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BioInvasions Records (2019) Volume 8, Issue 3: 575–581

CORRECTED PROOF

Rapid Communication First record of drifting muticum (Yendo) Fensholt thalli on the Algerian coasts of Cherchell and Sidi Fredj

Myriam Benali1,*, Ilhem Djebri1, Dallal Bellouis1, Louiza-Nesrine Sellam1,2 and Chafika Rebzani-Zahaf1 1Marine Environment and Biological Oceanography Laboratory, Faculty of Sciences and Biology, University Of Science and Technology Houari Boumediene (USTHB)BP 32 El-Alia, Bab Ezzouar, Algiers, Algeria 2Aix-Marseille University, CNRS, University of Toulon, IRD,Mediterranean Institute of Oceanography (MIO), UM 110,13288 Marseille, *Corresponding author E-mail: [email protected]

Citation: Benali M, Djebri I, Bellouis D, Sellam L-N, Rebzani-Zahaf C (2019) First Abstract record of drifting (Yendo) Fensholt thalli on the Algerian The Japanese Sargassum muticum (Yendo) Fensholt is reported for the first coasts of Cherchell and Sidi Fredj. time from the Algerian coasts in Cherchell and Sidi Fredj, which are approximately BioInvasions Records 8(3): 575–581, 80 and 30 km, respectively, west of Algiers. Observations of drifting specimens, https://doi.org/10.3391/bir.2019.8.3.13 collected in March 2015 and March and April 2017, suggest that this non-indigenous Received: 6 February 2018 species has reached Algerian waters. However, S. muticum cannot yet be considered Accepted: 22 April 2019 established since the collected were not fixed to substrata, were not Published: 15 July 2019 fertile, and there was no evidence of colonization. Potential vectors of spread for S. muticum into the area include shipping, farming and circulation. In Handling editor: Christopher McKindsey the future, intensive survey and monitoring actions are needed to detect any fertile Thematic editor: Amy Fowler or attached fronds. Copyright: © Benali et al. This is an open access article distributed under terms of the Creative Commons Attribution License Key words: non-indigenous species, drifting materials, non-established, vectors, survey (Attribution 4.0 International - CC BY 4.0).

OPEN ACCESS. Introduction Sargassum muticum (Yendo) Fensholt (Phaeophyceae: ) was described for the first time from by Yendo (1907) as Sargassum Kjellmanium f. muticus. It is native to the North Western Pacific coasts (Critchley 1983; Joefsson and Jansson 2011; Engelen et al.2015) where it has been described as a minor component of the Japanese Sargassum group (Critchley 1983; Critchley et al. 1986) and as “inconspicuous” according to Givernaud (1984). However, it has also been considered as the most invasive beyond its native area by Norton (1977) and the most widespread invasive macroalgae by Engelen et al. (2015). Sargassum muticum was accidentally introduced by voluntary transfer of the Crassostrea gigas to Pacific North American coasts in the 1940s and then to European coasts in the 1970s (Supplementary material Table S1). It later spread to other parts of European shores, the and Atlantic North African coasts (Figure 1, Table S1). The alga’s invasive capacity seems to be mostly related to the following seven criteria:

Benali et al. (2019), BioInvasions Records 8(3): 575–581, https://doi.org/10.3391/bir.2019.8.3.13 575 First record of Sargassum muticum on the Algerian coasts

Figure 1. Worldwide distribution of Sargassum muticum, and main records in the Mediterranean Sea and Atlantic North African coast, with year of first observation (for details see Supplementary material Table S1).

1. A monoecious reproductive pattern, which may be the main reason for this species’ introduction and establishment success (Critchley 1983; Norton 1992); 2. A large capacity for dissemination and settlement by young germlings or adult, fertile plants, which may be carried via flotation over great distances (Deysher and Norton 1982; Norton and Deysher1989; Norton 1992; Josefsson and Jansson 2011); 3. The ability to reproduce both asexually via vegetative propagation and sexually (Loraine 1989); 4. A high fecundity rate with high propagule production (Josefsson and Jansson 2011); 5. High settlement success on various natural and artificial substrata. For example, it settles successfully on dead shells, plastic, steel, rocky blocks, and boat hulls in the Etang de Thau, an area characterized by sandy bottoms (Belsher 1991; Knoepffler-Peguy et al. 1985); 6. A high growth rate. Specimens can grow 2 to 4 cm/day in Swedish waters (Josefsson and Jansson 2011), at least 4 cm/day between April and July in Roche Harbor, Washington (Norton 1977), and up to an average of 6 cm/day over a week in May (up to 10 cm/day for the largest thalli) in the Mediterranean lagoon of Etang de Thau (Belsher 1991);

Benali et al. (2019), BioInvasions Records 8(3): 575–581, https://doi.org/10.3391/bir.2019.8.3.13 576 First record of Sargassum muticum on the Algerian coasts

Figure 2. Locations of Sargassum muticum drift algae specimens observed along the Algerian Coast.

7. Considerable ecological tolerance to temperature, irradiance, salinity variations (Hales and Fletcher 1989; Davison 2009) and disturbance; S. muticum is able to invade and then persist following disturbance (Williams and Smith 2007). This study reports the first occurrence of floating individuals of S. muticum on the Algerian coast, providing evidence for its possible further spread along the northern Africa coast. In addition, it provides morphological information on the specimens collected.

Observations in Algerian waters Two drifting specimens of Sargassum muticum were observed in March 2015 and March 2017 in Rocher Blanc (36.616943°N; 2.235121°W), a small creek about 600 m long, with low flow and stagnant waters, approximately 4 km from the fishing port of Cherchell. Another drifting plant was collected in Sidi Fredj (36.756306°N; 2.844894°W), an open sandy beach, approximately 1 km from the local marina (Figure 2). This latter alga was buried in the sandy bottom to a depth of 30 cm but was not fixed to a solid substrate. None of the three collected specimens bore receptacles (Figures 3 and 4). In the Mediterranean Sea, established and thus, attached populations are known only from Etang de Thau (France) and Venice Lagoon () (Knoepffler-Peguy et al. 1985; Curiel et al. 1998; Engelen et al. 2015). Thibaut et al. (2016) described the species as very abundant on the Languedoc coast (France) while they assumed it could have disappeared in some locations, such as Banuyls and Corsica (both in France). Only drifted specimens have been observed in Catalonia and Balearic (both in Spain)

Benali et al. (2019), BioInvasions Records 8(3): 575–581, https://doi.org/10.3391/bir.2019.8.3.13 577 First record of Sargassum muticum on the Algerian coasts

Figure 3. Holdfast, stipe, and primary branches of Sargassum muticum drift algae observed in Rocher Blanc. Photograph by Myriam Benali.

Figure 4. Blades and vesicles shapes and sizes of Sargassum muticum drift from Rocher Blanc, with lower structures on the lower left of the figure and structures further up the plant to the right and in the upper portions of the figure. Photograph by Myriam Benali.

(Gomez-Garreta 2001; Engelen et al. 2015; Aouissi et al. 2018).The vector to Algerian waters is presently unknown but may be related to shellfish which has recently increased in importance, to shipping activities via fouling, as well as via germlings that could have been transported by currents from near-by or more distant locations. These are also among the most important vectors for algae identified by Williams and Smith (2007).

Benali et al. (2019), BioInvasions Records 8(3): 575–581, https://doi.org/10.3391/bir.2019.8.3.13 578 First record of Sargassum muticum on the Algerian coasts

These first observations, within a year or two years, in two different areas, 50 km apart, confirm the species presence and arrival in Algerian waters, but not its establishment. Nevertheless, it seems important to indicate that the first records in some Atlantic areas, such as Belgium shores, The , and , were initially just observations of floating Sargassum that ultimately became important established populations. Critchley et al. (1987) reported that plants cast upon Dutch shores since 1977 preceded the presence of attached plants. Drift fronds are usually found 2–3 years prior to the discovery of attached plants in an area according to Rueness (1989). On Belgium coasts, the first observed plant was drifting (Coppejans et al. 1980). It took until 1999 (Zeebrugge) and 2000 (Sluice Dock, Oostende) before its autochthonous presence could be confirmed (Kerckhof et al. 2007). Monitoring could be done to detect the species’ presence along the Algerian coast.

Acknowledgements

We gratefully acknowledge the Aquatic Invasions team for their availability and precious recommendations. We express our deep gratitude to Chris McKindsey and Amy Fowler for their valuable and meticulous revision, both for language and scientific relevance, they significantly improved the quality of this note. We do not omit the anonymous reviewers for their pertinent remarks. The publication of this article is supported by the Open Access Publishing Fund of the International Association for Open Knowledge on Invasive Alien Species (INVASIVESNET).

References

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Supplementary material The following supplementary material is available for this article: Table S1. Main historical records of first observations of Sargassum muticum beyond its native range. Appendix S1. References to Table S1. This material is available as part of online article from: http://www.reabic.net/journals/bir/2019/Supplements/BIR_2019_Benali_etal_Table_S1.xlsx

Benali et al. (2019), BioInvasions Records 8(3): 575–581, https://doi.org/10.3391/bir.2019.8.3.13 581