.R., Thomas, R., Porter, R.D., Hellmann, J.J., Dukes, J.S., Lodge, D.M.,

Chavarria, G., 2007. Current Practices and Future Opportunities for Policy on

Climate Change and Invasive Species. Conserv Biol. 22, 585–592.

Rodríguez, J., García, A., Rodriguez, V., 1982. Zooplanktonic communities of

the divergence zone in the Northwestern Alboran Sea. Mar Ecol. 3, 133-142.

Sanford, E., 1999. Regulation of keystone predation by small changes in ocean

temperature. Science. 283, 2095–2097.

Smetacek, V., Zingone, A., 2013. Green and golden seaweed tides on the rise.

Nature. 504, 84–88.

Smith, .JE., Shaw, M., Edwards, R.A., Obura, D., Pantos, O., Sala, E., Sandin,

S.A., Smriga, S., Hatay, M., Rohwer, F.L., 2006. Indirect effects of algae on

coral: algae-mediated, microbe-induced coral mortality. Ecol Lett. 9, 835–845.

Sorte, C.J.B., Williams, S.L., Zerebecki, R.A., 2010. Ocean warming increases

threat of invasive species in a marine fouling community. Ecology. 91, 2198–

2204.
Stachowicz, J.J., Terwin, J.R., Whitlatch, R.B., Osman, R.W., 2002. Linking

climate change and biological invasions: Ocean warming facilitates

nonindigenous species invasions. Proc Nat. Acad Sci. 99, 15497–15500.

Streftaris, N., Zenetos, A., 2006. Alien marine species in the Mediterranean-the

100 ‘Worst Invasives’ and their impact. Mediterr Mar Sc. 7, 87-118.

van Tussenbroek, B.I., Arana, H.A.H., Rodríguez-Martínez, R.E., Espinoza-

Avalos, J., Canizales-Floresa, H.M., González-Godoy, C.E., Barba-Santosa,

M.G., Vega-Zepedab, A., Collado-Videsc, L., 2017. Severe impacts of brown

tides caused by Sargassum spp. on near-shore Caribbean seagrass communities.

Marine pollution bulletin. 122(1-2), 272-281.

Verlaque, M., Steen, F., De Clerck, O., 2009. Rugulopteryx (Dictyotales,

Phaeophyceae), a genus recently introduced to the Mediterranean. Phycologia.

48, 536-542.

Viard, F., Comtet, T., 2015. Applications of DNA-based Methods for the Study

of Biological Invasions. In: Canning-Clode, J. (Eds.), Biological Invasions in

Changing Ecosystems. De Gruyter Open, pp. 410-435.

Wethey, D.S., Woodin, S.A., 2008. Ecological hindcasting of biogeographic

responses to climate change in the European intertidal zone. Hydrobiologia. 606,

139–151.

Woolard, F.X., Moore, R.E., Roller, P.P., 1979. Halogenated acetic and acrylic

acids from the red alga Asparagopsis taxiformis. Phytochemistry. 18, 617–620.
Fig. 1. Rugulopteryx okamurae, invasion and competence with other species of
invasive algae and protected invertebrates from the precoralligenous habitat. A
and B: wrack deposits in the coast of El Estrecho MPA and Algeciras Bay (La
Línea de la Concepción). C: R. okamurae growing in shadow areas of the
intertidal pools in Isla de Tarifa integral reserve (year 2018, El Estrecho MPA).
D: subtidal natural rocky bottoms totally covered by R. okamurae and thallus
detail. E, F, G: competition for space on well-illuminated surfaces and
progressive displacement of other exotic/invasive macroalgae species previously
established on the coast of the Strait of Gibraltar: Dictyota cyanoloma, Dc and
Asparagopsis armata, Aa (E), A. taxiformis, At (F) and Caulerpa cylindracea, Cr
(G). H: competition for space in partially shadow habitats from precoralligenous:
habitat occuped by the threatened species Astroides calycularis (orange coral).
2-COLUMNS

Fig. 2. Distribution of R. okamurae in the Strait of Gibraltar and nearby areas.

Map A from El Aamri et al. (2018) and García-Gómez et al. (2018), both
describing results from summer 2017, and B and C this study: B (2017-2018) and
C (2018-2019 July). The bathymetric distribution of R. okamurae was
quantitatively sampled in ‘a’ Monte Hacho Site of Community Importance in
Ceuta. Sessile Bioindicators Permanent Quadrats station is located at ‘b” Tarifa
Island, in El Estrecho MPA.
2-COLUMNS
Fig. 3. Rugulopteryx okamurae mean coverage and standard deviation error bars
within the bathymetric range from 0 to 40 metres in Monte Hacho Site of
Community Importance, Ceuta. Numbers over columns represent groups
segregated by HSD of Tukey after one-way ANOVA (F5-84 = 93.96; P <0.01).

1-COLUMN
100
90
80
70
60
50
40
30
20
10
0
1-2

2-2

3-2

4-2

1-2

2-2

3-2

1-2

2-2

3-2

4-2

1-2

3-2

4-2

1-2

2-2

3-2

4-2
01

01

01

01

01

01

01

01

01

01

01

01

01

01

01

01

01

01
3

7
A. calycularis Mesophyllum sp Oscarella sp
R. okamurae Autochthonous brown algae Other species

Fig. 4. Temporal variation of benthic mean percent species coverage at Tarifa Island monitoring station fixed quadrats from
years 2013 to 2017 (1, 2, 3, 4 refer to random sampling times within each year). Species with less than 10% coverage
(Alcyonium sp., Aplidium sp., Asparagopsis armata, Crambe sp, Ircinia sp. and Polycitor adriaticum) were grouped under
‘Other species’.

1.5-COLUMNS
 Fig. 5. nMDS ordination for Tarifa Island monitoring stations community
evolution from years 2013 to 2017

1-COLUMN
Fig. 6. Monthly variation (blue shaded area), means (green line), maximums (red
line) and minimums (blue line) of Sea Surface Temperature (SST) in the Strait of
Gibraltar from the year 2000 to 2017. Adapted from Environmental Information
Network of Andalusia (Consejería de Agricultura, Ganadería, Pesca y Desarrollo
Sostenible, 2019).

2-COLUMNS

Table 1. PERMANOVA and PERMDISP (for the factor “Year”) results for

SBPQ monitoring stations coverage data (years 2013 to 2017) using (a) all bio-

indicator and non-indigenous species coverage and (b) excluding R. okamurae

from data. Pair-wise comparisons are based in Monte-Carlo P values.

 D
SS MS Pseudo-F P
f

(a) Including Rugulopteryx okamurae

Time 1 188
145.2 1.489 0.064
(Year) 3 7.6

372
Year 4 930.84 6.411 <0.01
3.4

3 351
Res 97.53 P(PERMDISP) = 0.271
6 1

5 912 Pair-Wise: 2017 ≠ (2014 = (2013 ≠

Total
3 2 (2015 = 2016)))

(b) Excluding Rugulopteryx okamurae

Time 1 173
133.68 1.319 0.121
(Year) 3 7.8

136
Year 4 341.06 2.551 <0.01
4.2

3 364
Res 101.36 P(PERMDISP) = 0.052
6 9.1

5 675 Pair-Wise: 2014 = (2013 ≠ (2015 =

Total
3 1.2 2016 = 2017))
The authors declare that they have no conflict of interest
Highlights:

-Rugulopteryx okamurae (asiatic macroalgae): extreme invasión in the Gibraltar

Strait from 2015 and global warming as posible cause.

-High impact due to the elimination or massive displacement of native species.

-More than 90% coverage between 10 and 20 meters (Ceuta littoral).

- It has been extended in 2018-2019 along the Atlantic and Mediterranean coasts
of the Southern Iberian Peninsula.

-SBPQ submarine sentinel stations detect with precision the initial fixation of
Rugulopteryx and its later local expansion.

The authors declare that they have no conflict of interest