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Research Article IJAAER(2020); 6(2): 125-133

ON THE PRESENCE OF THE NON-NATIVE OVATA BRUGUIÈRE, 1789 AND THE SPREAD OFF THE INVASIVE LEIDYI A. AGASSIZ, 1865 IN THE LEBANESE WATERS, EASTERN MEDITERRANEAN SEA

Ali Badreddine*, Ghazi Bitar*, Anthony Ouba**, Tamara Shiganova***

*Department of Marine Biology, Faculty of Sciences, Lebanese University, Hadath, Beirut, LEBANON **Faculty of Sciences, American University of Technology-AUT, Fidar - Halat, Byblos, LEBANON ***Shirshov Institute of Oceanology, Russian Academy of Sciences, 36 Nahimovskiy Prospekt, Moscow, RUSSIA, 117997

*Corresponding author: [email protected]

Abstract The two non-native ctenophores Bruguière, 1789 and Mnemiopsis leidyi A. Agassiz, 1865, were reported off the Lebanese waters. Beroe ovata Bruguière, 1789, a specialized predator on Mnemiopsis leidyi, was collected and photographed, on May 2th 2019 during fieldwork in Beirut waters. While, Mnemiopsis leidyi was reported for the first time on April 27th 2009, to date, it is widely distributed from the south to the north of the Lebanese waters. The most possible pathway of the introduction of those is a spreading, or bringing with ballast waters from the Black Sea.

Keywords - Beroe ovata, Mnemiopsis leidyi, non-native species, Lebanese waters, eastern Mediterranean Sea.

INTRODUCTION M. leidyi (Shiganova and Malej, 2009). Beroe ovata Bruguière, 1789, known Accordingly, M. leidyi, with a higher as the American brown comb jelly, and its capacity of invasion, was first found, in prey Mnemiopsis leidyi A. Agassiz, 1865, 2005 (Shiganova and Malej, 2009), in the known as the American comb jelly, are Mediterranean Gulf of Trieste (northern native to the Atlantic coast of the Americas Adriatic Sea), and near Marseille in the (Shiganova and Malej, 2009). As it was Berre Lagoon. Successively, M. leidyi identified by genetic analyses both have spread to different locations of the northern, been introduced by ballast waters first in the western and eastern Mediterranean basin Black Sea from the vicinity of the Gulf of (Shiganova et al., 2019a; Dragičević et al., Mexico or Caribbean areas (Ghabooli et al., 2019; Malej et al., 2017; CIESM, 2015; 2010; Bayha et al., 2004) and expanded into Galil, 2012; Costello et al., 2012; Turan et the Azov, Caspian, Baltic and North seas al., 2010; Galil et al., 2009; Boero et al., (Shiganova et al., 2018; Shiganova et al., 2009; Shiganova et al., 2001a, b). 2014a; Shiganova and Malej, 2009; In the Southern Levantine Sea, M. Mirzoyan et al., 2006; Kideys et al., 2004; leidyi was reported for the first time in 2009 Shiganova et al., 2001c). (Galil et al., 2009), B. ovata went after its In the Mediterranean Sea, the prey in 2011 (Galil et al., 2011; K Ali et al., American Beroe ovata was first reported in 2015). Recently, B. ovata is well reported in November 2004, in the northern Evoikos this area of the Mediterranean (Galil, 2012; Gulf, Greece (Shiganova et al., 2007; Galil et al., 2011). While, its prey the Kawsar Ali et al., 2015) and a year later, in invader M. leidyi has already been well the Bay of Piran, northern Adriatic Sea, established in this region (Turan et al., 2010; where B. ovata has been found with its prey,

125 Galil et al., 2009; Shiganova, 1997; K Ali et Beroe ovata has wide miter-shaped al., 2012). flattened body with remarkable lateral So, the goal of our note is, first to compression. Its body is not less than three report the presence of the brown comb jelly, times compressed in paragastral plane. The B. ovata in the Lebanese waters and its well- aboral end of body is rounded, while the oral established prey, the invasive comb jelly, M. end is almost straight and wider than the leidyi in this region. body width, which is characteristic only for B. ovata. The meridional canals lay under 8 MATERIALS AND METHODS rows of ciliary combs, which extend about One specimen of B. ovata was three-quarters of the distance from the apical collected and photographed on May 2th sense organ towards the mouth. Side 2019, during a field work offshore Beirut branches (devirticulae) may be placed in waters (33°52’42.67”N, 35°.28’11.15”E, connection one with another by means of an Figure 1). Concerning M. leidyi, it was anastomosing network of them in the body firstly observed by one of the authors (Ghazi (Figure 2A, B) (Shiganova et al., 2001c). Bitar), on April 27th 2009, also in Beirut Mnemiopsis leidyi is characterized waters (33°54’11.25”N, 35°28’57.64”E). by the presence of two lateral lobes Subsequently, the full list of M. leidyi originated near the level of aboral organ, and sightings along the entire Lebanese coast is four smaller auricles under the two oral presented in Table 1 (see also Figure 1). lobes, which is characteristic only for M. Additional supporting information leidyi in comparison with other species regarding the sightings, including the belonging to the order Lobata (Figure 3A, location, date, proofs based on B). photos/personal communications with It is worth noting that the way of experts and divers, and references (when introduction of B. ovata in the Lebanese available), are provided in Table 1. waters, like its prey M. leidyi, is more RESULTS AND DISCUSSION related with ballast waters. From a morphological point of view, Concerning the current status of the B. ovata and its prey M. leidyi (Figure 2A, invader M. leidyi, the results of observations B; 3A, B) in the Lebanese waters is similar indicate a significant increase in the to the specimen described in the Southern abundance of this comb jelly along the Levantine Sea (Galil et al., 2011; Turan et Lebanese coast since its first record in 2009 al., 2010; Galil et al., 2009) and in the Black until today, when the species spread along Sea (Shiganova et al., 2001; Zahid Hussain the entire Lebanese coast from the south to et al., 2013). the north (Table 1, Figure 1).

Table 1. Records of Mnemiopsis leidyi along the Lebanese coasts from 2009 until 2020

Location Date Photo References/ or proofs/ or comments

Nakoura 23-03-2011 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 28-08-2013 Yes RAC/SPA-UNEP/MAP, 2014.

El-Baiada 16-09-2015 Yes Result confirmed by one of the authors (Ghazi (Nakoura) Bitar) during a field work. 20-09-2015 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 22-09-2015 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 19-09-2009 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 17-10-2009 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. Tyre 30-05-2010 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work.

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Continuation of Table:1 06-04-2011 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. Many records Yes Personal observations by one of the authors in 2019 (Anthony Ouba) during a field work. Saida 12-08-2020 Yes Result confirmed by professional diver Captain Mohammad-El Serge during a field work. Saadiyet 02-04-2010 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. Khalde 18-04-2010 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 27-04-2009 Yes First record of M. leidyi confirmed by one of the authors (Ghazi Bitar) during a field work. 03-07-2009 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 15-09-2009 Yes Result confirmed by one of the authors (Ghazi Beirut Bitar) during a field work. 07-07-2010 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 29-03-2011 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. Many records Yes Personal observations by one of the authors in 2019 (Anthony Ouba) during a field work. 22-04-2013 No Katsanevakis et al., 2020 Jounieh 05-03-2016 No Katsanevakis et al., 2020

Byblos 03-10-2016 Yes SPA/RAC-UN Environnent/MAP, 2017.

Kfar Abida 17-04-2010 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. Batroun 26-09-2010 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 18-06-2011 Yes Result confirmed by one of the authors (Ghazi Ras Chekaa Bitar) during a field work. 24-06-2012 Yes RAC/SPA-UNEP/MAP, 2014.

El Heri 27-08-2015 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 25-04-2010 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 22-06-2011 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. Enfeh 02-08-2012 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 23-06-2013 Yes RAC/SPA-UNEP/MAP, 2014.

13-08-2014 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 18-03-2015 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. 31-08-2015 Yes Result confirmed by one of the authors (Ghazi Bitar) during a field work. Palm Island 30-05-2019 Yes Result confirmed by a diver Hilal Sfarjalani.

Ramkine 29-05-2011 Yes Result confirmed by one of the authors (Ghazi Island Bitar) during a field work.

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The present record of B. ovata and by the high by M. leidyi was the spread off its prey, M. leidyi in the observed in the Levantine Sea (Galil, 2012; Lebanese waters confirms the fact that the Kawsar Ali et al., 2015). two non-native ctenophores are tolerant of a From another point of view, the wide range of salinity and temperature presence of B. ovata in the Lebanese waters, (Shiganova et al., 2019a, 2019b, 2018; may be probably capable of controlling the Galil, 2012; Mirzoyan et al., 2006; populations of M. leidyi. As proved, it has Shiganova et al., 2001c). As Shiganova et al. been confirmed a decrease on the population (2019b) predicted, they are now recorded in of M. leidyi in presence of its important the warmest (South Levantine Sea) areas of predator B. ovata in the Black Sea the basin. (Shiganova et al., 2018, 2014a, 2001) and The importance of our note proofed outside of it, in the Sea of Marmara again by the fact that M. leidyi is one of the (Isinibilir et al., 2004). As well as, in the most harmful invasive species, which is a Southern Levantine Sea, the native comb simultaneous hermaphrodite and capable for jelly sensu Mayer, 1912, was self-fertilization. In addition, it has high recently observed and photographed feeding and growth rates potential preying on the invasive American comb (Shiganova et al., 2019a, 2019b). Moreover, jelly M. leidyi (Galil and Gevili, 2013; M. leidyi is also known for its high rate of Kawsar Ali et al., 2011). zooplankton consumption, including eggs In this context, it is really and larvae of fish and invertebrates important to follow up the current status of (Shiganova et al., 2019a, b). As a the non-native ctenophore M. leidyi in the consequence, the high abundance of M. Lebanese waters, to reduce the risk of their leidyi may promptly reduce the local impacts as competitor on local commercial zooplankton stocks and affects indirectly species stocks and total ecosystem state. their consumers planktophagous fish With the aim to encourage monitoring of (through the trophic cascade), as it was these gelatinous invaders B. ovata and M. demonstrated in all the seas invaded by this leidyi and other harmful gelatinous species, species such as the Black, Baltic, Caspian we launch an awareness campaign on and even the Mediterranean (Shiganova et jellyfish along the Lebanese coast (Fig. 4) al., 2019a, b; Hashemi et al., 2019; Malej et that will help to detect new species of jellies al., 2017; Shiganova et al., 2014b; Roohi et and evaluate the current status of those that al., 2010; Galil, 2009; Boero et al., 2009; already present, especially the non-native Haslob et al., 2007; Shiganova et al., 2001a, ones, as B. ovata and M. leidyi that are not 2001b; Shiganova, 1997; Öztürk and easily recorded during monitoring by Öztürk, 1996; Tabassum Yaseen et al., traditional methods. 2016). As a result, in the Southern Levantine Sea, the spreading of this invasive AKNOWLEDGMENT ctenophore caused the decrease of the fish T.A. Shiganova performed the study within stocks, damage the fishing gears of the the framework of State assignment of the fishermen and disrupt some coastal Ministry of Education and Science of the installations (Galil, 2012; Turan et al., 2010; Russian Federation - theme #0149-2019- Galil, 2009; Fazal Munsif et al., 2015). Also, 0010. a decrease of the zooplankton stock caused

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Figure 1. Map of the Lebanese coast showing the location where Beroe ovata where collected and photographed and all the locations of Mnemiopsis leidyi records.

Figure 2. Specimen of Beroe ovata photographed in the Lebanese waters. 2A. Photo showed the rounded aboral end and the widened oral end of Beroe ovata; 2B. Photo showed the meridional canal with the typical anastomoses of Beroe ovata (Photo: Ali Badreddine).

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Figure 3. Mnemiopsis leidyi in the Lebanese waters. 3A. M. leidyi in the Palm-Island waters; 3B. Aggregations of M. leidyi with the indigenous jellyfish Rhizostoma pulmo in the Palm- Island waters (Photos: Hilal Sfarjalani).

Figure 4. Poster with the discovered jellies in the Lebanese waters published at ©Facebook and presented to the society in many sites of the Lebanese coast.

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