A lionfish (Pterois miles) invasion has begun in the Mediterranean Sea

Until now, few sightings of the alien lionfish Pterois miles have been reported in the Mediterranean and it was questionable whether the species could invade this region like it has in the western Atlantic. Here, we present evidence from divers and fishermen that lionfish have recently increased in abundance and within a year colonised almost the entire south eastern coast of Cyprus, likely due to sea surface warming. At least 23 different fish are reported of which 6 were removed. Groups of lionfish exhibiting mating behaviour have been noted for the first time in the Mediterranean. Managers need this information and should alert stakeholders to the potential ecological and socio-economic impacts that may arise from a lionfish invasion. Actions could involve incentives to engage divers and fishermen in lionfish removal programmes, as these have worked well at shallow depths in the Caribbean. Given that the Suez Canal has recently been widened and deepened, measures will need to be put in place to help prevent further invasion.


Introduction
The Mediterranean Sea represents around 0.82 % area and 0.3 % volume of the world ocean but it contains 4-18 % of described marine organisms and is a biodiversity hotspot with estimated 17,000 species (Coll et al. 2010).Mediterranean ecosystems face multiple anthropogenic threats such as climate change, over fishing and alien invasions (Kletou & Hall-Spencer 2012).Mediterranean seawater temperatures are steadily increasing, and alien species are spreading, causing community shifts and tropicalization (Lejeusne et al. 2010;Montefalcone et al. 2015).There are now >1000 alien species in the Mediterranean and the majority are thermophilic species that have entered the eastern basin through the Suez Canal (Katsanevakis et al. 2014).Recent enlargement of this canal coupled with sea surface warming is raising concerns that this problem will get worse (Galil et al. 2015).
Lessepsian fish invasion rates are now increasing rapidly; ca 40 % of the 130 alien fish species now living in the Mediterranean have been reported since 2001 and these have expanded their geographical range during this time (Zenetos et al. 2012).The bluespotted cornetfish Fistularia commersonii colonised almost the entire Mediterranean in just 7 years (Azzurro et al. 2012) where it now poses a threat to local ecosystems since it feeds on a large variety of prey (41 taxa) and specialises on juveniles of the commercial fish Boops boops and Spicara smaris (Bariche et al. 2009).The pufferfish Lagocephalus sceleratus has now reached the central Mediterranean (Azzurro et al. 2014) and is expanding west (Souissi et al. 2014).It eats economically important cephalopods Sepia officinalis and Octopus vulgaris (Cuvier 1797) and is classed as a fisheries pest (Kalogirou 2013).Some countries have initiated invasive fish eradication programmes, for example the Cypriot authorities have been compensating fishermen for their pufferfish catches during the reproductive season, resulting in massive removals of pufferfish biomass from the eastern Mediterranean (Rousou et al. 2014).
Few worldwide fish invasions of similar magnitude are documented; the introduction of the red lionfish Pterois volitans and the devil firefish P. miles in the western Atlantic is one of the fastest and most ecologically harmful marine fish introductions to date (Albins & Hixon 2013).In their native range, P. miles occur in the Indian Ocean from South Africa to the Red Sea and Persian Gulf, and east to Sumatra while P. volitans are observed in both the western and central Pacific and western Australia.Pterois volitans looks similar to P. miles but has an additional dorsal fin ray and an extra anal fin ray (Schultz 1986).A decade after either intentional or accidental aquarium release in Florida, P. volitans became fully established throughout the southeast United States and the Caribbean Sea, extending to South America and much of the Gulf of Mexico (Schofield et al. 2015).The alien lionfish population has low genetic diversity and is thought to originate from a small founder population in the southeast United States (Betancur-R et al. 2011).The lionfish are generalist carnivores and can feed on a large variety of fish and crustaceans although large individuals prey almost exclusively on fish (Côté et al. 2013b).Lionfish spawn every 4 days year-round, producing around two million buoyant gelatinous eggs per year (Morris et al. 2009).Their eggs are planktonic and can ride the ocean currents and cover large distances for about a month before they settle (Ahrenholz & Morris 2010).In western Atlantic, lionfish are more abundant than in their native region and have become the dominant predator on coral reefs with a great impact on native reef fishes, decreasing the abundance of >40 prey species by 65 % on average, in just 2 years (Green et al. 2012).Their dramatic invasive success results from a combination of factors such as early maturation and reproduction, anti-predatory venomous defences and ecological versatility of the lionfish coupled with naïve prey and the overfishing of native predators (Côté et al. 2013a).
In the Mediterranean Sea, one P. miles was recorded in 1991 off Israel (Golani & Sonin 1992).After two decades of silence, two specimens were captured off the coast of Lebanon in 2012 (Bariche et al. 2013).Soon after, two more were reported in a newspaper article, captured off Cyprus and in 2014, another specimen was sighted in Turkey, then in 2015 two more were captured in Cyprus and then sighted in Rhodes in Greece (Turan et al. 2014;Oray et al. 2015;Crocetta et al. 2015;Iglésias & Frotté 2015).Recently, several records were reported from south Turkey indicating a westerly migration of the species towards the Aegean Sea (Turan & Öztürk 2015).Hitherto, lionfish were reported only occasionally in the eastern Mediterranean Sea and their successful invasion in the Mediterranean Sea is questionable due to unfavourable oceanographic conditions that limit the wide dispersion of lionfish larvae (Johnston & Purkis 2014).
In this article, we present evidence that the threat of lionfish invasion in the eastern Mediterranean Sea is real and is probably underway.Sightings of the lionfish P. miles from the coastal waters of south Cyprus are becoming more frequent in contrast to recent model predictions (Poursanidis 2015).Furthermore, groups of lionfish have been sighted together for the first time in the Mediterranean.

Materials and methods
In 2015 reports of lionfish sightings on electronic social media/networks and within the local community of divers and fishermen became more frequent.To map lionfish distribution around Cyprus, we collated information from local divers and spearfishermen who reported lionfish encounters in the coastal waters.In-person and telephone interviews were conducted.Interviewees with proof of lionfish sightings willingly provided the evidence (photographs and/or videos) for the purposes of this study.Date of sighting, locality (area and depth) and other information were recorded for validated lionfish sightings.In addition, governmental officers of the Department of Fisheries and Marine Research (DFMR) of the Ministry of Agriculture, Rural Development and Environment shared information and specimens captured in trammel nets by local coastal fishermen.

Results
The lionfish P. miles has spread rapidly and colonised almost the entire south eastern coast of Cyprus, from Limassol (south) to Protaras (south east) in just 1 year (Fig. 1).Divers and government officers that were questioned in this study mentioned >10 additional lionfish sightings and captures that were unfortunately not photographed so are not included in our database.
Officers from DFMR provided four specimens for the purposes of this study.One is now alive in an aquarium at DFMR offices and another is among the first two undocumented reports made from Cyprus back in February 2013 (Bariche et al. 2013).More details about these specimens are presented in Fig. 2. Most validated reports of lionfish come from scuba divers and freedivers across south Cyprus.Here we list 24 new sightings of at least 19 different fish (Fig. 3, Table 1).
Three pairs of lionfish have been photographed, one at Zenobia wreck at 20 m depth, another near Cape Kiti at 42-43 m (Photo D, Fig. 3) and one more at Cyclops caves near Cape Greco at 12-15 m depth.The Cyclops pair has been photographed many times by different recreational scuba divers both as singletons or together (Photos C, I, J, O, Q, W and X, Fig. 3).The distinctive stripe pattern of these two individuals allows their identification through photos and the tracking of their movement.They were documented together at the same rock formation for a period of 2 months between July and September 2015 (Photos O, Q, W and X, Fig. 3).It is noteworthy that one individual from the pair named β with a unique stripe pattern on its left side, may have been reported on the other side of Cape Greco, around 10 km from Cyclops caves, several months earlier in October 2014 (Photo C, Fig. 3).The other individual, named α, has very distinctive stripes on its right side and was first sighted at Cyclops caves on 7 of July 2015 and the next day it was reported towards Green bay, about 2 km to the north east (Photos I and J, Fig. 3).Two weeks later it was found back at Cyclops caves with β where they remained together for at least 2 months.About a week before the pairing was sighted at Cyclops caves, a third lionfish was reported at the site but it was not sighted again thereafter (Photo L, Fig. 3).Recently, a different lionfish has joined the pair (Photo X, Fig. 3).

Discussion
The possibility of a lionfish invasion in the Mediterranean Sea and the potential ecological and socio-economic impacts that may follow have been largely neglected by the regional scientific community, managers and other stakeholders.Few validated reports of lionfish sightings exist from the region, which creates muted concern and uncertainty about the ability of the species to colonise the Mediterranean.Furthermore, model simulations have suggested that this would be unlikely to happen (Johnston & Purkis 2014) although the warming and acidification of Mediterranean waters due to CO 2 emissions may require The lionfish first appeared in the eastern Mediterranean at about the same time that they were first reported off Florida.There they spread rapidly and colonised almost all warm parts of the east coast of United States, the Gulf of Mexico and the entire Caribbean Sea (Schofield et al. 2015) whereas more than two decades passed for a second sighting to occur in the Mediterranean Sea.
Here, we present >20 lionfish sightings (mostly by divers) from the coastal waters of south Cyprus during over the past year, providing evidence that the lionfish invasion in the Mediterranean Sea is becoming a clear threat that Fig. 3 Photographs of lionfish from the south coast of Cyprus captured by recreational scuba divers, free-divers or spear-fishermen.Further details on Table 1 requires the immediate attention of officials and the engagement of stakeholders.It appears that the lionfish have found their niche, formed reproductive populations and are now established.Lionfish are normally solitary animals and only gather in groups to mate (Fishelson 1975).While some lionfish stay put, like one that remained on the Zenobia wreck for at least 6 weeks, some travel up to 2 km a day (α from the Cyclops pair).In the western Atlantic, lionfish have been found in a wide variety of habitats including hard bottom and patchy reefs, seagrass beds and wrecks (Claydon et al. 2012).The lionfish reported in this study were found at depths ranging from 3 to 43 m and the majority were found on vertical rock walls or at the entrance of small caves.Three were found on breakwater defences, three were on wrecks and one was spearfished near an oil pipeline.So far, no lionfish have been spotted in seagrass Posidonia oceanica (Linnaeus) Delile 1813 meadows.Genetic research is needed to assess dispersion pathways of the lionfish and to find out whether they have come from Lessepsian migration and/or through aquarium release.
Lionfish have very few documented natural predators due to their venomous spines.Native groupers in the western Atlantic have learned to eat this non-indigenous species (Maljković et al. 2008) and in at least three cases reported herein groupers have been seen close to lionfish.It remains to be seen whether native groupers such as Epinephelus marginatus will learn to prey on lionfish and control their invasion.Restrictions on fishing seem sensible to help threatened IUCN Red List species such as the Mediterranean dusky grouper, as these may in turn help control the spread of invasive fish (Mumby et al. 2011).
Judging from the recent increase in P. miles in the eastern Mediterranean Sea, its few natural predators, the dispersal capabilities of their planktonic larvae and its ability to adapt to a range of habitats, we suspect that a rapid expansion throughout the Mediterranean Sea may soon follow with significant impacts on local ecosystems and fisheries.Furthermore, CO 2 emissions which are warming the Mediterranean Sea and the construction of a deeper and wider Suez Canal are expected to increase invasion rates (Galil et al. 2015;Hall-Spencer & Allen 2015).
Lionfish are slow moving and easy to collect by divers and we know, from the western Atlantic experience, that early detection and a rapid response is the first line of defence to mitigate impacts of the lionfish invasion (Morris et al. 2009).Targeted removal by divers has reduced lionfish abundance at shallow depths in the western Atlantic (Frazer et al. 2012;Albins & Hixon 2013).Mediterranean stakeholders (especially divers and fishermen) should be engaged with education and outreach, training and the provision of incentives for removal efforts.The fact that only about a tenth of the lionfish reported by divers in this study were removed from the ecosystem is testimony to the lack of knowledge about the potential impacts of a lionfish invasion.We believe that many will be motivated to aid removal efforts.When the venomous dorsal, pelvic fin and anal fin spines are removed, the lionfish is safe to consume and this can be promoted.Removal programs should be combined with efforts to restore populations of potential predators of lionfish, such as the dusky grouper.

Fig. 2
Fig. 2 Photographs of lionfish from the south Cyprus captured by professional fishermen using trammel nets.a was captured in Amathounta, Limassol in February 2013 and it is one of the first two lionfish that were reported in Cyprus (Bariche et al. 2013); b was captured at Cape Gata, Akrotiri, Limassol in January 2015 at the depth of 15 m; c is a living specimen captured at Cape Kiti, Larnaca in May 2015 at the depth of 40 m; d was captured at Ayios Theodoros near Zygi in July 2015 at the depth of 15 m

Table 1
Lionfish sightings details from divers who took the photographs in Fig.3.Coordinates are best available estimates