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First records of non-indigenous species in port of Arzew (Algeria: southwestern Mediterranean)

Maritime transport is considered to be one of the main causes of transfer of non-indigenous species (NIS), through biofouling of ships’ hulls and ballast water. Ports and marinas constitute hot spots for the introduction of species carried by international shipping and therefore are important sites for initiating biological monitoring. In this study, the port of Arzew (Algeria, Southern Mediterranean) was surveyed for the presence of NIS and cryptogenic species. The fouling communities of floating submerged structures and the hull of a fishing vessel were sampled with a scraper blade. After fixing and separating, the organisms were identified to the lowest possible taxonomic level. The results revealed the presence of 10 NIS and cryptogenic species, including: 1 Ascidiacea, 2 Bryozoa, 3 Crustacea, 1 Mollusca, 1 Porifera, and 2 Polychaeta. Five species are reported for the first time from the Algerian coast. This study contributes to the knowledge of non-native species on the Algerian coast and in the Southern Mediterranean and establishes a baseline dataset for future assessments of NIS in ports of Algeria.


Introduction
Marine biological invasions are considered one of the most important direct drivers of biodiversity loss and have a serious impact on ecosystem services (Katsanevakis et al., 2014). The Mediterranean Sea is one of the marine basins most affected by such invasions, fostered by the opening of the Suez Canal, intense maritime traffic, aquaculture, and the aquarium trade (Streftaris et al., 2006;Galil, 2009).
Maritime transport appears to be the main cause of transfer of NIS, through biofouling of ship hulls and ballast water (Gollasch, 2002;Bouda et al., 2018). In the West Mediterranean, shipping remains the most prominent route for these introductions (Zenetos et al., 2012). Therefore, ports and marinas constitute an important site for the introduction of species carried by international shipping (Ulman et al., 2017).
Docks and floating objects in ports provide solid surfaces characterized by continuous immersion at a constant, shallow depth, thus providing protection from the seabed's predators. Such surfaces support an abundant fouling biota and appear to favour NIS (Neves et al., 2007;Glasby et al., 2007). Therefore, ports are important sites for initiating biological monitoring (Awad et al., 2014).
In the Mediterranean, as in many parts of the world, many ports and marinas have been surveyed for the presence of NIS. However, such monitoring is rare in the southern Mediterranean compared to the north. Among these rare studies, we cite the monitoring of the marinas of El Kantaoui and Cap Monastir (Tunisia) and El Alamein (Egypt) (Sghaier et al., 2019).
In Algeria, only two studies have investigated the biodiversity in ports (Rebzani-Zahaf, 2003;Grimes, 2010), targeting the soft substrate macrozoobenthos. The port of Arzew is the most important port in Algeria. Bouda et al. (2016; conducted a theoretical risk assessment of species introduction by ballast water and biofouling on ship hulls (as an indicator of the importance of propagule pressure) and demonstrated that the port of Arzew is vulnerable to new introductions. However, there is a lack of data on the presence of non-native species in this port.
This study aimed to: (i) assess for the first time the presence of NIS in the port of Arzew, which is considered the most important port in Algeria; (ii) contribute to the knowledge of non-native species on the Algerian coast and in the Southern Mediterranean; and (iii) establish a baseline dataset for future assessments of NIS in Algerian ports.

Study area
The port of Arzew ( Fig. 1) is located east of Cape Carbon in Arzew Bay, at 350 km west of Algiers and 500 km east of the Strait of Gibraltar. It is principally used for the export of hydrocarbons, and to a lesser extent for trade and fisheries. This implies that most boats systematically unload their ballast water during the loading operation and thus large quantities of ballast water originating from other ports around the world are discharged at the port of Arzew (Bouda et al., 2016). Therefore, the risk of species introduction is very high. According to the report of the Regional Marine Pollution Emergency Response Centre for the Mediterranean Sea (REMPEC, 2008), the port of Arzew was classified as one of the Mediterranean ports most vulnerable to this type of risk. Biofouling constitutes an additional risk for the introduction of NIS (Bouda et al., 2018).

Sampling
Sampling was performed in two periods, early winter (December 2018) and spring (April 2019). Given that Arzew is mainly an oil and gas port and due to restrictions imposed by the port authorities, sampling focused only on floating structures (e.g. mooring buoys and tires used for berthing protection and ropes) and on the hull of a fishing vessel. Careful scraping was performed us-ing a blade, in a way that allowed for the identification of taxa and the estimation of abundance (low or high). All samples were carefully stored in collecting bags and were immediately fixed with formalin (4-5%). In the laboratory, samples were sieved through a 1 mm mesh. All animals were sorted and identified to the lowest possible taxonomic level. Photographs and videos of fouling communities were also taken. The taxonomic nomenclature of all identified species was verified according to the World Register of Marine Species (WoRMS Editorial Board, 2020).

Results and Discussion
A total of 10 NIS and cryptogenic species were identified in the port of Arzew (Table 1, Fig. 2), including: 1 Ascidiacea, 2 Bryozoa, 3 Crustacea, 1 Mollusca, 1 Porifera, and 2 Polychaeta. Five of these species are reported for the first time on the Algerian coast; 4 are considered as cryptogenic, 6 aliens (1 casual and 5 established).
Botryllus schlosseri (Pallas, 1766) According to Zenetos et al. (2017), the tunicate Botryllus schlosseri, which is distributed worldwide and shows marked polymorphism in chromatic patterns and colony shapes, is considered cryptogenic for the Mediterranean Sea. It has been shown that the taxon B. schlosseri is a complex of five genetically differentiated species (Lopez-Legentil et al., 2006;Bock et al., 2012) and all are present in the Mediterranean. Regarding the origin of this species, two theories should be noted. The first theory considers that the ascidian originated from the Mediterranean and spread around the world with shipping (Berril, 1950;Carver et al., 2006); the second theory is that B. schlosseri may have been introduced to Europe as early as the 1500s from the Pacific Ocean, the centre http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 10/01/2021 09:58:33 | of botryllid diversity (Carlton, 2005). Population genetics studies showed the possibility that the Mediterranean is a centre of diversity for B. schlosseri, and probably its site of origin (Lejeusne et al., 2011;Reem et al., 2017). In this study, B. schlosseri was abundant on almost all sampled structures and was also recorded in the port of Algiers (personal observation, BB).

Bugula neritina (Linnaeus, 1758)
The Bryozoan Bugula neritina is a common fouling organism worldwide, and reported from almost all seas. The cosmopolitan distribution of this species is probably due to shipping introductions. According to Coll et al. (2010) B. neritina has an Indo-Pacific origin and was spread by ships during the 19 th and 20 th centuries. However, data from a molecular study (Fehlauer-Ale et al., 2014) revealed that B. neritia is a complex of three cryptic species, but unfortunately Mediterranean populations were not considered in that study. Therefore, this species will be categorized as a cryptogenic species until more information is available (Zenetos et al., 2017). B. neritina is one of the dominant fouling organisms in many Mediterranean harbours (Ramadan et al., 2006;Spagnolo et al., 2019). B. neritia was not mentioned in the latest inventory of bryozoans from the Algerian coast (D'Hondt & Ben Ismail, 2008). This is the first report of this species in Algeria. This bryozoan was very abundant in the port of Arzew.
Bugulina stolonifera (Ryland, 1960) The erect bryozoan Bugula stolonifera is widely reported from ports around the world, including the Atlantic and Pacific Oceans and the Mediterranean (Ryland et al., 2011). It was first described by Ryland (1960) in samples taken from the port of Swansea (Great Britain) and from older specimens of a herbarium purchased by the British Museum; these samples dating back to before 1875 are labelled "British coast" but this label is not supported by the record. If this label is correct, the species would clearly not be a recent introduction in Great Britain. According to Ryland (1960), B. stolonifera was already present in the Mediterranean (Corsica), where it was confused with Bugulina spicata by Calvet (1902). However, the native range of B. stolonifera is unclear, especially because this species is easily confused with other species, such as B. californica (Cohen & Carlton, 1995), B. avicularia and B. plumosa (Ryland et al., 2011) and there are no molecular studies to suggest an evolutionary origin. Bugulina stolonifera has been reported from Algeria as B. avicularia (Gautier, 1955).

Elasmopus pectenicrus (Spence Bate, 1862)
The amphipod Elasmopus pectenicrus has a circumtropical distribution: Atlantic Ocean, Red Sea, Indian Ocean, Pacific Ocean (described from New Guinea) (Bellan-Santini et al., 1982). It has long been considered as a Red Sea immigrant, but recent taxonomic studies pointed out that E. pectenicrus is actually a group of cryptic species; consequently, it is considered cryptogenic (Marchini & Cardeccia, 2017). Elasmopus pectenicrus is found in different habitats such as infralittoral algal communities, shell bottoms and artificial habitats (Zakhama-Sraieb & Charfi-Cheikhrouha, 2010) and fine sandy beds (Bakalem & Dauvin, 1992). A very high abundance associated with hydroid communities on artificial habitats was found in this study. The first observation of this amphipod along the Algerian coast was made in 1989 by Bakalem & Dauvin (1992). Zeuxo coralensis Sieg, 1980 The tanaidacean Zeuxo coralensis has a circumtropical distribution (Masunari & Sieg, 1980). In the Mediterranean Sea it was discovered for the first time in the Bay of Algeciras (South Spain) between 1992 and 1993 on both artificial and natural substrates (Sánchez-Moyano & García-Gómez, 1998) and in the Levantine Seas (Zenetos et al., 2010). In this study Z. coralensis was observed on a ship hull and on a tire.
Paracerceis sculpta (Holmes, 1904) Native to the north-east Pacific, Pracerceis sculpta has been recorded in several places, including Hong Kong, Brazil and Australia (Munguia & Shuster, 2013). Its first record in the Mediterranean Sea dates back to 1978 from Tunis (Rezig, 1978). Henceforth, this isopod seems to be present throughout the Mediterranean basin (Zenetos et al., 2010). During our sampling, P. sculpta was present on a tire and on the hull of a fishing vessel. This represents the first report of this species in Algeria. (Barnard, 1927) The nudibrach was first described from the south African coast in 1927 where it is considered common in shallow waters along the whole east coast of South Africa (Betti et al., 2015). It was always found in Zostera meadows or under stones in intertidal areas. Edmunds (1977) reported Godiva quadricolor for the first time in the Atlantic Ocean (Ghana) on a boat hull. Also, G. quadricolor was reported from Australia (Willan, 1987). The first record of this species in the Mediterranean dates to 1985 in the Gulf of Naples, where it was confused with Facelina coronata (Betti et al., 2015). Cervera et al. (2010) reported this species in the Bay of Algeciras (Strait of Gibraltar), Betti et al. (2015) observed it from the Ligurian Sea and Gerovasileiou et al. (2017) from France. In this study, one specimen was found on a rope. Nevertheless, this individual was damaged and quickly began to lose its cerates, but was identified by its numerous blue, yellow and orange striped cerates. It is undoubtedly non-native to the Mediterranean, where it was introduced by maritime transport. Hydroides dirampha Mörch, 1863 Hydroides dirampha was found twice in the study area, on a tire and on the hull of a boat. It seems that this species originated from the American coast of the tropical Atlantic (Gulf of Mexico, Caribbean, West Indies, Brazil) where it is abundant and not limited to port environments (Zibrowius, 1973). it was recorded for the first time in the Mediterranean Sea at the port of Naples in 1870. Nowadays it is common in the whole Mediterranean basin. H. dirampha was reported for the first time in Algeria in 1983 at the port of Algiers as H. lunulifera (Rebzani-Zahaf, 2003). Later, Grimes (2010) reported it under the same name without location details.

Godiva quadricolor
Hydroides elegans (Haswell, 1883) Hydroides elegans is a circumtropical species, extending into the warm-temperate zone, and is considered to be an alien species for the Mediterranean Sea, introduced on ship hulls (Zibrowius, 1991). This species was very abundant in the study area, found in dense aggregations on almost all submerged artificial surfaces. High levels of abundance have also been reported from several Mediterranean ports (Zibrowius, 1991;Spagnolo et al., 2019). A comparison of studies on biofouling communities between the years 1960 and 1999 in the Eastern harbour of Alexandria (Ramadan et al., 2006) revealed that the serpulid H. elegans was the most dominant species in all studies. The species has previously been reported from Algeria as Hydroides norvegicus by Rebzani-Zahaf (2003), who collected it in 1983 at the port of Algiers. Klautau, Monteiro & Borojevic, 2004 The calcareous sponge Paraleucilla magna was first described from Rio de Janeiro, Brazil (Klautau et al., 2004). In the Mediterranean Sea, this species was first identified at four different localities in Italy (Taranto, Porto Cesareo, Brindisi and Naples), and in Spain, Malta, Croatia, Montenegro, Turkey, Cyprus and Greece (for details see Gerovasileiou et al., 2017). Moreover P. magna was discovered on the southern shore of the Mediterranean Sea, in Algeria (port of Algiers and Pisan Island of Bejaia) in 2018 (Bachetarzi et al., 2019) and Tunisia (marina of Cap Monastir (Sghaier et al., 2019); port of Bizerte, personal observation). Despite the unknown origin of P. magna in the Mediterranean Sea this calcareous sponge is considered a NIS (Zammit et al., 2009). Bivalve aquaculture and shipping are the most probable vectors responsible for its spread. In this study P. magna was abundant in the port of Arzew on almost all artificial substrates. Pierri et al. (2010) reported that P. magna plays a structural role within the studied fouling community in the Mar Piccolo of Taranto (Italy).

Paraleucilla magna
Among the species found during this study, it is useful to note the presence of Hydroides dianthus, which has long been considered as alien to the Mediterranean and originated from the Atlantic coast of North America. According to a recent molecular study (Sun et al., 2017), the global invader H. dianthus seems to have originated from the Mediterranean Sea. It has however been removed from the Mediterranean aliens list of established species (Zenetos et al., 2017).
The number of non-native or cryptogenic species found in this preliminary study greatly underestimates the actual number of non-native species that may be present in the port of Arzew because: (i) it was not possible to identify all taxa due to the lack of taxonomic expertise (e.g. Sipincula, Cirripedia, Polychaeta: Errantia, etc.); (ii) sampling was restricted in terms of area, depth and substrate type; and (iii) the sampled surface was below the minimal sampling area, as suggested by other surveys in Mediterranean port communities (Hewitt & Martin, 2001;Spagnolo et al., 2019).
Indeed, if we compare the number of NIS found during this study (6 species) with the number of non-native species found in 5 Italian ports (Western Mediterranean), the number was clearly lower, as Ferrarion et al.
(2017) recorded 12 NIS in the port of Genoa, 8 in the port of La Spezia, 11 in the port of Leghorn, 12 in the port of Olbia and 14 in the port of Porto Torres. Three species were found in all of these ports and the port Arzew: H. dirapmha, H. elegans and P. sculpta.
In the most recent inventory of introduced marine species of Algeria, Grimes et al. (2018) listed 39 NIS and 11 cryptogenic species. Although there have been some new reports of NIS from the Algerian coast since this work (e.g. Callinectes sapidus (Benabdi et al., 2019), Paraleucilla magna (Bachetarzi et al., 2019)), it is probable that the number of NIS in Algeria remains largely underestimated, due to the lack of taxonomists and biomonitoring programmes. Data from this monitoring of ports will provide vital information on the distribution of NIS in Algeria and on the southern Mediterranean coast. This information will serve as a baseline for future monitoring inside and outside Algerian ports.