Lionfish Invasion and Its Management in the Mediterranean Sea

LIONFISH INVASION AND ITS MANAGEMENT IN THE MEDITERRANEAN SEA

Edited by M. Fatih HÜSEYİNOĞLU and Bayram ÖZTÜRK

LIONFISH INVASION AND ITS MANAGEMENT IN THE MEDITERRANEAN SEA

All rigths are reserved. No part of the publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means without the prior permission from the Turkish Marine Research Foundation (TUDAV). © Turkish Marine Research Foundation ISBN: 978-975-8825-41-7 Citation: Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication number: 49, Istanbul, Turkey, 121 pages.

Cover photo: Pterois miles © Bayram Öztürk (TUDAV) Available from: Turkish Marine Research Foundation (TUDAV) P.O. Box: 10, Beykoz, Istanbul, Turkey Tel: 0(216) 424 07 72 Fax: 0(216) 424 07 71 E-mail: tudav@tudav.org www.tudav.org Printed: MetinCopyPlus / Artı Dijital & Baskı Merkezi Türkocağı Cad. 3/A Türkiye Gazeteciler Cemiyeti Altı İran Konsolosluğu Karşısı Cağaloğlu/Fatih/İstanbul Tel: 0212 527 61 81 E-mail: info@metincopyplus.com www.metincopyplus.com

ii

Contents PREFACE………………………………………………………………….…...iv Controlling the lionfish invasion in the eastern Mediterranean Sea Murat Bilecenoğlu…………………………………………………………….....1 The invasion and establishment of lionfish species (Pterois spp.) as a major threat to marine biodiversity of Turkey Cemal Turan........................................................................................................10 The current status of lionfish invasion in Greece and future steps towards control and mitigation Ioannis Giovos, Ioannis Batjakas, Nikolaos Doumpas, Thodoros Eystratios Kampouris, Dimitris Poursanidis, Vangelis Paravas……………………...……17 What is the roar about? Lionfish targeted removals in Costa Rica (Central America) and Cyprus (Mediterranean Sea) Carlos Jiménez, Burak Ali Çiçek, José Ugalde Jiménez, Louis Hadjioannou, Mehmet Fatih Huseyinoglu………………………………………………..…...34 Iron Lion Zion: the successful, albeit lingered, invasion of the lionfish in the Israeli Mediterranean Sea Nir Stern, Shevy B.S. Rothman……………………………………………..….51 The need for international environmental regulations on artificial waterways: The Suez Canal case Senem Atvur, Ceren Uysal Oğuz…………………………………………..…...57 Lionfish envenomation: epidemiology, management and prevention Selin Gamze Sümen, Bengüsu Mirasoğlu, Şamil Aktaş………………………...70 Marine aquariums and lionfish trade in Turkey Zeynep Gülenç……………………………………………………………..…..88 Lionfish and scuba diving Murat Draman……………………………………………………………..….100 Lionfish preparation for cooking in Turkey Tolga Manacıoğlu, Simge Manacıoğlu …………………………….…............110

iii

PREFACE Lionfish is a common name for several species from the teleost fish family of Scorpaenidae. It is a very attractive fish with wing-like patterns of beautiful fin structures; it is very hardy and tolerant to various water parameters and environmental conditions; and it is marvelously colorful, therefore it is one of the most popular aquarium fish among the hobbyists of the world. However, these mentioned properties have as well make this fish a very dangerous one: (i) Color and pattern scheme is a warning that it is highly venomous, to an extent that it can kill a human with a weak immune system; (ii) Its hardiness and tolerance make it a very persistent species which can withstand various and even/ever changing conditions in different ecosystem types, announcing it as a real survivor; (iii) Having a high reproduction and feeding rate, it can sweep ecosystems easily without the presence of a frequent natural predator or a successful scavenger which feeds on its eggs, larvae or juveniles.

A single specimen of a Mediterranean Pterois miles was recorded in 1992 almost synchronously with a few individuals P. volitans in Florida, USA, however past two decades showed no other repeated occurrences while West Atlantic is almost completely invaded with dire consequences.

Starting from 2012, lionfish sightings increased with the anticlockwise order of main Eastern Mediterranean currents. With a bitter example in the hand, scientists have a common concern regarding this fish to be a problem child for the rest of the Mediterranean, so a load of science and public awareness campaigns are directed in the Levantine countries.

This is the first book trying to cover the various aspects of the invasion of the lionfish P. miles in the Mediterranean Sea as well as suggestions for its population control – including recipes since it found its way to restaurant tables already.

Different approaches of the papers in this book show that the problem has many faces: genetic, ecological, social, comparative biological, touristic and even gastronomic.

Finally, we thank all authors who contributed to this book with their effort, namely their time and extent knowledge, as well as their continuous passion for the protection of the Mediterranean biodiversity.

M. Fatih HÜSEYİNOĞLU Bayram ÖZTÜRK December, 2018

iv

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

Controlling the lionfish invasion in the eastern Mediterranean Sea Murat BILECENOĞLU Department of Biology, Faculty of Arts & Sciences, Aydın Adnan Menderes University, 09010 Aydın, TURKEY Corresponding author: mbilecenoglu@adu.edu.tr

Introduction The number of alien species becoming major invasive threat has been increasing in the Mediterranean Sea remarkably. A potentially detrimental Indo-Pacific species, Pterois miles, have recently been introduced to the Levantine basin, which may unfavorably affect not only the structure and function of local ecosystems, but also the socio-economy, fisheries, biodiversity and even human health. What we have learned so far from this undesired introduction is as follows: 1) the single P.miles individual recorded off the Israeli coast during 1991 (Golani and Sonin 1992) is an indication of an unsuccessful invasion attempt, since no further occurrence records were given within the next two decades, 2) the current lionfish invasion in the eastern Mediterranean Sea is probably a recent event (Bariche et al. 2013), 3) the current lionfish populations in the Mediterranean are a product of multiple invasion events via the Suez Canal (Stern et al. 2018), 4) its range expansion speed is remarkably high; the species crossed the eastern basin just within two years, reaching to Italy and Tunisia (Azzurro et al. 2017), 5) several Mediterranean countries could not effectively respond to the accelerating lionfish invasion (Bilecenoğlu 2017). It is worth to mention that some scientists are doubtful about an invasion comparable to the Atlantic, since computer modeling predicts low connectivity between potential lionfish habitat along the Mediterranean coastline, so the basin is not claimed to be particularly conducive to the establishment of lionfish (Johnston and Purkis 2014). However, current observations available in various parts of the Mediterranean Sea indicate an increasing abundance of P.miles, whose establishment success may be attributed to the combination of its life history characteristics including the rapid growth (Johnson and Swenarton 2016), high fecundity and capability of spawning throughout the year (Gardner et al. 2015), opportunistic and voracious feeding habits (Eddy et al. 2016) and tolerance to a wide range of environmental conditions (Whitfield et al. 2007). Moreover, natural biological controls (i.e. predators, diseases) are quite scarce, promoting the lionfish as a hard to beat opponent.

1

Managing the lionfish invasion Attempts to hinder biological invasions can be divided into three main stages, 1) keeping them out, 2) if they get in, finding and trying to eradicate them as quickly as possible, and 3) if they cannot be eradicated, managing them at low levels (Mack et al. 2000; Simberloff et al. 2005).

Considering the Mediterranean Sea, keeping invaders out is the most challenging option in the battle against alien species, since it is almost impossible to entirely close the Suez Canal, which is responsible from majority of the tropical species introductions. Indeed, scientists are currently concentrated on predicting the probable negative effects of the Suez Canal enlargement, which has not (at present) led to a wave of new bioinvasions as anticipated (Zenetos 2017).

Preventing invaders at source should not be ignored that certainly requires close cooperation of countries neighboring the Suez Canal.

According to the data available, none of the eastern Mediterranean countries have attempted to eradicate the initially introduced population of lionfish, for a variety of predictable reasons. In fact, eradicating lionfish (or any other successfully established invasive alien species) with currently available tools and technology is almost impossible (CĂ´tĂŠ et al. 2014). Common problems require regional and international cooperation, but yet many Mediterranean countries face similar constraints in the invasive species efforts, such as low public awareness (the situation in Lebanon has recently been examined by Azzurro and Bariche 2017), inadequate monitoring capacity, absence of clear and agreed priorities for action, lack of effective emergency response measures, outdated or inadequate legislation and poor co-ordination between government and other stakeholders (Genovesi and Shine 2004).

Recalling the last option to hinder biological invasions (if you can’t eradicate them, then manage them), the most tangible action was taken in Cyprus by the EU funded project RELIONMED-LIFE (Preventing a lionfish invasion in the Mediterranean through early response and targeted removal). Such important attempts with scientific basis are expected to increase in number also in other countries, which will help to achieve the desired goal of minimizing negative impacts of lionfish.

Current controls The aim of control is to reduce the density and abundance of an invasive alien species (IAS) to keep its impact to an acceptable level in the long term (Genovesi and Shine 2004). Controlling invasive lionfish populations has become a major objective of many countries and achieving lionfish control objectives require appropriately prepared plans since the most essential resources (such as money, trained staff, etc.) are limited (Usseglio et al. 2017). According to the experience 2

gained from the Atlantic coasts, culling is currently the most efficient management strategy used to control the existing lionfish populations. For lionfish removal activities, the first step should be to identify sites of particular interest, such as ecologically sensitive sites, spawning aggregation areas, nursery sites, marine protected areas or tourism areas (Morris 2012). Frazer et al. (2012) suggested that targeted removals by volunteers can reduce Pterois spp. abundances across multiple sites and thus represent a viable option for shifting direct impacts of lionfish away from highly vulnerable components of ecosystems. Removal efforts are effective in reducing the number and size of invasive lionfish at the southern Caribbean (de LeĂłn et al. 2013), Trinidad and Tobago (Alemu 2016), Belize (Searle et al. 2012) and several other localities.

Resources are limited in most cases, so public involvement in detection and control efforts are generally desired. Available means of detection and removal include supervised volunteers, derbies, fishing clubs, dive clubs, researchers engaged in lionfish-specific studies, NGOs, partner agencies, etc. (McCreedy et al. 2012). Lionfish removal can also become a part of the tourism trade, especially by the presence of divers or tourists who enjoy diving and snorkeling, which also has a potential to contribute to the local economy (Morris 2012).

Human consumption The tasty flesh of the lionfish provided a very good opportunity in turning a problem into a benefit. Human consumption of lionfish is a plausible option for creating harvest pressure because of their firm and mild meat, and a demand for lionfish providing high market value and additional incentives for harvesting could be created (Morris and Whitfield 2009). Scorpaenids appear to be a part of the Mediterranean cuisine for centuries, so locals will probably find the taste familiar. Anyhow, this benefit comes with its own risks. In most "eating invader" campaigns, the fundamental objective is to eat the target species out of existence, just as humans have done for many native species; however, encouraging the complete removal of the monetarily valuable species could be hard once a species becomes an economic resource (NuĂąez et al. 2012).

Robots vs. lionfish Lionfish invasion tend to begin in shallow habitats, progressing to deeper (slightly over 100 m) habitats with time (Nuttall et al. 2014). Thus lionfish presence in deep waters is a major concern for lionfish management and control, since they are inaccessible to spearfishers and culling efforts in shallow depths may be replenished by larval export from lionfish at depth (Johnson and Swenarton 2016). An innovative solution for the above mentioned problem is the use of lionfish-hunting robots, in which quite remarkable progress have been made lately. For example, researchers from the Worcester Polytechnic Institute have developed an autonomous robot that is capable of hunting down lionfish all on its own (Lombardi et al. 2018), while a non-profit organization (RISE - Robots in Service of the Environment, www.robotsise.org) have built a human steered robot that stun the fish, allowing the robot to suck it into a holding tank. Since these 3

robots are capable of operating more hours per day and at greater depths than human divers, they may effectively control the lionfish population at the local level. There is no doubt that robotic technologies could significantly increase our ability to tackle the wide range of problematic invasive species across the world in the near future, but relevant costs are currently quite high and might be prohibitive particularly for developing nations (Sutherland et al. 2010).

Natural predators Due to their venomous spines, lionfish naturally bear few natural predators. A notable Lessepsian invader, Fistularia commersonii, might potentially consume lionfish (most probably juveniles) in the Mediterranean Sea (Bariche et al. 2013).

Groupers may also feed on lionfish, as they do in the Atlantic (Morris and Whitfield 2009), but there are currently no data to reveal whether the probable predation mortality on lionfish will be significant enough to provide reduction in the existing established population. This is not an expected option at least for Turkey, where Epinephelus marginatus stocks are poorly managed and under heavy fishing pressure (Bilecenoğlu 2011), while current abundance of the species (and its confamilial members) in rest of the eastern Mediterranean basin is not well documented.

Suggested actions in the Mediterranean Sea Although there are many controls available for use against lionfish, the existing population in the Mediterranean Sea is too widespread for complete eradication, so management should be focused on specific regions (such as marine protected areas as a priority). All management efforts should aim at minimizing the negative effects of the invasive lionfish on native marine communities.

•

•

•

Monitoring activities: Lionfish population(s) should be monitored in order to assess their abundance, distribution and habitat utilization. Monitoring in different stages (initial/advanced) of invasion and methods in data collection (i.e. in situ observations, targeted captures) should be determined according to the characteristics of each unique habitat available in the eastern Mediterranean. Standardized methodology is of great importance.

Controlling populations: Sustained lionfish removals are proved to be very efficient even at local levels. Divers, snorkelers, recreational and commercial anglers and researchers will probably be the most effective staff, who are required to be appropriately trained prior to any kind of lionfish cull. A variety of tools are available to control lionfish, each with specific pros and cons, for example hand nets (low cost; effective for all sizes of lionfish), spear guns (high cost; effective for larger fish), slurp guns (high cost; live capture), etc. (see McCreedy et al. 2012 for details).

Research priorities: Majority of the scientific studies published so far on Mediterranean lionfish populations have concentrated on their distribution (see Azzurro et al. 2017), while a few molecular biology studies (e.g. Bariche 4

•

et al. 2017; Stern et al. 2018) and public awareness analysis (Azzurro and Bariche 2017) exist. Finding out the bio-ecological characteristics of lionfish in the Mediterranean Sea is crucial, hence age/growth, feeding, reproduction etc. of the species should be studied across its distribution range. Effective management relies on sound scientific knowledge.

Public awareness: Increasing public awareness of lionfish impacts is essential to generate support for effective management. Posters, fact sheets and sighting forms should be prepared and distributed throughout the Mediterranean countries impacted from lionfish invasion. People are not only needed to know how an invasive species like lionfish can harm the ecosystems and socio-economy, but also should be cautioned against handling lionfish and made aware of the health risks from their stings; an example from Turkey is presented in Figure 1.

5

Figure 1. The poster produced by TUDAV (Turkish Marine Research Foundation) in Turkey announcing lionfish threat

6

References Alemu, J.B. (2016) The status and management of the lionfish, Pterois sp. in Trinidad and Tobago. Marine Pollution Bulletin 109: 402-408.

Azzurro, E., Bariche, M. (2017) Local knowledge and awareness on the incipient lionfish invasion in the eastern Mediterranean Sea. Marine and Freshwater Research 68(10): 1950-1954.

Azzurro, E., Stancanelli, B., Di Martino, V., Bariche, M. (2017) Range expansion of the common lionfish Pterois miles (Bennett, 1828) in the Mediterranean Sea: an unwanted new guest for Italian waters. Bioinvasion Records 6(2): 95-98.

Bariche, M., Kleitou, P., Kalogirou, S., Bernardi, G. (2017) Genetics reveal the identity and origin of the lionfish invasion in the Mediterranean Sea. Scientific Reports 7: 6782. doi: 10.1038/s41598-017-07326-1 Bariche, M., Torres, M., Azzurro, E. (2013) The presence of the invasive Lionfish Pterois miles in the Mediterranean Sea. Mediterranean Marine Science 14(2): 292-294.

Bilecenoğlu, M. (2011) The current status and recommendations for the conservation of grouper (Epinephelus marginatus) in Turkey. Ulusal Deniz Koruma Alanları Sistemi, Denizel Değerlerimiz Serisi 1: 1-8 (in Turkish, with English abstract).

Bilecenoğlu, M. (2017) Is Turkey ready to face with lionfish (Pterois spp.) invasion? Journal of Black Sea/Mediterranean Environment 23(1): 75-80.

Côté, I.M., Akins, L., Underwood, E., Curtis-Quick, J., Green, S.J. (2014) Setting the record straight on invasive lionfish control: Culling works. PeerJ PrePrints doi: 10.7287/peerj.preprints.398v1 de León, R., Vane, K., Bertuol, P., Chamberland, V.C., Simal, F., Imms, E., Vermeij, M.J. (2013) Effectiveness of lionfish removal efforts in the southern Caribbean. Endangered Species Research 22: 175-182.

Eddy, C., Pitt, J., Morris Jr. J.A., Smith, S., Goodbody-Gringley, G., Bernal, D. (2016) Diet of invasive lionfish (Pterois volitans and P. miles) in Bermuda.

Marine Ecology Progress Series 558: 193-206.

7

Frazer, T.K., Jacoby, C.A., Edwards, M.A., Barry, S.C. Manfrino, C.M. (2012) Coping with the Lionfish Invasion: Can Targeted Removals Yield Beneficial Effects?. Reviews in Fisheries Science 20(4): 185-191.

Gardner, P.G., Frazer, T.K., Jacoby, C.A., Yanong, R.P.E. (2015) Reproductive biology of invasive lionfish (Pterois spp.). Frontiers in Marine Science 2(7): 110.

Genovesi, P., Shine, C. (2004) European Strategy on Invasive Alien Species.

Council of Europe Publishing, Nature and Environment No. 137, 68 pp.

Golani, D., Sonin, O. (1992) New records of the Red Sea fishes, Pterois miles (Scorpaenidae) and Pteragogus pelycus (Labridae) from the eastern Mediterranean Sea. Japanese Journal of Ichthyology 39(2): 167-169.

Johnston, M.W., Purkis, S.J. (2014) Are lionfish set for a Mediterranean invasion?

Modelling explains why this is unlikely to occur. Marine Pollution Bulletin 88(12): 138-147.

Johnson, E.G., Swenarton, M.K. (2016) Age, growth and population structure of invasive lionfish (Pterois volitans/miles) in northeast Florida using a lengthbased, age-structured population model. PeerJ 4: e2730 doi: 10.7717/peerj.2730.

Lombardi, J., Godsey, W., Kelly, B., Uvarov, N., Yuzvik, A. (2018) Autonomous lionfish harvester. Major qualifying project, Worcester Polytechnic Institute, 67 pp. https://digitalcommons.wpi.edu/mqp-all/2499/ Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M., Bazzaz, F.A. (2000) Biotic invasions: causes, epidemiology, global consequences, and control.

Ecological Applications 10: 689-710.

McCreedy, C., Toline, C.A., McDonough, V. (2012) Lionfish Response Plan: A Systematic Approach to Managing Impacts from the Lionfish, an Invasive Species, in Units of the National Park System. Natural Resource Report NPS/NRSS/WRD/NRR—2012/497. National Park Service, Fort Collins, Colorado, 99 pp.

Morris, J.A.Jr. (Ed.). (2012) Invasive Lionfish: A Guide to Control and Management. Gulf and Caribbean Fisheries Institute Special Publication Series Number 1, Marathon, Florida, USA. 113 pp.

Morris J.A.Jr., Whitfield, P.E. (2009) Biology, Ecology, Control and Management of the Invasive Indo-Pacific Lionfish: An Updated Integrated Assessment. NOAA Tech Memo NOSNCCOS 99. 57 pp.

8

Nuñez, M.A., Kuebbing, S., Dimarco, R.D., Simberloff, D. (2012) Invasive species: to eat or not to eat, that is the question. Conservation Letters 5: 334341.

Nuttall, M.F., Johnston, M.A., Eckert, R.J., Embesi, J.A., Hickerson, E.L., Schmahl, G.P. (2014) Lionfish (Pterois volitans [Linnaeus, 1758] and P. miles [Bennett, 1828]) records within mesophotic depth ranges on natural banks in the Northwestern Gulf of Mexico. Bioinvasions Records 3(2): 111-115.

Searle, L., Chacon, N., Bach, L. (2012) The Belize Lionfish Management Plan: An Overview of the Invasion, Mitigation Activities and Recommendations.

ECOMAR Technical Publication No 1, 80 pp.

Simberloff, D., Parker, I.M., Windle, P.N. (2005) Introduced species policy, management, and future research needs. Frontiers in Ecology and Environment 3: 12-20.

Stern, N., Jimenez, C., Hüseyinoğlu, M.F., Andreou, V., Hadjioannou, L., Petrou, A., Öztürk, B., Golani, D., Rothman, S.B.S. (2018) Constructing the genetic population demography of the invasive lionfish Pterois miles in the Levant Basin, Eastern Mediterranean.

Mitochondrial DNA Part A, doi: 10.1080/24701394.2018.1482284.

Sutherland, W.J., Clout, M., Côté, I.M., Daszak, P., Depledge, M.H., Fellman, L., Fleishman, E., Garthwaite, R., Gibbons, D.W., De Lurio, J., Impey, A.J., Lickorish, F., Lindenmayer, D., Madgwick, J., Margerison, C., Maynard, T., Peck, L.S., Pretty, J., Prior, S., Redford, K.H., Scharlemann, J.P., Spalding., M., Watkinson, A.R. (2010) A horizon scan of global conservation issues for 2010.

Trends in Ecology and Evolution 25(1): 1-7.

Usseglio, P., Selwyn, J.D., Downey-Wall, A.M., Hogan, J.D. (2017) Effectiveness of removals of the invasive lionfish: how many dives are needed to deplete a reef? PeerJ 5: e3043 doi: 10.7717/peerj.3043.

Whitfield, P.E., Hare, J.A., David, A.W., Harter, S.L., Muñoz, R.C., Addison, C.M. (2007) Abundance estimates of the Indo-Pacific lionfish Pterois volitans/miles complex in the Western North Atlantic. Biological Invasions 9: 5364.

Zenetos, A. (2017) Progress in Mediterranean bioinvasions two years after the Suez Canal enlargement. Acta Adriatica 58(2): 347-358.

9

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

The invasion and establishment of lionfish species (Pterois spp.) as a major threat to marine biodiversity of Turkey Cemal TURAN Molecular Ecology and Fisheries Genetics Laboratory, Marine Science and Technology Faculty, Iskenderun Technical University, Iskenderun, TURKEY Corresponding author: cemal.turan@iste.edu.tr

The invasion and establishment of alien species are amajor threat to marine biodiversity, marine structure and function which also have economic and human health implications (Charles and Dukes 2007; Otero et al. 2013). There are 10 valid species of the genus Pterois in the world (Froese and Pauly 2016). Lionfish inhabit warm marine waters at depths from 1 to 300 feet on hard bottom, mud bottoms, mangroves, sea grasses and coral reefs (Albins and Hixon 2008; Ferreira 2015). The high feeding rates of lionfish pose a serious threat to benthic ecosystems (Morris and Akins 2009; Higgs 2013).

Figure 1. Lionfish Pterois miles from Keldağ, Iskenderun Bay, Turkey (by C.Turan).

Lionfish Pterois miles was recorded for the first time from the Mediterranean Sea at Haifa Bay in 1991 (Golani and Sonin 1992), and later lionfish P. miles were reported from Lebanon coast (Bariche et al. 2013) and Cyprus coast (Evripidou 2013) in the Mediterranean Sea. Lionfish P. miles was first time reported from 10

Turkish marine waters in 2014 that a single specimen was captured in the Iskenderun Bay, north-eastern Mediterranean part of Turkey (Turan et al. 2014).

Therefore, the occurrence of this species in the Turkish waters seems to be due to its range expansion from the southern to the northern Mediterranean (Figure 2).

Figure 2. Spatial and temporal distribution and possible migration direction of Pterois miles in the Mediterranean Sea. , indicate location and direction of the migration according to the records. The numbers are arranged according to the time of occurrence.

1, Golani and Sonin (1992); 2, Bariche et al. (2013); 3, Evripidou (2013); 4, Turan et al.

(2014); 5, Yaglioglu and Ayaş (2016); 6, Turan and Öztürk (2015).

After first observation of P. miles in Iskenderun Bay, rapid expansion was observed from Iskenderun Bay to Mersin and Antalya Bays (Turan and Öztürk 2015; Yaglioglu and Ayaş 2016). First observation of P. miles from the Aegean Sea was reported from Fethiye Bay in July 2015 and Dalyan coast in August 2015 (Figure 2) (Turan and Öztürk 2015). These observations indicate that P. miles is 11

successfully and rapidly expanding from the Mediterranean coasts northward to the Aegean Sea (Figure 2). Its extension in the Aegean Sea may be determined by sea temperature (Turan et al. 2016).

Figure 3. Pterois volitans from Iskenderun Bay, Turkey (by C. Turan).

The red lionfish Pterois volitans (Linnaeus 1758) (Figure 3) is distributed in the Pacific Ocean (North and South), Atlantic Ocean (North and South) and also found in the Indo-West Pacific Ocean (Schultz 1986; Whitfield et al. 2002; Kimball et al. 2004; Froese and Pauly 2016). Red lionfish Pterois volitans was recorded for the first time from Iskenderun Bay, north-eastern Mediterranean part of Turkey (Gurlek et al. 2016) that was first record of the red lionfish P. volitans along the Mediterranean Sea. Westward extension of the red Lionfish Pterois volitans along the Mediterranean Coast of Turkey was rapidly started with Mersin Bay (Ayas et al. 2018) and then Antalya Bay (GĂśkoÄ&#x;lu et al. 2017) that indicate the establishment of the red lionfish in the Mediterranean Sea.

12

Figure 4. Dusky grouper Ephinephelus marginatus feeds on lionfish in Keldag, Iskenderun Bay, Turkey (by C.Turan).

Grouper species such as dusky grouper and gold blotch grouper feed on the lionfishes (Figure 4) (Turan et al. 2017). Therefore, top predators are very important to decrease lionfishes populations that indicate conservation of top predators to struggle lionfishes in Turkish marine waters since fishing activities such as trawling and purse seiner and also nets do not help to struggle lionfish which usually inhabit under big rocks and caves. On the other hand, few individuals were also captured with trawlers (Figure 5).

Lionfish density tends to be increased in marine waters of Turkey, and also along the Mediterranean Sea. There are 10 valid species of the lionfishes inhabiting in the Pacific Ocean and Atlantic Ocean, and it is not known at the moment, how many other species will come to the Mediterranean Sea. The tropicalization of the Mediterranean Sea will probably increase the number of lionfishes and other similar Erythrean fishes (Turan et al. 2016, 2018).

13

Figure 5. Lionfish captured with other fish by trawlers in the Iskenderun Bay, Turkey (by C. Turan).

Countries in the western Atlantic and now in the Mediterranean Sea facing serious problems with lionfishes and organising many campaigns to eradicate lionfish (Wanted: Lionfish, TÜDAV). However, some researchers point out that complete eradication of lionfish is impossible, these campaigns only help to keep their population under control and protect the native marine ecosystems.

References Albins, M.A., Hixon, M.A. (2008) Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Marine Ecology Progress Series 367: 233-238.

Ayas, D., Şen Ağılkaya, G., Yağlıoğlu, D. (2018) New occurrence of the red lionfish Pterois volitans (Linnaeus, 1758) in the north eastern Mediterranean (Yeşilovacık Bay). Düzce Üniversitesi Bilim ve Teknoloji Dergisi 6(4): 871-877.

Bariche, M., Torres, M., Azzurro, E. (2013) The presence of the invasive Lionfish Pterois miles in the Mediterranean Sea. Mediterranean Marine Science 14(2): 292-294.

14

Charles, H., Dukes, J.S. (2007) Impacts of invasive species on ecosystem services. In Biological Invasions (ed., Nentwig, W.) Ecological Studies, Vol. 193, Springer-Verlag, Berlin. pp. 217-237.

Evripidou, S. (2013) The Free Library. Toxic Lionfish makes its way to Cyprus waters. Available at https://www.thefreelibrary.com/Toxic+lionfish+makes+its+way+to+Cyprus+wa ters.-a0319558097 (accessed 20 Feb. 2013).

Ferreira, C.E., Luiz, O.J., Floeter, S.R., Lucena, M.B., Barbosa, M.C., Rocha, C.R., Rocha, L.A. (2015) First record of invasive lionfish (Pterois volitans) for the Brazilian coast. PLoS One 10(4): e0123002.

Froese, R., Pauly, D. (2016) FishBase. World Wide electronic publication. http://www.fishbase.org, version (07/2016) (accessed 23 Jul. 2016).

Golani, D., Sonin, O. (1992) New records of the Red Sea fishes, Pterois miles (Scorpaenidae) and Pteragogus pelycus (Labridae) from the eastern Mediterranean Sea. Ichthyological Research 39(2): 167-169.

Gรถkoฤ lu, M., Teker, S., Julian, D. (2017) Westward extension of the lionfish Pterois volitans Linnaeus, 1758 along the Mediterranean coast of Turkey. Natural and Engineering Sciences 2(2): 67-72.

Gurlek, M., Erguden, D., Dogdu, S.A., Uyan, A., Turan, C. (2016) First record red lionfish, Pterois volitans (Linnaeus, 1785) in the Mediterranean Sea. Natural and Engineering Sciences 1(3): 27-32.

Higgs, N.D. (2013) The feeding habits of the Indo-Pacific lionfish Pterois volitans at artificial lobster habitats in the Bahamas. First published online January 2013. www.nickhiggs.com, 2-2 (accessed 02 Oct. 2018).

Kimball, M.E., Miller, J.M., Whitfield, P.E., Hare, J.A. (2004) Thermal tolerance and potential distribution of invasive lionfish (Pterois volitans/miles complex) on the east coast of the United. Marine Ecology Progress Series 283: 269-278.

Morris, J.A., Akins, J.L. (2009) Feeding ecology of invasive lionfish (Pterois volitans) in the Bahamian archipelago. Environmental Biology of Fishes 86: 389.

Otero, M., Cebrian, E., Francour, P., Galil, B., Savini, D. (2013) Monitoring Marine Invasive Species in Mediterranean Marine Protected Areas (MPAs): A strategy and practical guide for managers. IUCN. Malaga, Spain. pp. 136.

15

Schultz, E.T. (1986) Pterois volitans and Pterois miles: two valid species. Copeia 1986(3): 686-690.

Turan, C., Ergüden, D., Gürlek, M. (2016) Climate change and biodiversity effects in Turkish Seas. Natural and Engineering Sciences 1(2): 15-24.

Turan, C., Ergüden, D., Gürlek, M., Yaglioglu, D., Uyan, A., Uygur, N. (2014) First record of the Indo-Pacific lionfish Pterois miles (Bennett, 1828) (Osteichthyes: Scorpaenidae) for the Turkish marine waters. Journal of Black Sea/Mediterranean Environment 20(2): 158-163.

Turan, C., Gürlek, M., Başusta, N., Uyan, A., Doğdu, S., Karan, S. (2018) A checklist of the non-indigenous fishes in Turkish Marine Waters. Natural and Engineering Sciences 3(3): 333-358.

Turan, C., Öztürk, B. (2015) First record of the lionfish Pterois miles from the Aegean Sea. Journal of Black Sea/Mediterranean Environment 21(3): 334-338.

Turan, C., Uygur, N., İğde, M. (2017) Lionfishes Pterois miles and Pterois volitans in the North-eastern Mediterranean Sea: Distribution, habitation, predation and predators. Natural and Engineering Sciences 2(1): 35-43.

Whitfield, P.E., Gamer, T., Viues, S.P., Gilligan, M.R., Courtenay Jr., W.R., Ray, G. C., Hare, J.A. (2002) Biological invasion of the Indo-Pacific lionfish Pterois volitans along the Atlantic coast of North America. Marine Ecology Progress Series 235: 289-297.

Yaglioglu, D., Ayas, D. (2016) New occurrence data of four alien fishes (Pisodonophis semicinctus, Pterois miles, Scarus ghobban and Parupeneus forsskali) from the North Eastern Mediterranean (Yeşilovacık Bay, Turkey).

Biharean Biologist 10(2): 150-152.

16

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

The current status of lionfish invasion in Greece and future steps towards control and mitigation Ioannis GIOVOS1*, Ioannis BATJAKAS2, Nikolaos DOUMPAS1, Thodoros Eystratios KAMPOURIS2, Dimitris POURSANIDIS3, Vangelis PARAVAS1 iSea, Environmental Organisation for the Preservation of the Aquatic Ecosystems, 11 Ochi Av., 55438, Agios Pavlos, Thessaloniki, GREECE 2 Department of Marine Sciences, School of the Environment, University of the Aegean, Mytilene, Lesvos Island, 81100, GREECE 3 Foundation for Research and Technology - Hellas (FORTH), Institute of Applied and Computational Mathematics, rslab.gr, N. Plastira 100, Vassilika Vouton, 70013, Heraklion, GREECE 1

*Corresponding

author: ioannis.giovos@isea.com.gr

Current state of the expansion and establishment of the invasive lionfish in Greece The common lionfish, Pterois miles (Scorpaeniformes, Scorpaenidae, Pteroinae) is considered one of the most invasive species in the world, causing a significant amount of detrimental effects in the invaded communities (Albins and Hixon 2008). Within its native range P. miles is distributed in the Indian Ocean from South Africa to the Red Sea and the Persian Gulf. In the early 90s the Caribbean Sea experienced the beginning of the species devastating invasion, starting from Florida (Albins and Hixon 2008). Within five years, lionfish had invaded the largest parts of the Caribbean Sea (Mumby et al. 2011), and colonised approximately 7.3 million km2 of the western Atlantic and Caribbean regions (Côté et al. 2013). In the Mediterranean, P. miles was first recorded in 1991 off the Israeli coast (Golani and Sonin 1992), but it was not until 2012 that the species was recorded again in the basin, in Lebanon (Bariche et al. 2013). Since 2012, P. miles has been constantly expanding, invading new areas, as documented by numerous reports from countries of the Eastern Mediterranean, namely Lebanon (Azzurro et al. 2017b), Turkey (Turan et al. 2014, Turan and Öztürk 2015; Özbek et al. 2017; Turan et al. 2017), Cyprus (Jimenez et al. 2016; Kletou et al. 2016), Greece (Corsini-Foka and Kondylatos 2015; Sterioti 2016; Poursanidis and Marakis 2016; Giovos et al. 2018), Tunisia (Azzurro et al. 2017b) and Italy (Azzurro et al. 2017b). The species is currently considered as established in all Eastern Mediterranean basin (Kletou et al. 2016), including Greece (Giovos et al.

2018), raising serious concerns for the potential impacts on the local marine ecosystems and the native species, given the experience from other regions (Albins and Hixon 2008).

17

Figure 1. Some of the lionfish observations reported to the citizen science project of iSea “Is it Alien to you? Share it!!!”

In Greece, the first record of P. miles was reported in 2015 from Rhodes Island (Corsini-Foka and Kondylatos 2015) and over the last 3 years the species has expanded towards the northeast Aegean Sea (currently a record from Lipsi island is the northernmost reported location of the species in the basin) and has significantly increased its numbers (Giovos et al. 2018), with the south Cretan coast and the coast of Rhodes being already overwhelmed. Pterois miles is now expanding westwards within the Greek waters, as indicated by a recent report from Kythera Island, which was provided by a professional small-scale fisher to the citizen science project of the environmental non-governmental Greek organization iSea, “Is it Alien to you? Share it!!!” (Figure 1a) (Mitsou and Maximiadi 2018). Within the context of iSea’s citizen science project, several data on the species occurrence in Greek waters have been collected (up to date 105 reports), a significant dataset compared to the information that is available in scientific articles. Thus, this project has led up to as a unique and consistent tool for monitoring the expansion of the species. In the framework of species distribution modelling (SDM) and through the use of MaxEnt, occurrence data, in correlation with environmental predictors, such as sea surface temperature and salinity, calibrated with data from all Mediterranean countries (based though solely on literature data), it was shown that the lionfish has the potential to arrive at north Aegean, mainly at the Greek-Turkish coastline up to Lesvos island, while it will also be able to reach the Ionian Sea (Figure 2). The up-to-date westernmost 18

occurrence of the species in Greece has been confirmed through a report from Kythira Island (data from iSea’s citizen science project). Based on the latter, larvae of the lionfish could drift further west, transferred by surface currents. This can result in the expansion of the species according to the model’s prediction (Figure 3). This prediction is also supported by the records of P. miles coming from Italy in Sicily but also from Tunisia (Azzurro et al. 2017b).

Figure 2. Observations of lionfish reported to the citizen science project of iSea “Is it Alien to you? Share it!!!” in comparison to available data from the literature

A review of the foraging behaviour and feeding ecology of the invasive lionfish Pterois miles with preliminary data off Mediterranean waters In general, lionfish is a carnivory, opportunistic and generalist feeder, presenting ontogenic shifts on its diet (Peake et al. 2018), with seasonality and plasticity affected by the habitat type, the fish size (Layman and Allgeier 2012; Dahl and Patterson 2014), the time of the day (del Carmen García-Rivas et al. 2018) and the population density (Benkwitt 2016). In the Bahamas, lionfish found to be a more specialized feeder than some of the native snappers (Layman and Allgeier 2012) feeding during the day, peeking in the morning between 08:00 to 11:00 19

(Morris and Akins 2009). However, different studies from the Bahamas present dissimilarities on the lionfish prey composition. For instance, Morris Jr and Akins (2009) stated that 78% of the prey species were teleosts and crustaceans -mainly at younger individuals, (41%, in terms of volume). In contrary, Alexander and Hayes (2011) reported only three species, as main prey, and no effects on the local reef community. Last, Layman and Allgeier (2012) state that lionfish is predating almost exclusively on small fish species. On the other hand, studies from the Mexican Caribbean coast revealed that young lionfish are nocturnal feeders and prefer dark areas, whilst older individuals are diurnal preferring clear areas (del Carmen GarcĂ­a-Rivas et al. 2018). In addition, the prey composition of the species in the Mexican Caribbean found to be wide, including 34 species, belonging to 22 genera, 14 families and 5 orders (Valdez-Moreno et al. 2012). Furthermore, large individuals (>250 mm TL) were piscivorous while smaller ones (<200 mm) preferred benthic invertebrates (Dahl and Patterson 2014). Arredondo-ChĂĄvez et al. (2016) reported 76 prey species, 41 being fishes and 29 being crustaceans, belonging to Pomacentridae, Labridae, Scaridae, Rhynchocinetidae, Penaidae and Solenoceridae families accordingly.

Figure 3. Probability of occurrence based on Species Distribution Modelling output

20

Molecular techniques revealed 24 new lionfish prey species, such as Lutjanus campechanus from Mexico (Dahl et al. 2017). Data from Costa Rica identified several similarities with Mexico, for example, the lionfish diet varied significantly among studied sites, yet some important outcomes like that the prey items both in terms of volume (85%) and frequency (71%) were teleost species belonging mainly to Pomacentridae, Acanthuridae, Blenidae, Labridae and Serranidae families (Sandel et al. 2015). Similar findings, based on DNA metabarcoding, are reported from Puerto Rico, with 34 fish species belonging to Pomacentridae, Acanthuridae, Gobiidae, Apogonidae and Scaridae families (Harms-Tuohy et al.

2016).

A preliminary study from Greek waters 1, based on a few specimens, revealed that P. miles is a rather successful predator, since all individuals had full stomachs.

Also, it seems that the species though being an opportunistic carnivore is very specialized. Mainly, the prey was individuals of Family Pomacentridae (Figure 4). Furthermore, an individual of Family Gobiidae was observed, while the other prey items include an Alpheus sp. and two individuals belonging at the Suborder Pleocyemata (Table 1). Our findings are in accordance with preliminary results from the stomachs of lionfish from Cyprus collected in the context RELIONMED LIFE project, in which Chromis chromis was the most prevalent trophic item (personal communication with P. Kleitou).

To assess the lionfish diet in the Greek-Mediterranean waters in a better way, further and systematic research is required. The authors of this chapter section are preparing a relative article (Zannaki et al. in prep.) examining lionfish caught in the east Rhodes Island, Dodecanese, South Eastern Aegean Sea. In contrast to the findings presented above, the diet from approximately 50 specimens from that area displayed a quite decreased specialization. Teleost fish were the dominant prey items but even though members of the family Pomacentridae were present, they were not the main prey items. Generally, the present findings are in accordance with the findings from the Caribbean, since pomacentrids were the main prey of primarily Pterois volitans, in different areas. It should not be a surprise, since predators are attracted to species that resemble their usual prey.

The stomach content of eight lionfish individuals presented in Table 1 analysed by I.E. Batjakas and T.E. Kampouris.

1

21

Figure 4. Individuals of Family Pomacentridae, found in the stomach of lionfish from the Greek waters

In terms of predators, lionfish seem to have only few in the invaded regions. For instance, some grouper species have the potential to act as natural biocontrol through predation, but since they are overharvested the success is limited (Mumby et al. 2011; IUCN 2018). In the Bahamas, moray eels consumed injured, yet alive lionfishes and it seems that can be a control agent of the lionfish invasion (Pimiento et al. 2013). Moreover, on their native range in Egypt, lionfishes were observed avoiding the areas where moray eels occurred, indicating a predatorprey relationship (Bos et al. 2017). In Mediterranean waters, based on observations, there are similar indications that species such as Epinephelus marginatus and E. costae, consumed or have the potential to prey on lionfishes (Turan et al. 2017). Also, Turan et al. (2017) indicated Pempheris spp., Apogon spp. and Sargocentron rubrum as potential lionfish prey in the Mediterranean Sea. The public opinion about the invasive lionfish in Greece Invasive species are considered as a major threat for biodiversity and one of the foremost environmental concerns of our times, costing millions of euros to the local communities across the globe (Didham et al. 2005; Pimentel et al. 2005).

Public opinion plays an important role in the mitigation and management processes of invasive species by supporting (or not) the implementation of the relevant policies (Sharp et al. 2011). Often, opinions and proposals between managers, conservationists and other stakeholders are opposing, especially when involving measures of lethal eradication of invasive charismatic species or of species beneficial to the local communities. The common lionfish is a combination of a charismatic and partially beneficial invasive species, which attracts the public attention, while it is very popular for the diving community, 22

but also highly detrimental for the local ecosystems (Albins and Hixon 2008), posing a serious threat to commercially important (Valdez-Moreno et al. 2012) and endemic or critically endangered species (e.g. wrasse species in Belize; Rocha et al. 2015).

Since the introduction of P. miles in the Mediterranean Sea, two studies have dealt with the opinion of the public and the fishing communities towards the species (in Cyprus and Lebanon, respectively; Jimenez et al. 2017; Azzurro and Bariche 2017a). In the context of this work, we tried to understand the opinion of the Greek public and detect potential differences of the perception among stakeholders (e.g. professional and recreational fishers, scientists, managers, coast guards etc.) through an online skip logic questionnaire, consisting of 14 questions.

The questionnaire initiated with a section collecting the demographic information of the respondents, followed by a second section investigating their opinion (Figure 5). The questionnaire was distributed online through the social media channels of iSea between 1/8/2018 and 1/9/2018. In total 445 questionnaires were collected after the survey.

Figure 5. The skip logic questionnaire prepared for this work. Multiple choice answers can be found in Figure 5a and 5b

The majority of the respondents were men (≈78%), ranging between 25-54 years old (≈78%), acquired a higher education qualification (≈64%) and were inhabitants of Athens (≈34%), Thessaloniki (≈10%), Irakleio (≈6%), and Rhodes (≈5%). Regarding the question of the respondents’ occupation, the majority (≈30%) were not employed as one of the following occupations that are related to the marine environment, namely spear gun-fisher (≈22%), recreational fisher (≈19%), recreational scuba diver (≈13%), researchers (≈8%), professional scuba 23

diver (≈5%), professional fishers (≈1%), public servants, coast guard etc. (≈1%), chefs, restaurant employees, fishmongers (≈1%).

Almost 96% of the respondents replied that they are aware of the lionfish invasion in the Greek waters, primarily informed through internet blogs, sites and social media. More than 90% of all different stakeholders responded that they are aware of the detrimental effects of the lionfish in the local biodiversity and the local ecosystems (Figure 6a), and ≈89% believe that the species has also an adverse effect on the local economy (Figure 6b). These answers were independent of the respondents’ occupation in all cases. However, independently of the stakeholder group (e.g. fishers, divers, other), the statement “Lionfish attracts touristic traffic (e.g. divers) in the region” received a relatively high number of responses (≈9% of the total number of answers (Figure 6b). Interestingly, ≈93% of the respondents are aware that lionfish is venomous (Figure 6c), however only ≈67% of them know that the species is edible (Figure 6d) and only ≈42% declared that would eat one (Figure 6e), with the numbers being independent of the occupation.

Figure 6. (a) Percentage of responses about the impacts (positive/negative) of the lionfish on the local ecosystems and (b) the local economy, (c) if lionfish is venomous, (d) edible and (e) if the respondent would consume lionfish

The above results indicate that although the Greek public is relatively well informed about the lionfish invasion in the Greek waters and the fact that the species is highly venomous, still a large part of the public is not aware that the species is edible and therefore seems unlikely to insert the species in the Greek cuisines in the near future.

24

Lionfish in the Greek cuisine Fighting invasive alien species through gastronomy is a popular approach both in terrestrial and aquatic ecosystems (Nuñez et al. 2012). In the case of lionfish, promoting targeted removals for consumption in the context of food/cooking festivals is extremely attractive and has gained the attention of citizens, especially in the Caribbean and the near areas (Frazer et al. 2012). Such campaigns, when designed properly (Nuñez et al. 2012) have been proven valuable tools for lowering the expansion rate of P. miles by turning this unstoppable predator into a delicacy and at the same time enhancing participation and promote citizen stewardship. The “Lionfish Removal and Awareness Day Festival” in Florida is a successful example, in which scuba divers, celebrity chefs, fillet demonstrators and conservation vendors come together into a festival where everyone can taste a big variety of lionfish dishes, people learn about the problem and jointly move towards mitigation. Different recipes have been developed and a lot of chefs have mastered in gourmet lionfish dishes, while people continue consuming the species year round.

In Greece, lionfish was recorded for the first time only recently. Therefore, the species is still not part of the Greek cuisine, as happens with many other alien and invasive marine species, due to the fact that consumers are not familiar with them.

However, established citizen science communities in Greece that target invasive marine species (iSea, is it Alien to you? Share it!!!), receive an increasing amount of reports indicating a recently growing lionfish consumption and a strong interest to find and share recipes regarding the lionfish. Grilled and served plain, or with vegetables, sundried with mustard, or fried with mush and mayonnaise are only some of the recipes emerging through the above-mentioned community. In addition, and since online media nowadays offer the possibility to get informed about activities taking place on the other side of the world, there is a strong interest from the Greek public on Lionfish festivals, promoting them as a mitigation measure for the species expansion in Greece. The latter should not be underestimated and might be the basis for organising similar events in Greece, although specific guidelines must be followed.

The EU legislative framework and alternatives on biological invasions management Biodiversity in marine, brackish, freshwater and terrestrial environments is threatened by biological invasions and species/population monitoring and management are essential for biodiversity loss privation (European Commission 2014; Mačić et al. 2018). Therefore, bioinvasions are of public concern (e.g.

Andaloro et al. 2016). The Mediterranean Sea is the most heavily impacted ecoregion globally since besides other vectors like shipping and aquaculture (Katsanevakis et al. 2014), the Lessepsian migration is the main introduction pathway in the area (Katsanevakis et al. 2014). Additionally, to the above since 25

January 2015 the EU has put into force the EU Regulation 1143/2014 on Invasive Alien Species, fulfilling Action 16 of Target 5 of the EU 2020 Biodiversity Strategy. This legislative instrument provides for a set of measures to be taken across the EU in relation to invasive alien species, based on a list of Invasive Alien Species of Union Concern (Implementing Regulation (EU) 2016/1141).

The latter list is not exclusive, and Member States can also prepare national or regional lists with invasive species of concern. Up to date, the lionfish has not been included in the Invasive Alien Species list, although it is widespread in the Eastern Mediterranean Sea and has been assessed as a species with very high risk (top category) “...for arrival, establishment, spread and threat to biodiversity and associated ecosystem services across the EU within the next ten years…” in the latest horizon scanning by EU in 2015 (Roy et al. 2015). However, the Regulation foresees that Member States can propose additional species for inclusion in the Union list, according to Article 4(4) of the Regulation documented through a risk assessment. The Regulation 1143/2014 is also accompanied by a series of relevant acts providing additional tools to the Member States for the specification, update, and reporting on IAS of Union Concern. In order to update the list of Invasive Alien Species of Union Concern, EU utilises a committee and an independent “Scientific Forum” to regularly perform horizon scanning for prioritising prevention efforts. However, the actual implementation of the legislation and the enlisting of species depends, to a large extend, on the committee of the Member States’ representatives that have to take the final decisions. This can potentially limit the power of the scientific advice due to political (or economic) considerations (Genovesi et al. 2015) Regarding Greece, national legislation, Biodiversity Law 3937/2011 on the conservation of biodiversity and other provisions, Art. 12 (Hellenic Republic 2011), foresees that specific measures and assessments need to be taken under the auspices of the Ministry of Environment for the combating of Invasive Alien Species. However, the regional and EU level legislation are not uniform, yet specific commitments and obligations arise from the EU Biodiversity Strategy, the Marine Strategy Framework Directive, the IAS EU Regulation, as well as other international and national instruments that set specific objectives regarding non-indigenous species and biodiversity protection. In order to address such a regional and spatially extensive biodiversity threat a multidisciplinary approach is necessary, considering fisheries management, ecology, economy and society (Commission Staff Working Document 2014; Kampouris 2018), as well as the development and adoption of legal instruments and formally adopted action plans on national and regional scales. Over and above a key element to successfully tackle bioinvasions, the active involvement of stakeholders, such as sea users, fishermen etc. due to their strong ecological knowledge and experience (e.g.

Heyman and Granados-Dieseldorff, 2012; DeCelles et al. 2017; Azzurro et al.

2018) is necessary.

26

Recently, since 2017 and towards the above direction, an EU co-financed LIFE Biodiversity project (RelionMed LIFE16 NAT/CY/000832) has commenced, targeting to make Cyprus the â&#x20AC;&#x2DC;first line of defenceâ&#x20AC;&#x2122; against the invasion of the lionfish in the Mediterranean Sea. Among the projectâ&#x20AC;&#x2122;s actions, a risk assessment will be developed, compatible with the EU Regulation 1143/2014, which may lead to the inclusion of this species to the list of Invasive Alien Species of Union Concern, as well as a replication strategy that will provide the necessary tools and strategies that need to be set up and implemented in the Eastern Mediterranean Sea, in order to combat lionfish in the region. This effort constitutes the first and most significant initiative for tackling the invasive alien species expansion in the Mediterranean, that will provide important information and proposals that may result in a coherent and region-wide technical and strategic response.

Additionally, to the above, the EU has developed several initiatives and instruments that may pose as paramount tools and financing opportunities for targeting Invasive Alien Species and the risks that stem from their expansion in the Eastern Mediterranean Region. Among the latter, Blue Growth constitutes a long-term EU strategy that sets specific priorities on the knowledge and legal certainty improvement and on tailor-made measures regarding sea basin strategies. Regarding Mediterranean Sea and biodiversity protection, Blue Growth focuses at the Mediterranean basin strategy that sets priorities on the protection of the marine environment (COM 2014; UfM 2017; Kampouris 2018).

Additional financial instruments developed by EU that could provide necessary funds, but also other resources are the LIFE - the EU's financial instrument for environmental, nature conservation and climate action projects, the Horizon 2020 - the EU Research and Innovation programme, the EU Rural Development policy 2014-2020, that provides opportunities to address invasive alien species through national and regional rural development programmes, and the Regional Development funding that may also include action on invasive alien species.

Furthermore, conventions, such as OSPAR, CBD and the Barcelona convention, set specific priorities and action plans on the protection of biological diversity, and therefore Invasive and Alien Species monitoring and potential mitigation.

In conclusion, there is still a considerable gap and a delay on informing legislation, and a lack of joint actions regarding the implementation of regional strategies and action plans about bioinvasions within EU and the Mediterranean countries, also as a result of the geopolitical complexity of the region. Yet there are legal tools, alternatives and on-going efforts like the RelionMed LIFE project, the EU Regulation on Invasive Alien Species, the EU Biodiversity Strategy and the Marine Strategy Framework Directive or even Blue Growth that have the potential to act as a basis for protecting the native biodiversity and mitigating the alien species adverse effects.

27

References Albins, M.A., Hixon, M.A. (2008) Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Marine Ecology Progress Series 367: 233-238.

Alexander, A.K., Hayes, J.M. (2011) Red lionfish (Pterois volitans) invade San Salvador, Bahamas: No early effects on coral and fish communities. The International Journal of Bahamian Studies 17(2): 50-66.

Andaloro, F., Castriota, L., Falautano, M., Azzurro, E., Deidun, A., FenechFarrugia, A. (2016) Public feedback on early warning initiatives undertaken for hazardous non-indigenous species: the case of Lagocephalus sceleratus from Italian and Maltese waters. Management of Biological Invasions 7(4): 313-319 Arredondo-Chávez, A.F., Sánchez-Jimenez, J.A., Ávila-Morales, O.G., TorresChávez, P., Herrerias-Diego, Y., Medina-Nava, M., Madrigal-Guridi, X., Campos-Mendoza, A., Domínguez- Domínguez, O., Caballero-Vázquez, J.A. (2016) Spatio-temporal variation in the diet composition of red lionfish, Pterois volitans, (Actinopterygii: Scorpaeniformes: Scorpaenidae), in the Mexican Caribbean: insights into the ecological effect of the alien invasion. Acta Ichthyologica et Piscatoria 46(3): 185-200.

Azzurro, E., Bariche, M. (2017a) Local knowledge and awareness on the incipient lionfish invasion in the eastern Mediterranean Sea. Marine and Freshwater Research 68(10): 1950-1954 doi: 10.1071/MF16358.

Azzurro, E., Stancanelli, B., Di Martino, V., Bariche, M. (2017b) Range expansion of the common lionfish Pterois miles (Bennett, 1828) in the Mediterranean Sea: an unwanted new guest for Italian waters. BioInvasions Records 6(2): 95-98.

Azzurro, E., Bolognini, L., Dragičević, B., Drakulović, D., Dulčić, J., Fanelli, E., Grati, F., Kolitari, J., Lipej, L., Magaletti, E., Marković, O., Matić-Skoko, S., Mavrič, B., Milone, N., Joksimović, A., Tomanić, J., Scarpato, A., Tutman, P., Vrdoljak, D. Zappacosta, F. (2018) Detecting the occurrence of indigenous and non-indigenous megafauna through fishermen knowledge: A complementary tool to coastal and port surveys. Marine Pollution Bulletin (in press) doi: 10.1016/j.marpolbul.2018.01.016.

Bariche, M., Torres M., Azzurro, E. (2013) The presence of the invasive lionfish Pterois miles in the Mediterranean Sea. Mediterranean Marine Science 14(2): 292-294.

28

Benkwitt, C.E. (2016) Invasive lionfish increase activity and foraging movements at greater local densities. Marine Ecology Progress Series 558: 255-266.

Bos, A.R., Sanad, A.M., Elsayed, K. (2017) Gymnothorax spp. (Muraenidae) as natural predators of the lionfish Pterois miles in its native biogeographical range.

Environmental Biology of Fishes 100(6): 745-748.

Commission Staff Working Document (2014) Marine Knowledge 2020: roadmap, Innovation in the Blue Economy realising the potential of our seas and oceans for jobs and growth. Brussels 2014. pp. 34 Corsini-Foka, M., Kondylatos, G. (2015) First occurrence of the invasive lionfish Pterois miles in Greece and the Aegean Sea. In: New Mediterranean Biodiversity Records (F., Crocetta, D., Agius, P., Balistreri et al.). Mediterranean Marine Science 16(3): 682-702.

Côté, I.M., Green, S.J., Hixon, M.A. (2013) Predatory fish invaders: Insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biological Conservation 164: 50-61.

Dahl, K.A., Patterson III, W.F. (2014) Habitat-specific density and diet of rapidly expanding invasive red lionfish, Pterois volitans, populations in the Northern Gulf of Mexico. PLoS ONE 9(8): e105852.

Dahl, K.A., Patterson III, W.F., Robertson, A., Ortmann, A.C. (2017) DNA barcoding significantly improves resolution of invasive lionfish diet in the Northern Gulf of Mexico. Biological Invasions 19(6): 1917-1933.

DeCelles, G.R., Martins, D., Zemeckis, D.R., Cadrin, S.X. (2017) Using fishermen’s ecological knowledge to map Atlantic cod spawning grounds on Georges Bank. ICES Journal of Marine Science 74(6): 1587-1601. del Carmen García-Rivas, M., Machkour-M’Rabet, S., Pérez-Lachaud, G., Schmitter-Soto, J.J., Céréghino, R., Doneys, C., St-Jean, N., Hénaut, Y. (2018) Age-dependent strategies related to lionfish activities in the Mexican Caribbean.

Environmental Biology of Fishes 101(4): 563-578.

Didham, R.K., Tylianakis, J.M., Hutchison, M.A., Ewers, R.M., Gemmell, N.J. (2005) Are invasive species the drivers of ecological change?. Trends in Ecology & Evolution 20(9): 470-474.

European Commission (2014) Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Official Journal of European Union 317: 35-55.

29

European Commission (2016) Commission Implementing Regulation (EU) 2016/1141 of 13 July 2016 adopting a list of invasive alien species of Union concern pursuant to Regulation (EU) No 1143/2014 of the European Parliament and of the Council. Official Journal of European Union 189: 4-8.

European Commission (2016) Commission Implementing Regulation (EU) 2016/145 of 4 February 2016 adopting the format of the document serving as evidence for the permit issued by the competent authorities of Member States allowing establishments to carry out certain activities concerning invasive alien species of Union concern pursuant to Regulation (EU) No 1143/2014 of the European Parliament and of the Council. Official Journal of European Union 30: 1-6.

European Commission (2017) Commission Implementing Regulation (EU) 2017/1263 of 12 July 2017 updating the list of invasive alien species of Union concern established by Implementing Regulation (EU) 2016/1141 pursuant to Regulation (EU) No 1143/2014 of the European Parliament and of the Council.

Official Journal of European Union 182: 37-39.

European Commission (2017).Commission Implementing Regulation (EU) 2017/1454 of 10 August 2017 specifying the technical formats for reporting by the Member States pursuant to Regulation (EU) No 1143/2014 of the European Parliament and of the Council. Official Journal of European Union 208: 15-27.

Frazer, T.K., Jacoby, C.A., Edwards, M.A., Barry, S.C., Manfrino, C.M. (2012) Coping with the lionfish invasion: Can targeted removals yield beneficial effects? Reviews in Fisheries Science 20(4): 185-191.

Genovesi, P., Carboneras, C., VilĂ , M., Walton, P. (2015) EU adopts innovative legislation on invasive species: a step towards a global response to biological invasions? Biological Invasions 17(5): 1307-1311.

Giovos, I., Kletou, P., Paravas, P., Marmara, D., Romanidis-Kyriakidis, G., Poursanidis, D. (2018) Citizen scientists monitoring the establishment and expansion of Pterois miles (Bennett, 1828) in the Aegean Sea, Greece. Cahiers de Biologie Marine 59: 359-365.

Golani D., Sonin, O. (1992) New records of the Red Sea fishes, Pterois miles (Scorpaenidae) and Pteragogus pelycus (Labridae) from the eastern Mediterranean Sea. Japanese Journal of Ichthyology 39(2): 167-169.

Harms-Tuohy, C., Schizas, N.V., Appeldoorn, R.S. (2016) Use of DNA metabarcoding for stomach content analysis in the invasive lionfish Pterois volitans in Puerto Rico. Marine Ecology Progress Series 558: 181-191.

30

Hellenic Republic (2011) Law 3937/2011, on the conservation of biodiversity and other provisions. Hellenic Government Gazette vol. A no 60, 1619-1666.

Available at: http://www.et.gr/idocs-nph/search/pdfViewerForm.html? args=5C7QrtC22wFYAFdDx4L2G3dtvSoClrL8MFAMkmC8uPjtIl9LGdkF53U Ixsx942CdyqxSQYNuqAGCF0IfB9HI6qSYtMQEkEHLwnFqmgJSA5WIsluVnRwO1oKqSe4BlOTSpEWYhszF8P8UqWb_zFijBnq9npGcZXT0A7yxNzYzo X_qsoBKm6CJHMEnkEICVu7 (accessed 30 Oct. 2018).

Heyman, W.D., Granados-Dieseldorff, P. (2012) The voice of the fishermen of the Gulf of Honduras: Improving regional fisheries management through fisher participation. Fisheries Research 125-126: 129-148.

IUCN (2018) The IUCN Red List of Threatened Species. Version 2018-1. 〈www.iucnredlist.org〉 (accessed 18 Sept. 2018).

Jimenez, C., Andreou, V., Hadjioannou, L., Petrou, A., Abu Alhaija, R., Patsalou, P. (2017) Not everyone's cup of tea: Public perception of culling invasive lionfish in Cyprus. Journal of the Black Sea/Mediterranean Environment 23(1): 38-47.

Jimenez, C., Petrou, A., Andreou, V., Hadjioannou, L., Wolf, W., Koutsoloukas, N., Abu Alhaija, R. (2016) Veni, vidi, vici: The successful establishment of the lionfish Pterois miles in Cyprus (Levantine Sea). Rapp Comm int Mer Médit 41: 417.

Kampouris, T.E. (2018) Blue Growth as a tool for sustainable fisheries management of threatened fisheries resources. A case study of the spiny lobster fishery off Aegean Sea. 9th International Black Sea Symposium, Blue Growth as a driver for regional development. 20-21 March 2018 ICBSS, Athens, Greece.

Katsanevakis, S., Coll, M., Piroddi, C., Steenbeek, J., Lasram B.R.F., Zenetos, A., Cardoso, A.C. (2014) Invading the Mediterranean Sea: Biodiversity patterns shaped by human activities. Frontiers in Marine Science 1: 32.

Kletou, D., Hall-Spencer, J., Kleitou, P. (2016) A lionfish (Pterois miles) invasion has begun in the Mediterranean Sea. Marine Biodiversity Records 9: 1-7.

Layman, C.A., Allgeier, J.E. (2012) Characterizing trophic ecology of generalist consumers: A case study of the invasive lionfish in The Bahamas. Marine Ecology Progress Series 448: 131-141.

Mačić, V., Albano, P.G., Almpanidou, V., Claudet, J., Corrales, X., Essl, F., Evagelopoulos, A., Giovos, I., Jimenez, C., Kark, S., Marković, O., Mazaris, A.D., Ólafsdóttir, G.A., Panayotova, M., Petović, S., Rabitsch, W., Ramdani, M., Rilov, G., Tricarico, E., Fernández, T.V., Sini, M., Trygonis, V. Katsanevakis, S.

31

(2018) Biological invasions in conservation planning: A global systematic review. Frontiers in Marine Science 5: 178.

Mitsou, E., Maximiadi, M. (2018) New records of Lagocephalus sceleratus (Gmelin, 1789), Cassiopea andromeda (Forsskål, 1775) and Pterois miles (Bennett, 1828) in Greek MSFD areas. Mediterranean Marine Science (in press).

Morris Jr, J.A., Akins, J.L. (2009) Feeding ecology of invasive lionfish (Pterois volitans) in the Bahamian archipelago. Environmental Biology of Fishes 86(3): 389-398.

Mumby, P.J., Hardborne, A.R., Brumbaugh, D.R. (2011) Grouper as a natural biocontrol of invasive lionfish. PLoS ONE 6(6): e21510.

Nuñez, M.A., Kuebbing, S., Dimarco, R.D., Simberloff, D. (2012) Invasive Species: to eat or not to eat, that is the question. Conservation Letters 5: 334-341. Özgür Özbek, E., Mavruk, S., Saygu, I., Oztürk, B. (2017) Lionfish distribution in the eastern Mediterranean coast of Turkey. Journal of Black Sea/Mediterranean Environment 23(1): 1-16.

Peake, J., Bogdanoff, A.K., Layman, C.A., Castillo, B., Reale-Munroe, K., Chapman, J., Dahl, K., Patterson III, W.F., Eddy, C., Ellis, R.D., Faletti, M., Higgs, N., Johnston, M.A., Muñoz, R.C., Sandel, V., Villasenor-Derbez, J.C., Morris Jr, J.A. (2018) Feeding ecology of invasive lionfish (Pterois volitans and Pterois miles) in the temperate and tropical western Atlantic. Biological Invasions 20(9): 2567-2597.

Pimentel, D., Zuniga, R., Morrsion, D. (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States.

Ecological Economics 52: 273-288.

Pimiento, C., Monaco, E., Barbour, A.B., Siliman, B.R. (2013) Predation on the speared lionfish, Pterois volitans, by spotted moray, Gymnothorax moringa.

Florida Scientist 76(3-4): 391-394.

Poursanidis, D., Marakis, P. (2016) Range expansion of the lionfish in Karpathos Island. In: New Mediterranean biodiversity records (C. Mytilineou, E. Akel, N. Babali et al.). Mediterranean Marine Science 17(3): 794-821 doi: 10.12681/mms.1976.

Rocha, L.A., Rocha, C.R., Baldwin, C.C., Weigt, L.A., McField, M. (2015) Invasive lionfish preying on critically endangered reef fish. Coral Reefs 34(3): 803-806.

32

Roy, H.E., Adriaens, T., Aldridge, D.C., Bacher, S., Bishop, J.D.D., Blackburn, T.M., Branquart, E., Brodie, J., Carboneras, C., Cook, E.J., Copp, G.H., Dean, H.J., Eilenberg, J., Essl, F., Gallardo, B., Garcia, M., García-Berthou, E., Genovesi, P., Hulme, P.E., Kenis, M., Kerckhof, F., Kettunen, M., Minchin, D., Nentwig, W., Nieto, A., Pergl, J., Pescott, O., Peyton, J., Preda, C., Rabitsch, W., Roques, A., Rorke, S., Scalera, R., Schindler, S., Schönrogge, K., Sewell, J., Solarz, W., Stewart, A., Tricarico, E., Vanderhoeven, S., van der Velde, G., Vilà, M., Wood, C.A., Zenetos, A. (2015) Invasive Alien Species - Prioritising prevention efforts through horizon scanning ENV.B.2/ETU/2014/0016. European Commission.

Sandel, V., Martínez-Fernández, D., Wangpraseurt, D., Sierra, L. (2015) Ecology and management of the invasive lionfish Pterois volitans/miles complex (Perciformes: Scorpaenidae) in southern Costa Rica. Revista de Biología Tropical 63(1): 213-221.

Sharp, R.L., Larson, L.R., Green, G.T. (2011) Factors influencing public preferences for invasive alien species management. Biological Conservation 144(8): 2097-2104 doi: 10.1016/j.biocon.2011.04.032.

Sterioti, A. (2016) First record of Pterois miles from Kriti, Greece. In: New Mediterranean biodiversity records (T. Dailianis, O. Akyol, N. Babali et al.).

Mediterranean Marine Science 17(2): 608-626.

Turan, C., Ergüden, D., Gürlek, M., Yağlıoğlu, D., Uyan, A., Uygur, N. (2014) First record of the Indo-Pacific lionfish Pterois miles (Bennett, 1828) (Osteichthyes: Scorpaenidae) for the Turkish marine waters. Journal of Black Sea/Mediterranean Environment 20(2): 158-164.

Turan, C., Öztürk, B. (2015) First record of the lionfish Pterois miles (Bennett 1828) from the Aegean Sea. Journal of Black Sea/Mediterranean Environment 21(3): 334˗368.

Turan, C., Uygur., N, İğde, M. (2017) Lionfishes Pterois miles and Pterois volitans in the North-eastern Mediterranean Sea: Distribution, habitation, predation and predators. Natural and Engineering Sciences 2(1): 35-43.

Union for the Mediterranean (UfM) (2017). Blue Economy in the Mediterranean.

Valdez-Moreno, M., Quintal-Lizama, C., Gómez-Lozano, R., del Carmen GarcíaRivas, M. (2012) Monitoring an alien invasion: DNA barcoding and the identification of lionfish and their prey on coral reefs of the Mexican Caribbean.

PLoS ONE 7(6): e36636

33

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

What is the roar about? Lionfish targeted removals in Costa Rica (Central America) and Cyprus (Mediterranean Sea) Carlos JIMÉNEZ1*, Burak Ali ÇIÇEK2, José Ugalde JIMÉNEZ3, Louis HADJIOANNOU1, Mehmet Fatih HUSEYINOGLU4 1 Enalia Physis Environmental Research Centre (ENALIA), Acropoleos St. 2, Aglanjia 101, Nicosia; CYPRUS 2 Society of Nature and Culture, TEKNOPARK, No. 6, Famagusta, CYPRUS 3 Asociación de Pescadores Artesanales del Caribe Sur (APACS), Puerto Viejo, Limón; COSTA RICA 4 Biosphere Research Center, Istanbul, TURKEY *Corresponding

author: c.jimenez@enaliaphysis.org.cy

Introduction The management of invasive and native species with increasing populations is a topic of great concern in conservation ecology with multi-pronged complications.

Knowledge on the invasive species biogeography, biology and ecological impacts need to be generated and publicized in order to assist in the prioritization of resources and actions. Difficult decisions need to be taken at given stages of the population trajectory of invasive species that present difficult situations. For example, which are the options managers will have when confronting an invasion that is already beyond the point where eradication is possible? Experience shows that managers reaction might be the result of their cultural background, evaluation of available information on technological options and on the species’ impacts (e.g. ecological), and engagement with the public (Thresher and Kuris 2004; Humair et al. 2014; Kuebbing and Simberloff 2015 Van der Wal et al. 2015; Crowley et al. 2017a).

Notwithstanding the best alternative in the decision-making process, management of invasive species, native or not (Simberloff et al. 2012; Wilson et al. 2016; Larson et al. 2017; Rejmánek and Simberloff 2017), is controversial to the bone.

Recently, the very essence of invasive ecology is “emotionally” contested and manager decision-criteria and final responses to invasives criticized as well (e.g.

Davis et al. 2011; Schlaepfer et al. 2011; Vince 2011; Simberloff et al. 2012; Gozlan et al. 2013; Shackelford et al. 2013; Hill and Hadly 2018), although with mixed results (Humair et al. 2014; Kuebbing and Simberloff 2015; Van der Wal et al. 2015). Delays in important decisions regarding the line of action to confront expanding invasive species might render late-actions impractical or ineffective.

On this already conflictive scenario, removal of invasive species, as an action for maintenance management to keep population numbers low, is another source of contention (Simberloff et al. 2012, 2013; Simberloff 2013; Crowley et al. 2017b).

34

In spite of that, there is public support and participation for some removal actions, for example of the cane toad (Australia) or the Burmese python (Florida), indicating the general perception regarding invasive species, perception that nonetheless can be conflictive. However, public perception and thus, support for these activities changes and may stop entirely (Fortwangler 2013; Gozlan et al.

2013; Simberloff et al. 2013; Carballo-Cárdenas and Tobi 2016; Crowley et al.

2017b, 2018).

Lionfish removal events started in the Caribbean less than ten years ago (Barbour et al. 2011; Biggs and Olden 2011; Akins 2012; Frazer et al. 2012; Albins and Hixon 2013) and despite of questioning from diverse stakeholders and debate about the benefits and costs (Frazer et al. 2012; Carballo-Cárdenas 2015; Carballo-Cárdenas and Tobi 2016), they are today popular activities among the general public and one of the actions discussed in maintenance management schemes (e.g. Malpica-Cruz et al. 2016; Green et al. 2017). Like other planned removal of dangerous and venomous fish species (e.g. Kwik 2012), public health aspects as well as lessening ecological impacts are among the main arguments to put forward lionfish removal events. Comparing two removal events that took place in 2018 in manifestly distinct social and ecological contexts, tropical Costa Rica and subtropical Cyprus, this study aimed to describe the lessons learned in the 6-yr experience of removal event organization in Costa Rica, and discuss possible adaptations of that knowledge to the recent effort in Cyprus to organize further public removals of lionfish.

Materials and Methods Study sites Costa Rica The southern Caribbean coast of Costa Rica (Figure 1a) has numerous important habitats, such as coral reefs (e.g. fringing, patch and banks), seagrass meadows (Thalassia testudinum), coastal lagoons and mangroves. The study site with the removal activities is the Gandoca-Manzanillo Wildlife Refuge (Spanish acronym REGAMA), which has 4,436 hectares of marine protected areas. These very diverse ecosystems, already under stress due to poor land-management (e.g. agriculture; Cortés et al. 2010), got bad news about ten years ago. A few solitary lionfish, an unwelcomed guest already infamous in the Caribbean region, were first noticed by local fishermen in 2008 in shallow coral reefs within the REGAMA (Molina-Ureña 2009). In May 2009, while working with local divers in other reefs of the area and offshore coral banks (e.g. Longshoal in Puerto Viejo), lionfish juveniles and adults were found by one of us (C.J.) down to a depth of -30m. The first specimen was officially collected for the Museum of Comparative Zoology of the University of Costa Rica. During the next weeks and months, lionfish were spotted in even more areas along the coast and since then, it has established in almost all coral habitats of the region (Sandel et al. 2015;

35

Suárez 2016) reaching mean densities of about 92±130 fish/ha (mean±SD; Sandel et al. 2015).

Cyprus Famagusta Bay at the eastern coast of Cyprus (Figure 1b) is a large bay with extensive seagrass meadows (Posidonia oceanica), hard and softbottom habitats, and numerous submerged rocky outcrops that extend to a depth of -45m and more.

The seagrass meadows in the bay have been confirmed as important foraging grounds for marine turtles in Cyprus (Snape 2015). The first confirmed reports of lionfish in Cyprus were in Winter 2012/2013 (Jimenez et al. 2016). Few juveniles were found at -35m depth. It was during the subsequent months that observations increased from diverse locations and started to appear in the social networks (Evripidou 2013, Kletou et al. 2016). By 2015, lionfish was well stablished around the island including Famagusta Bay (Jimenez et al. 2016) and started to be a usual sight for divers and in the fishermen catch using nets, traps, and even in anglers’ rods. However, unconfirmed reports might bring earlier the date for the onset of the lionfish spreading and establishment in Cyprus. An underwater photographer found one small individual in 2011 and the photo was included in a temporal exhibition that year (G. Payiatas, comm. pers. 2017). On another instance, a seasoned recreational fisherman recalled how in 2011 a relative who was net-fishing with him near Famagusta Bay, was painfully stung by a strange and “colourful” fish never seen before by them. The fish was immediately recognized when they were shown a photograph of a recently-dead lionfish in 2017. All in all lionfish in Cyprus is today wide-spread in shallow and deephabitats (-40 to -150m depth; Jimenez et al. submitted), reaching high mean densities of about 351±333 fish/ha (0.04±0.03 fish/m2; mean±SD) that fluctuate seasonally and according to depth (Jimenez in prep.).

Targeted removal events Periodical removals of lionfish, barridas in Spanish, started in Costa Rica in 2012 as an initiative of the recently created Association of Artisanal fishing folk of the Southern Caribbean Coast (Spanish name Asociación de Pescadores Artesanales del Caribe Sur). The Association has an extensive program with actions to study and tackle different aspects of the lionfish invasion. These actions include public awareness campaigns, periodical removals in different reefs of the coast, the popular tournament held once a year, and the remarkably effective program to deploy traps, nasas in Spanish, to catch lionfish at depths beyond the removal event depth limit. Research by the association on the biology of the species utilize samples and observations gathered during the periodical barridas, which are performed by experienced divers and fishermen and financed by the private sector. Since its humble beginning in 2012 (only three freedivers in the fringing reef of Pta. Uva, inside the REGAMA), the tournament grew in popularity and outreach and now sports an average attendance of about 500 or more visitors and it is held always in Manzanillo (inside the REGAMA). In one recent event, local competitors shared the experience with participants from Greece, Italy, United 36

States of America, Venezuela, Panama, Spain, Cuba and Nicaragua. The first tournament to remove lionfish in Cyprus was held in June 10, 2018 and it was organized by a local Hunting Association. This Association also arranges yearly removals of another invasive fish species, the silver-cheeked toadfish (Lagochephalus sceleratus). In this study we concentrate on the comparison of the Costa Rican tournament in October 2018 with the event celebrated in Cyprus.

Figure 1. Study sites in the Gandoca-Manzanillo Wildlife Refuge (Spanish acronym REGAMA), Caribbean coast of Costa Rica (a) and Famagusta Bay in Cyprus, Mediterranean Levantine Sea (b). Circles indicate locations where lionfish populations are established (Jimenez et al. 2016; in prep.)

Results The Costa Rican tournament of 13-14 October 2018 had a participation of 50 free divers and 50 scuba divers. Figure 2 shows the evolution of the participation per category in this tournament since its inception in 2012. Since 2016, hundred participants are considered the maximum capacity that the organization can handle because all costs are covered by the Association. For example, participants are given t-shirts, gear to remove lionfish (pole spear and containers), and every team is provided with a boat with fuel and a captain. The participants in the tournament in Cyprus listed their teams in two categories (1 team scuba diving, 13 freediving) with a total of 49 competitors (Figure 2).

37

Figure 2. Number of participants in the tournaments to remove lionfish in Costa Rica (Pta. Uva 2012/2013, Manzanillo 2014-2018) and in Cyprus (Famagusta 2018) according to category (scuba or freediving). Total of participants for that yearâ&#x20AC;&#x2122;s event is given in blue

In general, freediving is the category that brings in more lionfish in Costa Rica and in Cyprus (Figure 3). The 2018 catch of this category in Costa Rica was for the first time lower than what is usually caught by scuba divers. The Costa Rican tournament of 2017 also stands alone since the catch for that year was the lowest for any event and category since the beginning of the activity in 2012 (Figure 3).

In comparison, the total catch of lionfish during the first tournament in Cyprus (315 lionfish) was about double of the highest catch ever in Costa Rica (153 lionfish in 2014).

Figure 3. Number of lionfish removed in the tournaments in Costa Rica (Pta. Uva 2012/2013, Manzanillo 2014-2018) and in Cyprus (Famagusta 2018) according to category (scuba or freediving). Total of lionfish for that yearâ&#x20AC;&#x2122;s event is given in blue

38

As mentioned before, during the removal event in Costa Rica, there are various land-based activities for all participants (Figure 4a) including the visitors that are not competing in the removals. Talks were given in which the most remarkable aspects of the lionfish biology and ecology are summarized and illustrated with fresh samples product of the removal event (Figure 4b). There where stands to demonstrate how to prepare and cook lionfish and different recipes where prepared for the attendants to degust. These activities continued during the second day when the category scuba competed (Figure 4c) and culminated in the afternoon when the prizes were given to the winning teams in each category (Figure 4d).

Prize-wining categories were different between the two tournaments. Three categories are usually evaluated in Costa Rica: smallest and largest-sized lionfish, and the most lionfish caught by any team. In Cyprus only one category was considered in the 2018 tournament, the heaviest catch of lionfish brought in by any team. The prizing was also different between the two competitions; trophies in Costa Rica, and trophies and cash in Cyprus.

Figure 4. Some of the competitors during the first day (category freediving) of the lionfish removal tournament held in Manzanillo, Costa Rica (13-14 October 2018) (a); participantsâ&#x20AC;&#x2122; experience in the sea and spearfishing varies significantly. Competitors and visitors of the tournament are given talks by staff members of the Association on the general biology and ecology of Pterois spp. (b). During the second day of the tournament the divers of the category scuba remove lionfish down to a depth of -25m (c). Prizewinning team (category freediving) of local fishermen and divers (d). All photographs by ASOPACS.

39

The activities associated to the removal event in Cyprus consisted of an early morning inscription of participants followed by the initiation of the event with both categories (scuba and freediving) happening at the same time, although at different locations and distance from the coast. While the scuba diving team (Figure 5a) removed lionfish at two popular dive sites in Famagusta Bay, 1.7 miles offshore (-35 to -40m depth), freedivers searched for lionfish at various sites along a stretch of coast of about 8km (-10 to -25m depth). Three hours after initiation of the event, the competitors and visitors gathered at the weighing point and the lionfish catch brought in by each team was inspected and weighted by the judges (Figure 5b). In total, over 300 medium to large-sized specimens were removed from the sea on that day (Figure 3). Interestingly, only 3 females were found in a sample of 11 specimens (30-37.1cm total length; 390-885gr fresh weight) from this catch.

The prizes by category (Figure 5c) where given at a local restaurant and competitors and visitors to the event were given to taste lionfish dishes (Figure 5d) prepared following a traditional Cypriot recipe for fish (particularly scorpionfish; Jimenez in prep.).

Figure 5. Some of the participants (category scuba) in the 1-day removal event held in Famagusta Bay, Cyprus (June 2018); some of them participate in research activities about the lionfish and are familiar with the sea and spearfishing (a). Partial catch of medium/large-sized lionfish while is inspected and weighted by the organizers of the event (b). Prize-winning team (category freediving) (c). Most of the catch of the tournament was given to a local restaurant where it was cooked and given to the participants and guests (d). All photographs by C. Jimenez.

40

No accidents were reported in the 2018 event in Costa Rica. Since 2012, only one accident occurred in 2017 and it was due to the improper manipulation of the lionfish by a member of the jury. During the Famagusta 2018 event, three freedivers got stung on the hands and abdomen while handling the fish underwater. On-site first aid treatment was promptly administrated in the form of warm-water compresses followed by a visit to the hospital only if the pain did not recede. Treatment at the hospital consisted of more warm-water treatment and painkillers that effectively decreased the pain. Other divers and fishermen that had the misfortune of being stung by lionfish in Cyprus since 2012 were not that lucky to receive the proper treatment in the hospitals; this is mostly due to medical staff being not familiar with lionfish envenomation (Jimenez et al. in prep.).

Policing the removal events in Costa Rica in order to avoid illegal extraction of fish species other than lionfish is done by a signed agreement with the participants. In this document, participants commit themselves to follow the rules of the event (given in a separate document publicized broadly), specifically the restriction to catch only lionfish. Another control to ensure the agreement is respected is by having designated captains on the embarkations transporting participants. The captains are members or close collaborators of the Association.

By preventing the illegal spearfishing of fish species other than lionfish, this approach allows to perform removals within the protected area of REGAMA. In Cyprus, the organizers inspected the embarkations participating in the event by using a high-powered boat and had constant contact by mobile telephones with the embarkations.

Discussion and Conclusions The present study sought to show the particularities of invasive lionfish removal events or tournaments taking place at two distant and remarkably different localities. In addition to the obvious sociocultural differences between tropical, Caribbean Costa Rica and subtropical Cyprus, the marine environment and the history of the lionfish invasion are distinct. However, contrasting the removal events in both countries facilitates to identify diverse aspects that Cyprus, the most recently invaded area and with only one removal event to date, could benefit by adapting those that are relevant to its local conditions. Most importantly, to learn from the six yearsâ&#x20AC;&#x2122; experience in Costa Rica on how to define realistic maintenance management goals that can be achieved with public participation in activities such as the removal events and with parallel removals performed by trained staff.

Motivation to engage in these maintenance management activities varies substantially between stakeholders, geographical location, the species itself, and the evolution of the public and manager perception on the need to sustain removals of lionfish - or any other invasive species (Simberloff 2013, 2014; 41

Carballo-Cárdenas 2015; Carballo-Cárdenas and Tobi 2016; Crowley et al.

2017a; Green et al. 2017). Costa Rica and Cyprus have experienced the initial awe produced by the rapid establishment of Pterois spp. and, to a degree, various form of scepticism and reticence to culling (e.g. Suárez 2016; Jimenez et al.

2017). However, stakeholder perception changes and support for activities to remove lionfish is currently more accepted in both countries (Fendt 2015; Sandel et al. 2015; Jimenez in prep.; Kleitou et al. submitted). The time to change the general perception and to accept and implement removals as part of the maintenance management options was relatively short in Costa Rica (less than two years since the first reports in mid-2009). This was mostly due to the country’s long trajectory dealing with environmental issues, the quick reaction by the academia informing authorities and general public, interest from managers on the issue, and because the Caribbean has already background information and experience on the removal of lionfish. Information is available as published reports, scientific contributions as well as National Plans to tackle Pterois spp. ecological impacts. Noteworthy is the fact that the first removal events in Caribbean Costa Rica were performed, unofficially, by the private sector as early as 2010, only a few months after the first reports of lionfish in the country were made public and when the general perception on culling was still not clear. These independent removals were stopped soon after due to uncertain legislation on this matter (Sandel et al. 2015).

Clearly, there are aspects of the Costa Rican experience in removing lionfish throughout organized tournaments that the Cypriot case could benefit. Periodical removals by trained and experienced staff from the Association and tournaments with the participation of stakeholders of diverse backgrounds and ages are two different activities, although complementary, that have specific goals. Intrinsic social aspects need to be considered in the planning of these two management actions as well as the impacts (effectiveness) on the lionfish populations and the environment in general. Periodical removals or Barridas are more efficient in removing lionfish than the popular tournaments; experience and training are major factors here (see below). However, tournaments are better activities or platforms to educate the general public, which during the 2-day event participate in educational activities (e.g. cooking of lionfish) and talks held under a festive atmosphere. This explain partially the popularity, high attendance and interest the tournaments exert in the general public. The awareness of being part of an action (i.e. first-hand experience) to tackle an environmental/ecological problem frequently creates an organic and positive response from managers and the public interested in these topics (e.g. Kuebbing and Simberloff 2015; Buhrmester et al.

2018) but can also be the source of intense conflicts (Simberloff 2013; Crowley et al. 2017b, 2018). But beyond any reasonable doubt, the removal of the infamous lionfish, an otherwise stunning fish species, is a thrill that the participants experience and, in consequence, is a recurrent reason given to participate (Jimenez et al. 2017; in prep.). Carefully planned educational activities of wide outreach, which were mentioned before, aim to educate and lessen 42

potential conflicts between stakeholders with different perspectives or values (Crowley et al. 2017b).

The necessity to have both activities, the tournaments and the periodical removals, led to include in Costa Rica the private sector in the process. This sector provides the means to perform frequent-enough removals and along significant sections of the coast in order to make a significant effect in the lionfish populations. Important as well was the implementation of a monitoring program for the evaluation of the effectiveness of removals but also for the study of the recolonization processes. Managers, academics and staff of the Association all participate in the long-term analysis of the data. For example, as observed in other parts of the invaded areas in the Caribbean, Gulf of Mexico and Western Atlantic (Côté and Smith 2018; Harms-Tuohy et al. 2018 and references therein), the effectiveness of tournaments and between removals differ among sites in the REGAMA (Sandel et al. 2015), suggesting that there are still many aspects of the invasion story that need to be elucidated before we could predict the impact of removal events (Green et al. 2017; Côté and Smith 2018). In addition to these studies, monitoring of the participants is needed; not often the participants’ performance is placed into context to explain the removal success in terms of catch. The number of participants, their experience, commitment, fitness, knowledge of the seascape where culling is performed and of the lionfish ecology, are all factors that influence removals (e.g. Anderson et al. 2017; Green et al.

2017; Usseglio et al. 2017) and might account for the observed differences in the lionfish catch between years (Costa Rica) and study sites (Costa Rica vs. Cyprus).

Other factors also play a role in explaining differences of removal efficiency, particularly the temporal variability in the lionfish populations (demography), behavioural traits, environmental conditions, habitat and native faunal characteristics (Green et al. 2014; Côté et al. 2014; Usseglio et al. 2017; Côté and Smith 2018; Harms-Tuohy et al. 2018). One factor to consider here is the prizewinning categories. More often than not these categories are disregarded and weigh of catch is the chief criteria. However, the experience has demonstrated that to be effective, tournaments prize-wining categories should include the smaller and larger lionfish, and the largest catch brought in by any team. The first experience in Cyprus only prized the largest weight of the catch.

Local knowledge is necessary to screen within participants in the removal activities in order to adequately evaluate effectiveness. Costa Rican tournaments are popular locally and internationally and participants have, inevitably, multiple backgrounds and their knowledge of the sea varies significantly. For example, participants based far from the coast as well as those with sporadic or at least infrequent visits to the sea, are usually not well acquainted with the seascape and how to find and effectively catch lionfish. Training of this type of participants before the removal event is impractical. The efforts should be concentrated in the between removals performed by recurrent volunteers of staff whose ability can be better monitored and improved as well as the efficiency in producing data 43

necessary for the studies. On the other hand, training in the form of briefings on how to handle the fish underwater and providing the proper containers for the catch will minimize the risk of participants in the tournaments of being stung.

This type of accident that happens underwater is one of the most common in Cyprus when divers try to remove the lionfish from the spear-pole or the speargun (Jimenez in prep.).

In Cyprus, the 2018 event had participants with experience in spearfishing (including pole-spears) and were familiar with the areas. However, these may not be the only reasons for the high catch brought in by the teams. It seems that the lionfish invasion in Cyprus hasn’t levelled off yet; its populations are currently increasing attaining high densities even in small areas (Jimenez in prep.), reducing thus the time spent by divers searching for the fish. This is particularly true for those divers with knowledge of habitats where the lionfish can be found (e.g. Green et al. 2017). However, spending more time handling the catch when lionfish is found in great densities might slow-down the diver (Usseglio et al.

2017). Important to note is that even though population of other invasive species are known to have increased and stabilized/declined (Simberloff and Gibbons 2004; Simberloff 2013), there is only one example, to the best of our knowledge, for the decrease of lionfish abundance in a few areas of Bahamas without maintenance management removals (Benkwitt et al. 2017). To sit and wait (no action) with the expectation that the invasion will wear-off (see Thresher and Kuris 2004) is detrimental for the native species communities and involves a high risk since there is no guarantee that the lionfish populations are going to decline neither knowledge of when will that happen. To reduce lionfish populations to levels that their ecological impacts are lessened (at least on a local scale) is the best we can do (Simberloff 2014; Green et al. 2014, 2017; Benkwitt et al. 2017) and might be considered a form of temporal eradication.

There is a new initiative in Cyprus to have periodic removal events at different parts of the coast together with activities to raise public awareness. The RELIONMED-Life project (http://relionmed.eu/) started in 2017 and until 2021, will organize removal events and tournaments; the former will be conducted 25 times within two years whereas the latter with a 3-mo frequency for two years.

But if the experience gained in experimental maintenance management from other invaded areas could be applied in the Mediterranean (Levantine Sea), removals to be ecologically effective need to be very frequent (monthly), very effective (high catches), spatially dispersed along the coast (scale of kilometres, including Marine Protected Areas), performed at various depths (beyond recreational scuba and freediving depth limit), and sustained for long periods of time (years) (Barbour et al. 2011; Green et al. 2014, 2017; Johnston and Purkis 2015; Suárez 2016; Andradi-Brown et al. 2017a, b; Usseglio et al. 2017; Côté and Smith 2018; Giakoumi et al. 2018; Harms-Tuohy et al. 2018; Jimenez et al. submitted). Other initiatives and projects will be launched to study and tackle the invasion of the lionfish in the new invaded areas of the Mediterranean and elsewhere across the 44

Atlantic Sea. These efforts should continue and not being impaired by the growing denialism on invasive species (see Ricciardi and Ryan 2018). No-action or “let nature take its course” is a high-risk decision with likely dire consequences for the environment. Maintenance management in the form of removals is a pragmatic and realistic alternative to inaction and is endorsed by various national plans in the invaded areas (Graham et al. 2017). It is highly recommended to managers to continue supporting and engaging in tournaments and periodical removals or barridas that lessen the ecological effects of the lionfish invasion.

Acknowledgements The research has been partially funded in Cyprus by Enalia Physis Environmental Research Centre research program, Nephila Works Ltd., the Stelios Bi-communal 2017 awards (grantees L.H. and B.A.C.), Deep Dive Diving Centre, and Mr. Nick Galea. We acknowledge in Costa Rica the contributions of the Interamerican Foundation (IAF), GEF Small Grants Programme UNDP (project COS/SGP/FSP/OP5/Y3/BD/13/104), the support and advice from the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR)Universidad de Costa Rica, and the staff and die-hard collaborators of the Asociación de Pescadores Artesanales del Caribe Sur.

References Akins, J.L. (2012) Control Strategies: Tools and Techniques for Local Control.

In: Invasive Lionfish: A Guide to Control and Management. (ed., Morris J.A.J.) Gulf and Caribbean Fisheries Institute Special Publication Series. Marathon, USA, 1: 24-47.

Albins, M.A., Hixon, M.A. (2013) Worst case scenario: potential long-term effects of invasive predatory lionfish (Pterois volitans) on Atlantic and Caribbean coral-reef communities. Environ Biol Fishes 96: 1151-1157.

Anderson, L.G., Chapman, J.K., Escontrela, D., Gough, C.L.A (2017) The role of conservation volunteers in the detection, monitoring and management of invasive alien lionfish. Manage. Biol Invasions 8: 589-598.

Andradi-Brown, D.A., Grey, R., Hendrix A., Hitchner, D., Hunt, C.L., Gress, E., Madej, K., Parry, R.L., Regnier-McKellar, C., Jones, O.P., Arteaga, M., Izaguirre, A.P., Rogers, A.D., Exton, D.A.(2017a) Depth-dependent effects of culling – do mesophotic lionfish populations undermine current management? R Soc open sci 4: 170027 doi: 10.1098/rsos. 170027.

Andradi-Brown, D.A., Vermeij, M.J.A., Slattery, M., Lesser, M., Bejarano, I., Appeldoorn, R., Goodbody-Gringley, G., Chequer, A.D., Pitt, J.M., Eddy, C., Smith, S.R., Brokovich, E., Pinheiro, H.T., Jessup, M.E., Shepherd, B., Rocha, L.A., Curtis-Quick, J., Eyal, G., Noyes, T.J., Rogers, A.D., Exton, D.A. (2017b) 45

Large-scale invasion of western Atlantic mesophotic reefs by lionfish potentially undermines culling-based management. Biol Invasions 19: 939-954.

Barbour, A.B., Allen, M.S., Frazer, T.K., Sherman, K.D. (2011) Evaluating the potential efficacy of invasive lionfish (Pterois volitans) removals. PLoS One 6: e19666.

Benkwitt, C.E., Albins, M.A., Buch, K.L., Ingeman, K.E., Kindinger, T.L., Pusack, T.J.K., Stallings, C.D., Hixon, M.A. (2017) Is the lionfish invasion waning? Evidence from the Bahamas. Coral Reefs 36: 1255-1261.

Biggs, C.R., Olden, J.D. (2011) Multi-scale habitat occupancy of invasive lionfish (Pterois volitans) in coral reef environments of Roatan, Honduras. Aquat Invasions 6: 347-353.

Buhrmester, M.D., Burnham, D., Johnson, D.D.P., Curry, O.S., Macdonald, D.W., Whitehouse, H. (2018) How moments become movements: Shared outrage, group cohesion, and the lion that went viral. Front Ecol Evol 6: 54 doi: 10.3389/fevo.2018.00054.

Carballo-Cárdenas, E.C. (2015) Controversies and consensus on the lionfish invasion in the Western Atlantic Ocean. Ecol Society 20: 1-24.

Carballo-Cárdenas, E.C., Tobi, H. (2016) Citizen science regarding invasive lionfish in Dutch Caribbean MPAs: Drivers and barriers to participation. Ocean Coast Manag 133: 114-127.

Côté, I.M., Darling, E.S., Malpica-Cruz, L., Smith, N.S., Green, S.J., CurtisQuick, J., Layman, C. (2014) What doesn't kill you makes you wary? Effect of repeated culling on the behaviour of an invasive predator. PLoS One 9: e94248.

Côté, I.M., Smith, N. (2018) The lionfish Pterois sp. invasion: Has the worst-case scenario come to pass? Re-evaluating the lionfish invasion. J Fish Biol 92: 660689.

Cortés, J., Jimenez, C., Fonseca, A., Alvarado, J. (2010) Status and conservation of coral reefs in Costa Rica. Int J Trop Biol 58 (Suppl. 1): 33-50.

Crowley, S.L., Hinchliffe, S., McDonald, R.A., Lee, T.M. (2017a) Invasive species management will benefit from social impact assessment. J Appl Ecol 54: 351-357.

Crowley, S.L., Hinchliffe, S., McDonald, R.A. (2017b) Conflict in invasive species management. Frontiers Ecol Environ 15(3): 133-141.

46

Crowley, S.L., Hinchliffe, S., McDonald, R.A. (2018) The parakeet protectors: Understanding opposition to introduced species management. J Environ Manage (in press) doi: 10.1016/j.jenvman.2017.11.036.

Evripidou, S., (2013) Toxic Lionfish makes its way to Cyprus waters. https://www.thefreelibrary.com/Toxic+lionfish+makes+its+way+to+Cyprus+wa ters.-a0319558097.

Davis, M.A., Chew, M.K., Hobbs, R.J., Lugo, A.E., Ewel, J.J., Vermeij, G.J., Brown, J.H., Rosenzweig, M.L., Gardener, M.R., Carroll, S.P., Thompson, K., Pickett, S.T.A, Stromberg, J.C., Del Tredici, P., Suding, K.N., Ehrenfeld, J.G., Grime, J.P., Mascaro, J., Briggs, J.C. (2011) Don't judge species on their origins.

Nature 474: 153-154.

Fendt, L. (2015) Counterattack: How one community fends off an unwanted fish.

Hakai Magazine. Available at https://www.hakaimagazine.com/videosvisuals/counterattack-how-one-community-fends-unwanted-fish/ (accessed 15 Oct. 2018).

Fortwangler, C. (2013) Untangling introduced and invasive animals. Environ Soc Adv Res 4: 41-59.

Frazer, T.K., Jacoby, C.A., Edwards, M.A., Barry, S.C., Manfrino, C.M. (2012) Coping with the lionfish invasion: Can targeted removals yield beneficial effects?

Rev. Fisheries Sci 20: 185-191.

Giakoumi, S., Pey, A., Di Franco, A., Francour, P., Kizilkaya, Z., Arda, Y., Raybaud, V., Guidetti, P. (2018) Exploring the relationships between marine protected areas and invasive fish in the world's most invaded sea. Ecol Appl (in press) doi: 10.1002/eap.1809.

Gozlan, R.E., Burnard, D., Andreou, D., Britton, J.R. (2013) Understanding the threats posed by non-native species: public vs. conservation managers. PLoS One 8: e53200.

Graham, R.E., Fanning, L.M. (2017) A comparison of eight country plans for the invasive Indo-Pacific lionfish in the wider Caribbean. Global Ecol Conserv 12: 253-262.

Green, S.J., Dulvy, N.K., Brooks, A.M., Akins, J.L., Cooper, A.B., Miller, S., Côté, I.M. (2014) Linking removal targets to the ecological effects of invaders: a predictive model and field test. Ecol Applications 24: 1311-1322.

Green, S.J., Underwood, E., Akins, J.L. (2017) Mobilizing volunteers to sustain local suppression of a global marine invasion. Conserv Lett 10: 726-735.

47

Harms-Tuohy, C.A., Appeldoorn, R.S., Craig, M.T. (2018) The effectiveness of small-scale lionfish removals as a management strategy: effort, impacts and the response of native prey and piscivores. Manag Biol Invasions 9(2): 149-162.

Hill, A.P., Hadly, E.A. (2018) Rethinking “Native” in the Anthropocene. Front Earth Sci 6: 96.

Humair, F., Edwards, P.J., Siegrist, M., Kueffer, C. (2014) Understanding misunderstandings in invasion science: why experts don’t agree on common concepts and risk assessments. NeoBiota 20: 1-30.

Jimenez, C., Andreou, V., Hadjioannou, L., Petrou, A., Abu Alhaija, R., Patsalou, P. (2017) Not everyone’s cup of tea: Public perception of culling invasive lionfish in Cyprus. J Black Sea/Mediterranean Environment 23: 38-47.

Jimenez, C., Petrou, A., Andreou, V., Hadjioannou, L., Wolf, W., Koutsoloukas, N., Abu Alhaija, R. (2016) Veni, vidi, vici: The successful establishment of the lionfish Pterois miles in Cyprus (Levantine Sea). Rapp Comm int Mer Médit 41: 417.

Johnston, M.W., Purkis, S.J. (2015) A coordinated and sustained international strategy is required to turn the tide on the Atlantic lionfish invasion. Mar Ecol Prog Ser 533: 219-235.

Kletou, D., Hall-Spencer, J.M., Kleitou, P. (2016) A lionfish (Pterois miles) invasion has begun in the Mediterranean Sea. Mar Biodiver Rec 9: 46 doi: 10.1186/s41200-016-0065-y.

Kuebbing, S.E., Simberloff, D. (2015) Missing the bandwagon: Nonnative species impacts still concern managers. NeoBiota 25: 73-86.

Kwik, J.T.B. (2012) Controlled culling of venomous marine fishes along Sentosa Island beaches: A case study of public safety management in the marine environment of Singapore. Raffles Bull Zool 25: 93-99.

Larson, B.M.H., Van Der Wal, R., Fischer, A., Selge, S. (2017) Origin might matter; people matter, too (a response to the comment by Rejmánek and Simberloff (2017)). Environ Conserv 44: 100-101.

Malpica-Cruz, L., Chaves, L.C.T., Côté, I.M. (2016). Managing marine invasive species through public participation: lionfish derbies as a case study. Marine Policy 74: 158-164.

Molina-Ureña, H. (2009). El pez león del Indo-Pacífico: Nueva especies invasora en Costa Rica. Revista Biocenosis 22: 21-30.

48

Rejmánek, M., Simberloff, D. (2017) Origin matters. Environ Conserv 44: 97-99.

Ricciardi, A., Ryan, R. (2018) The exponential growth of invasive species denialism. Biol Invasions 20: 549-553.

Sandel, V., Martínez-Fernández, D., Wangpraseurt, D., Sierra, L. (2015) Ecology and management of the invasive lionfish Pterois volitans/miles complex (Perciformes: Scorpaenidae) in Southern Costa Rica. Rev Biol Trop 63: 213-21.

Schlaepfer, M.A., Sax, D.F., Olden, J.D. (2011) The potential conservation value of non-native species. Conserv Biol 25: 428-437.

Shackelford, N., Hobbs, R.J., Heller, N.E., Hallett, L.M., Seastedt, T.R. (2013) Finding a middle-ground: the native/non-native debate. Biol Conserv 158: 55-62.

Simberloff, D. (2013) Invasive Species: What Everyone Needs to Know. Oxford University Press. 352 pp.

Simberloff, D. (2014) Biological invasions: What’s worth fighting and what can be won? Ecol Engineering 65: 112-121.

Simberloff, D., Gibbons, L. (2004) Now you see them, now you don’t! – population crashes of established introduced species. Biol Invasions 6: 161-172.

Simberloff, D., Martin, J.L., Genovesi, P., Maris, V., Wardle, D.A., Aronson, J., Courchamp, F., Galil, B., Garcia-Berthou, E., Pascal, M., Pysek, P., Sousa, R., Tabacchi, E., Vila, M. (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28: 58-66.

Simberloff, D., Souza, L., Nunez, M.A., Barrios-Garcia, M.N., Bunn, W. (2012) The natives are restless, but not often and mostly when disturbed. Ecology 93: 598-607.

Snape, R.T.E. (2015) Artisanal fishers help to map marine turtle distribution and bycatch: further evidence for an important foraging ground in Famagusta Bay, North Cyprus. Testudo 8: 51-59.

Suárez, M. (2016) Traditional Fishing Folk’s Knowledge on Costa Rica’s Southern Caribbean Coast: A Critical Component in a Formula for Lionfish Reduction. In Severing F.N.R., Weijer C., Echteld E., Rutgers W., Dupey R. (eds.) Celebrating Multiple Identities: Opting out of neolcolonialmonolinguism, monoculturalism and mono-identification in the Greater Caribbean. Willemstad, University of Curaçao and Fundashon pa Planifikashon di Idioma. pp. 391-407.

49

Thresher, R.E., Kuris, A.M. (2004) Options for managing invasive marine species. Biol Invasions 6: 295-300.

Usseglio, P., Selwyn, J.D., Downey-Wall, A.M., Hogan, J.D. (2017) Effectiveness of removals of the invasive lionfish: how many dives are needed to deplete a reef? PeerJ 5: e3043.

Van der Wal, R., Fischer, A., Selge, S., Larson, B.M.H. (2015) Neither the public nor experts judge species primarily on their origins. Environ Conserv 42: 349355.

Vince, G. (2011) Embracing invasives. Science 331: 1383-1384.

Wilson, J.R.U., García-Díaz, P., Cassey, P., Richardson, D.M., Pyšek, P., Blackburn, T.M. (2016) Biological invasions and natural colonisations are different – the need for invasion science. NeoBiota 31: 87-98.

50

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

Iron Lion Zion: the successful, albeit lingered, invasion of the lionfish in the Israeli Mediterranean Sea Nir STERN1*, Shevy B.S. ROTHMAN2 1 National Institute of Oceanography, Israel Oceanographic and Limnological Research, Haifa, ISRAEL 2 School of Zoology, The George S. Wise Faculty of Life Sciences and the Steinhardt Museum of Natural History, Tel Aviv University, Tel Aviv, ISRAEL *Corresponding

author: nirstern@ocean.org.il

Alien invasive fish species in Israel The synergistic combination of the proximity of the Suez Canal to the Mediterranean coasts of Israel with the general anti-clockwise water circulation in the Levant Basin (Menna et al. 2012) ensure a continuous influx of invasive Red Sea and Indo-Pacific fauna into Israeli waters, and explain the higher number of established alien species in comparison with neighboring countries (Galil et al.

2016). The invasive fauna in Israel reside in almost every marine habitat, from the coastal rocky plateau to the sandy bottom down to 200 m deep (Galil et al.

2018). The local interest in studying and documenting this unique and intense biological invasion in Israel has begun well before the establishment of the country, in the early 20th century, and was initially noted in several faunal inventories (Galil 2007). Ever since, it has become a focal investigated interest among Israeli marine biologists, policy-maker organizations, stake holders and conservation agencies. Documentation of new invasive species are frequently published, while other aspects are also being investigated, such as trophic level evaluation (Goren et al. 2016), genetic population structure (Stern et al. 2018), molecular identification initiatives of invasive species (Karahan et al. 2017), and more.

The rich diversity of invasive species in the Israeli Mediterranean caused a variety of ecological and economic impacts on the local ecosystem. While the specific impacts of the invasive species are usually difficult to discern, some possess an indisputable impact, from both side of the spectrum. On the one hand, some commercial invasive species such as the goatfishes and the paneaid prawns are highly desirable by the Israeli fisheries industry, retaining a constant year-around high value (Galil 2007), whereas some others possess a highly detrimental impact, such as the nomad jellyfish Rhopilema nomadica that occasionally force fishermen to abandon their nets in the sea due to overloading in the swarming season (EastMed 2010).

Although it is well known that invasive species are responsible for the loss of global biodiversity and their management has to be seriously prioritized, the 51

authorities in Israel are facing a unique dilemma for immediate actions, as further detailed here through the case of the invasive lionfish Pterois miles (Bennett 1828).

The invasive lionfish chronology in the Israeli Mediterranean coast A single individual of a large adult lionfish (Pterois miles) was landed by a bottom trawler off the central coast of Israel, constituting the first and only record of the species in the Mediterranean Sea for more than two decades (Golani and Sonin 1992). Therefore, this record was disregarded and remained esoteric, despite proven evidences of the potential detrimental threat lionfish pose to natural ecosystems. The second sighting along the Israeli shores occurred on November 2013, within the northern Akhziv marine nature reserve, nearly one year after (Bariche et al. 2013) has documented the lionfish from Lebanese coasts, signifying the onset of a continuous and increasing wave of invasion. Despite its rapid range expansion throughout the Levant Basin (Turan et al. 2014), the lionfish has progressed in a relatively slow pace along the Israeli coastline. At first, sightings were few and remained restricted to Akhziv marine nature reserve, at 15-27 m depth. Only after 18 months, during May 2015, reports of sightings started to accumulate from Haifa Bay, and later that year, from central Israel, ~ 30 m deep. Although to date, the lionfish has been documented throughout the Israeli coastline, the majority are still restricted to the reefs of the northern coast, presumably a preferable habitat for the recruitment of juveniles. The scarcity of continuous rocky habitats in the Israeli coast may explain its relatively slow expansion rate throughout the coastline.

Among its various versatile traits, the lionfish also occupies large depth gradients, from the shallows to 300m mesophotic deep reefs (Nuttall et al. 2014; Gress et al. 2017). Currently, the majority of sightings along the Israeli coast were deeper than 20m, and relatively distanced from the coast (>800 m). Most observations were from natural and artificial reefs, such as wrecks, with several aggregations (> five individuals) at 30â&#x20AC;&#x201C;50m depth (Figure 1a, b). Recent reports also showed a slow transition of juvenile lionfish into shallow waters at ~5 m depth and in greater proximity to the shore (Figure 1c). Nonetheless, perhaps the biggest conservation concern should be upturned towards deeper reefs; recently, the presence of lionfish was documented using a Remotely-Operated Vehicle in five distant mesophotic reefs at 95-120 m depth along the Israeli coasts, signifying a possible future impact in this relatively conserved areas (Figure 2, Idan et al. unpub. data). NaĂŻve populations of indigenous mesopelagic benthic species, such as Anthias anthias and Helicolenus dactylopterus, may be strongly inflicted by this new voracious predator. Unfortunately, the combination of the fragmented morphology of these reefs and the difficulty in executing culling activities at these depths may additionally provide an untouched haven for refuge breeding hubs against shallow water culling campaigns.

52

In terms of population structure, a recent study (Stern et al. 2018) has investigated the genetic reservoir of the invasive lionfish in the Mediterranean and showed significantly low divergence in the invasion population compared to native habitat, indicating a future possible enrichment of this haplotype shortage, which in turn may further strengthen its successful establishment in the Mediterranean Sea.

Figure 1. (a) Lionfish in a wreck (F/V â&#x20AC;&#x2DC;Nizzanâ&#x20AC;&#x2122;) at 28m deep, Nahariya, Northern Israel.

Photo: O. Klein (b) Interaction of lionfish with round stingray Taeniurops grabatus, within Akhziv marine nature reserve at Northern Israel. Photo: S.B.S Rothman (c) Juvenile lionfish in the shallow rocky shore of Gordon, Tel Aviv. Photo by: Y. Halevi

Figure 2. Remotely Operated Vehicle (ROV) documentations of lionfish in the Israeli mesopelagic reefs. (a) Individual at 98m deep, Atlit, Northern Israel, September 2017 (b) Individual at 95m, Herzliya, Central Israel, March 2016.

53

The Israeli management dilemma Despite the unfeasible goal to eradicate a marine invasive species, management actions in the Western Atlantic indicate that targeted removal efforts can reduce lionfish abundance, providing benefits for the native reef community (Frazer et al. 2012). Thus, shortly after an increase in the lionfish population along the Israeli coast was detected, an urgent call has been addressed to the Israeli Nature and Parks Authorities (INPA) for removal measures to be initiated, by engaging volunteering divers and fishermen. Nonetheless, implementation of such management actions towards the lionfish in Israel, is currently postponed due to a unique dilemma: Israel also has a Red Sea coast and the lionfish is indigenous to the Red Sea, therefore it is designated as a protected species under Israeli regulations, with a strict ban on the fishing or trading of this species throughout the commercial and ornamental fish industries (The Israeli Ministry of Environmental Protection 2005). Ironically, these regulations prevent the execution of a management response in the Mediterranean, and are nowadays being debated by the authorities (Stern and Rothman 2018). To make things even more difficult for management authorities, large densities of invasive lionfish are currently found inside marine nature reserve and/or at depths greater than 20m, where SCUBA gear is required for effective culling activities.

Figure 3. A citizen science pamphlet made by the authors, for collecting evidences of lionfish in the Israeli Mediterranean and informing the public about its potential risks (in Hebrew).

54

Only once the legal grounds will be revised and amended, additional initiatives can be proposed. These can be the promotion of local culling derbies of lionfish and the exposure of its edibility to the unaware public, in terms of both its â&#x20AC;&#x2DC;Kosherâ&#x20AC;&#x2122; status and the careful handling of the species to avoid injuries from its venom. Meanwhile, a preliminary collaboration with the Israeli recreational divers, artisanal and industrial fishermen have been established through several social networks, encouraging to document the whereabouts of the lionfish in return to relevant and informative scientific knowledge (Figure 3, in Hebrew).

Future perspectives Considering the inevitable urgency in protecting the local environment from this threat, we posit that promoting actions of solidarity among the neighboring Levantine countries may contribute to the general success in mitigating the present and future impacts of the lionfish throughout the Mediterranean Sea. Harnessing the public assistance in culling activities, for example, will gain more positive responses if it will be addressed simultaneously in each county, and sharing local consequences and conclusions may improve the results of future activities. At the end, the lionfish is here to stay, and it is our responsibility to maximize the efficiency in mitigating its unfortunate detrimental effect.

References Bariche, M., Torres, M., Azzurro, E. (2013) The presence of the invasive lionfish Pterois miles in the Mediterranean Sea. Mediterranean Marine Science 14: 292294.

EastMed, F. (2010) Report of the Sub-Regional Technical meeting on the Lessepsian migration and its impact on Eastern Mediterranean fishery. Nicosia, Cyprus, December 5-7.

Frazer, T.K., Jacoby, C.A., Edwards, M.A., Barry, S.C., Manfrino, C.M. (2012) Coping with the lionfish invasion: can targeted removals yield beneficial effects?.

Reviews in Fisheries Science 20: 185-191.

Galil, B.S. (2007) Seeing Red: Alien species along the Mediterranean coast of Israel. Aquatic Invasions 2: 281-312.

Galil, B., Danovaro, R., Rothman, S., Gevili, R., Goren, M. (2018) Invasive biota in the deep-sea Mediterranean: an emerging issue in marine conservation and management. Biological Invasions doi: 10.1007/s10530-018-1826-9.

Galil, B.S., Marchini, A., Occhipinti-Ambrogi, A. (2016) East is east and West is west? Management of marine bioinvasions in the Mediterranean Sea. Estuarine, Coastal and Shelf Science 201: 7-16.

55

Golani, D., Sonin, O. (1992) New records of the Red Sea fishes, Pterois miles (Scorpaenidae) and Pteragogus pelycus (Labridae) from the eastern Mediterranean Sea. Ichthyological Research 39: 167-169.

Goren, M., Galil, B.S., Diamant, A., Stern, N. (2016) Invading up the food web?

Invasive fish in the southeastern Mediterranean Sea. Marine Biology 163: 180.

Gress, E., Andradi-Brown, D.A., Woodall, L., Schofield, P.J., Stanley, K., Rogers, A.D. (2017) Lionfish (Pterois spp.) invade the upper-bathyal zone in the western Atlantic. PeerJ 5: e3683.

Karahan, A., Douek, J., Paz, G., Stern, N., Kideys, A.E., Shaish, L., Goren, M., Rinkevich, B. (2017) Employing DNA barcoding as taxonomy and conservation tools for fish species censuses at the southeastern Mediterranean, a hot-spot area for biological invasion. Journal for Nature Conservation 36: 1-9.

Menna, M., Poulain, P., Zodiatis, G., Gertman, I. (2012) On the surface circulation of the Levantine sub-basin derived from Lagrangian drifters and satellite altimetry data. Deep Sea Research Part I: Oceanographic Research Papers 65: 46-58.

Nuttall, M.F., Johnston, M.A., Eckert, R.J., Embesi, J.A., Hickerson, E.L., Schmahl, G.P. (2014) Lionfish (Pterois volitans [Linnaeus, 1758] and P. miles [Bennett, 1828]) records within mesophotic depth ranges on natural banks in the Northwestern Gulf of Mexico. BioInvasions Records 3: 111-115.

Stern, N., Jimenez, C., Huseyinoglu, M.F., Andreou, V., Hadijioannou, L., Petrou, A., Öztürk, B., Golani, D., Rothman, S.B.S (2018) Constructing the genetic population demography of the invasive lionfish Pterois miles in the Levant Basin, Eastern Mediterranean. Mitochondrial DNA Part A 1-7.

Stern, N., Rothman, S.B. (2018) Divide and conserve the simultaneously protected and invasive species. Aquatic Conservation: Marine and Freshwater Ecosystems 2018: 1-2 doi: 10.1002/aqc.2950.

The Israeli Ministry of Environmental Protection (2005) Declaration of national parks, nature reserves, national sites and protected natural products. pp. 1-9 (in Hebrew).

Turan, C., Ergüden, D., Gürlek, M., Yağlıoğlu, D., Uyan, A., Uygur, N. (2014) First record of the Indo-Pacific lionfish Pterois miles (Bennett, 1828) (Osteichthyes: Scorpaenidae) for the Turkish marine waters. Journal of Black Sea/Mediterranean Environment 20: 158-163.

56

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

The need for international environmental regulations on artificial waterways: The Suez Canal case Senem ATVUR*, Ceren Uysal OĞUZ Akdeniz University, Faculty of Economics and Administrative Sciences, Department of International Relations, Antalya, TURKEY *Corresponding

author: senematvur@akdeniz.edu.tr

Introduction Since the ancient times, building waterways or canals have connected different aquatic realms. During the Ptolemaic period, the first canal project joining the Nile River with the Red Sea had launched in Ancient Egypt by expanding the irrigation canal that was built in the 19th century BCE. Then in the 7th century BCE in Ancient Greece the idea of constructing a canal connecting the Gulf of Corinth with Saronic Gulf had bloomed. Although the idea could not be realized until the 19th century, artificial waterways or canals, with their geographic and strategic roles, have become the engineering marvels of the modern era. Despite their benefits for the international navigation and trade, transboundary environmental degradation caused by these waterways has been neglected. The legal status of these canals, which is based on the supremacy of the state sovereignty, complicates mitigating the environmental impacts. As the fundamental of the modern international system is the sovereignty of the state, there are no supranational regulations regarding the environmental protection.

However, the international law, which is defined as the sum of the rules to preserve peace and the international order, regulates the harm caused by states and sanctions certain acts damaging other parties’ integrity. Therefore, protecting the environment could also be assessed in the context of collective interest and state’s obligations (Fitzmaurice 2013).

This study aims to discuss whether the environmental damage spread through artificial waterways could be limited by the improvement of transnational and supranational regulations. With the case study of Suez Canal, it is intended to reveal that a sovereign state’s unilateral act could harm neighbor or peripheral states. Besides the diplomatic mechanisms, a transnational regulation prohibiting environmental degradation by dire sanctions is considered as a solution for the transboundary impacts of environmental problems. But the critical point is, even if these regulations are adopted, the application would still depend on states.

Hence the global system needs a new perspective to ensure the sustainability of the environment and a new global structure which prioritizes the common interests of the humanity rather than the interest of a single state or a single group.

57

The status of the artificial waterways The artificial waterways, known mostly as canals are important passageways for the international transportation. Canals, together with rivers and straits, are asserted as an example of “international waterways” which “are used to a substantial extent by the commercial shipping or warships belonging to States other than the riparian nation or nations” (Baxter 1964 cited by Johnson 1968).

Although both straits and canals are admitted as international waterways, their legal statuses are completely different. The straits which ensure a natural passage between different seas and oceans are subjects of international law. The Corfu Channel Case which is brought to the International Court of Justice by the UK against Albania, became a principal reference for the codification of international law related to straits and different multilateral treaties signed since this decision have shaped the international regime (Lapidoth 1976).

However, the canals -artificial waterways- differ from natural watercourses with their legal status. There are various classifications of canals; geographical situation, navigation principals, capacity of vessels are the main measures according to which regulations of the canal could be assured (Lapidoth 1976).

Hence the essential difference between canals is related to the authority. For the inland canals which run through the single sovereign state, the state authority is fundamental (Pazarcı 2004). On the other hand, concerning inter-maritime canals, which connect two different seas or oceans and which are very crucial for the international commerce, there are still discussions on the sovereignty of the state.

The inter-maritime canals are also part of inland waters where the sovereignty of the state is recognized by the international law. However, discussions on the application of an international regime related to the canals - particularly important for the international transportation have been continuing (Lapidoth 1976) 1.

Therefore, it is obvious that although the canals are part of the state territory, the canals which have a strategic role for the global commerce, are also subject to the specific international treaties regulating the passage in accordance with the international law and the state sovereignty. One of these strategic waterways is the Suez Canal.

The Suez Canal: historical and legal aspects The Suez Canal was opened for general use on November 17, 1869. The Canal reduced the transit distance between Northern and Southern hemispheres by hundreds or thousands of miles and it was considered as a revolution in maritime activities when it became operational. The Suez waterway was constructed by the Compagnie Universelle du Canal Maritime de Suez which was founded by French citizen Ferdinand de Lesseps (Hoskins 1943). Hoskins (1943) claimed that there Different views on the application of international regime and the free passage from canals are not included in this study because the focus of this study is on environmental regulations related to canals.

1

58

were several problems regarding the legal status of the company that led to various types of litigation over the years. First of all, even though the company was supposedly international, it was predominantly French. Second, its corporate offices were established in Paris, while its administrative headquarters were located in Alexandria. Third, it started to operate the Canal as an international waterway under its own statutes, while in some respects it was subject to the French laws and in others to Egyptian and Turkish regulations and actually it was independent of international control.

According to Delson (1957), from the very beginning, Britain was the most important user of the Suez Canal which became vital in conducting imperial communications. In 1882 Britain occupied Egypt claiming that “the free and unimpeded navigation of the canal . . . and its freedom from obstruction or damage by acts of war, are matters of importance to all nations.” Britain also proposed an agreement to provide for freedom of passage for all ships. France, on the other hand, preferred the creation of an international commission. As a result, the “Constantinople Convention” which provided that the Suez Canal should always be open to non-discriminatory passage in time of war and peace was signed on October 29, 1888 by the great powers of the time: Great Britain, Austria-Hungary, France, Italy, Germany, Holland, Spain, Russia and the Ottoman Empire. Due to British opposition, the provision for the establishment of a supervisory commission never came into effect (Delson 1957). Article I of the Constantinople Convention respecting the Free Navigation of the Suez Maritime Canal states that “The Suez Maritime Canal shall always be free and open, in time of war as in time of peace, to every vessel of commerce or of war, without distinction of flag.” (Johnson 1968).

After the Ottoman Empire renounced all of her rights and titles over Egypt as of November 5, 1914, Britain proclaimed a protectorate over Egypt on December 18, 1914. During the First World War, Britain benefited from the strategic location of the Canal against the forces of Germany and the Ottoman Empire. In the aftermath of the war, Egypt declared independence on February 28, 1922.

According to the Treaty of Alliance signed between Britain and Egypt in 1936, it was recognized that while the Canal was an integral part of Egypt, it was also an essential means of communication between the different parts of the British Empire, therefore provision was made for insuring the defense of the Canal by British forces stationed in Egypt in collaboration with Egyptian forces. In 1948, after the creation of Israeli State, Egypt rejected Israeli vessels or cargoes bound for Israel to pass through the Suez Canal. In 1951, the Security Council called upon Egypt to terminate these restrictions as a violation of the Egyptian-Israeli Armistice Agreement of 1948. In 1954, the British and Egyptian governments agreed upon the evacuation of British forces by June 1956 (Delson 1957).

On July, 26 1956 the Universal Company of the Suez Maritime Canal was nationalized by the President Gamal Abdel Nasser and according to the Decree issued by Egypt “all its assets, rights and obligations are transferred to the Nation 59

and all the organizations and committees that now operate its management are hereby dissolved.â&#x20AC;? (Delson 1957). As Lapidoth (1976) underlines the Suez Canal, like all artificial waterways, is in principle subject to the sovereignty of the riparian state, Egypt. However, it has also been subjected by Constantinople Convention to a regime of free passage for all. The nationalization of the Canal triggered an international crisis and the British, French and Israeli troops launched a military intervention against Egypt. One of the reactions of Egypt was closing the Canal until 1957. In 1967, during the Six-Day War, the Canal was closed for the second time by Egypt. The Canal reopened to the international shipping in June 1975. During its closure, all users were forced to find reasonable alternative routes (Lapidoth 1976). In order to regain the significance of the Canal, enlargement plans were introduced by Egypt.

The expansion of the Suez Canal and its effects in the Mediterranean region When the Suez Canal was constructed in 1869, the length of the canal was 168 km, the depth was 8 meters, the width was 22 meters at the bottom, 61 to 91 meters at the surface; in every 8 to 10 kilometers passing bays were also built.

The capacity and the structure of the Canal have been modified since the opening.

Table 1 shows how the physical features of the Canal have been changed. By 2015, the existing waterway was enlarged through the 37 km-long expansion and a new 35 km-long lane parallel to the Canal was constructed (Malsin 2015).

As can be seen in Table 1, since the 1980s the Canal has been enlarged and the capacity of the ships using the canal has been augmented. After the 1990s, the intensification of the global commerce and the technological developments has increased the maritime traffic, so the enlargement of the Canal became a necessity for Egypt to compete in the global market. The new Canal project is also part of the idea to increase the transit passages through the Egyptian territory. Figure 1 indicates the plan of the new project. Facilitating the traffic in two directions and minimizing the waiting time for transit passage are the aims of the new canal construction (Suez Canal Authority 2018b). In addition to these objectives, the expected advantages of the new canal are to boost the national income, to shorten the passage time, to attract more ships to use the Canal, to increase the importance of the Canal among the international maritime routes, to strengthen national economy and to turn Egypt into an international logistic center (Suez Canal Authority 2018b).

60

61

164 --8 22 304

5000

km

km

m

m

feet

m²

DWT

Overall Length

ByPasses Length

Width at 11 m Depth

Water Depth Max.

Draft of Ship

Cross Sectional Area 30000

1200

35

14

60

27.7

175

1956

60000

1800

38

15.5

89

27.7

175

1962

170000

3600/ 4000

3250/ 3600 150000

56

20.5

53

19.5

77 170/ 190

77

189.80

1994

160/ 175

189.80

1980

185000

3850/ 4300

58

21

180/ 200

77

189.80

1996

210000

4350/ 4800

62

22.5

195/ 215

79

191.80

2001

Source: Suez Canal Authority (2018a). “Canal Characteristics”, https://www.suezcanal.gov.eg/English/About/SuezCanal/Pages/CanalCharacteristics.aspx (accessed 25 Sep. 2018).

Max. Loaded Ship

1869

Unit

Item

Table 1. Development of the Suez Canal

240000

4800/ 5200

66

24

205/ 225

80.5

193.30

2010

240000

4800/ 5200

66

24

205/ 225

113.3

193.30

2015

Figure 1. The New Suez Canal Project Source: Suez Canal Authority (2018b). “New Suez Canal”, https://www.suezcanal.gov.eg/English/About/SuezCanal/Pages/NewSuezCanal.aspx (accessed 26 Sep. 2018).

Despite the economic contributions of the new Canal, one of the most important adverse effects on the environment is the introduction of invasive species in the Mediterranean Sea. According to several studies, about 500 non-indigenous species (NIS) introduced in the Mediterranean Sea are considered Erythraean NIS i.e. species introduced through the Suez Canal (Galil et al. 2017). Scientists assert that some of these species such as lethally poisonous “silverside” pufferfish (Lagocephalus sceleratus), striped eel catfish (Plotosus lineatus), scyphozoan jellyfish (Rhopilema nomadica), highly venomous lionfish (Pterois miles), and two herbivorous rabbit fishes (Siganus luridus and Siganus rivulatus) create substantial health hazards along with negative environmental and economic effects. For instance, internal organs of the “silverside” pufferfish contain tetrodotoxin, a strong paralytic neurotoxin which causes vomiting, respiratory arrest, seizures, cardiac arrest, coma, and death. The striped eel catfish that spread along the Levant coastline from Egypt to Turkey has venom glands in the spines of the dorsal and pectoral fins, and glandular cells with proteinaceous toxin in its skin. The scyphozoan jellyfish has first recorded in the Mediterranean in the 1970s, forms large swarms in summer that affect tourism, fisheries and coastal installations such as power plants. Rabbit fishes, Siganus luridus and Siganus rivulatus, on the other hand, caused a serious decline in biogenic habitat complexity, biodiversity and biomass in the Levantine Basin (Galil et al. 2017; Galil et al. 2015). Bariche et al. (2013) note that the first example of highly venomous lionfish, Pterois miles, in the Mediterranean Sea was recorded in 1991

by Golani and Sonin (1992). Galil et al. (2017) explain that twenty years after the first specimen, several records of Pterois miles from Israel, Lebanon, Cyprus, Turkey and Tunisia were published by scientists. It confirms the existence of an 62

established population in the Levant and North Africa and if the population of lionfish expands, increasing numbers of injuries to swimmers, divers and fishers are also expected (Galil et al. 2017). As these examples show, the NIS in the Mediterranean are mostly entered through the enlarged Suez Canal. The negative environmental, economic impacts and the health problems caused by these invasive species are of concern to all coastal states in the Mediterranean. Hence the international cooperation for the protection of the Mediterranean Sea becomes inevitable.

International initiatives for the protection of the Mediterranean Sea The Mediterranean has been the cradle of different civilizations during the history. This semi-enclosed sea -connected to the Atlantic Ocean by strait of Gibraltar, to the Black Sea by the straits of Dardanelles and Bosporus, to the Red Sea by the Suez Canal- is also one of the major international maritime routes (Scovazzi 2018). Beyond the strategic importance of the Mediterranean, the ecological richness and biodiversity are other features of the region which are under pressure of different threats such as pollution, overfishing or offshore activities (hydrocarbon drilling or construction of pipelines). These threats originate from the insufficient prevention and the reluctance of the regional states.

One of these risks is the increasing number of invasive species which threatens the local species and ecological diversity in the Mediterranean. After the enlargement of the Suez Canal, it is obvious that the share of invasive species has augmented. Although Egypt applies environmental regulations and adopted some important international conventions, the transboundary effects caused by the countryâ&#x20AC;&#x2122;s initiatives could not be limited or sanctioned. In Table 2, the list of agreements or conventions related to the environmental problems that Egypt signed or ratified could be seen.

Table 2. List of environmental agreements or conventions Egypt signed or ratified Name of Convention Climate Change UN Framework convention on Climate change (UNFCCC) Kyoto Protocol Vienna Convention on the protection of the ozone layer Montreal Protocol on substances that deplete the ozone layer Paris Agreement Hazardous Substances and Wastes Basel Convention on the Control of Transboundary Movements of Hazardous Wastes and their Disposal

63

Date of Signature

Date of Ratification

Date of Entry into Force

6/9/1992

12/5/1994

3/5/1995

3/15/1999 3/22/1985

1/12/2005 5/9/1988

4/12/2005

9/16/1987

8/2/1988

4/22/2016 1/8/1993

Table 2. Continued Stockholm Convention on Persistent Organic 5/17/2002 5/2/2003 Pollutants Convention On The Ban Of The Import Into Africa 1/30/1991 5/18/2004 And The Control Of Transboundary Movement And Management Of Hazardous Wastes Within Africa (Bamako Convention) Marine Pollution Regional Convention for the Conservation of the 5/31/1990 8/20/1985 Red Sea and Gulf of Aden Environment (Jeddah Convention) Convention for the Protection of the Marine 2/16/1976 8/24/1978 7/9/2004 Environment and the Coastal Region of the Mediterranean Nature Conservation United Nations Convention on Biological 6/9/1992 6/2/1994 Diversity (UNCBD) Cartagena Protocol on Bio-safety to the 12/20/2000 12/23/2003 3/21/2004 Convention on Biological Diversity Nagoya Protocol on Access to Genetic Resources 1/25/2012 10/28/2013 and the Fair and Equitable Sharing of Benefits Arising from their Utilization Ramsar Convention on Conservation and Wise Use 9/9/1988 of Wetlands Agreement on the Conservation of Cetaceans of the 4/19/2010 7/1/2010 Black Sea, Mediterranean Sea and contiguous Atlantic Area (ACCOBAMS) Convention on the Conservation of Migratory 11/1/1983 Species of Wild Animals (CMS), Bonn convention Agreement on the Conservation of African- 8/20/1997 11/1/1999 11/1/1983 Eurasian Migratory Waterbirds (AEWA) Source: Arab Republic of Egypt, Ministry of Environment, Egyptian Environmental Affairs Agency, http://www.eeaa.gov.eg/en-us/laws/conventions.aspx (accessed 20 Sep. 2018).

Among these multilateral accords, “Convention for the Protection of the Marine Environment and the Coastal Region of the Mediterranean” is fundamental for maintaining the ecological balance in the Mediterranean region. This convention is actually the amended version of the “Convention for the Protection of the Mediterranean Sea against Pollution” known as “Barcelona Convention” which was adopted in 1976. The Convention with its seve n protocols 32 and the 32 These

are The Protocol for the Prevention of Pollution in the Mediterranean Sea by Dumping from Ships and Aircraft, The Protocol concerning Cooperation in Preventing Pollution from Ships and, in Cases of Emergency, Combating Pollution of the Mediterranean Sea, The Protocol for the Protection of the Mediterranean Sea against Pollution from Land-Based Sources and Activities, The Protocol concerning Specially Protected Areas and Biological Diversity in the Mediterranean, The Protocol for the Protection of the Mediterranean Sea against Pollution Resulting from Exploration and Exploitation of the Continental Shelf and the Seabed and its Subsoil, The Protocol on the Prevention of Pollution of the Mediterranean Sea by Transboundary Movements of Hazardous Wastes and their Disposal, The Protocol on Integrated Coastal Zone Management in the Mediterranean (UNEP and MAP, 2015).

64

“Mediterranean Action Plan” is called Barcelona system which emphasizes regional cooperation for the protection of the marine environment (Scovazzi 2018). According to the Article 4.1 of the Convention (UNEP, 2004): “The Contracting Parties shall individually or jointly take all appropriate measures in accordance with the provisions of this Convention and those Protocols in force to which they are party to prevent, abate, combat and to the fullest possible extent eliminate pollution of the Mediterranean Sea Area and to protect and enhance the marine environment in that Area so as to contribute towards its sustainable development”.

The Convention also underlines the responsibility of the Parties “to pursue the protection of the marine environment and the natural resources of the Mediterranean Sea Area as an integral part of the development process, meeting the needs of present and future generations in an equitable manner.” The Contracting Parties also accept that all kinds of pollution caused by dumping or discharge from ships or aircrafts; exploration and exploitation of the continental shelf, the seabed and the subsoil; land-based sources (directly from outfalls discharging into the sea or through coastal disposal or indirectly through rivers, canals or other watercourses, including underground watercourses, or through run-off) should be prevented through appropriate measures (Art. 5-6-7-8). The Convention also supports the cooperation between parties to reduce and eliminate the pollution (Art. 9). Article 10 of the Convention emphasizes the necessity of the measures to “protect and preserve biological diversity, rare or fragile ecosystems, as well as species of wild fauna and flora which are rare, depleted, threatened or endangered and their habitats” (UNEP 2004).

According to the Article 15, the Contracting Parties should give to the public appropriate access to information on the environmental state, and ensure the public participation in decision-making processes relevant to the field of 2 application of the Convention and the Protocols. The Article 16 states that “the Contracting Parties undertake to cooperate in the formulation and adoption of appropriate rules and procedures for the determination of liability and compensation for damage resulting from pollution of the marine environment in the Mediterranean Sea Area”. However, it is not clear how the judicial procedure would be established and functioned (Scovazzi 2018). Moreover, the damage of marine ecosystem caused by the factors other than the pollution has not been mentioned in the Convention; the vagueness of this kind of harm creates more complex transboundary problems.

The “Convention on Biological Diversity” signed in 1992 at the end of the Rio Summit provides the legal framework to the conservation of biological diversity.

In this context the Convention recognizes states’ sovereign rights “to exploit their own resources pursuant to their own environmental policies”, as well as “the responsibility to ensure that activities within their jurisdiction or control do not 65

cause damage to the environment of other States or of areas beyond the limits of national jurisdiction” (Art. 3) (UN 1992). The rights and obligations of any Contracting Party deriving from any international agreement would not be affected by the provisions of the Convention unless the exercise of those rights and obligations would cause a serious damage or threat to biological diversity (Art. 22) (UN 1992).

As international conventions mentioned above have shown, state sovereignty is the fundamental element of the international law and international relations. In this context, internal regulations and laws have become the primary sources to ensure environmental protection. However the prevention of transboundary hazards remains a challenging endeavor. Since the political agenda of the states prioritizes the military or economic issues rather than ecological problems, state measures for environmental protection remain limited or ineffective, and improving international cooperation and developing legally binding regulations including the sanctions are jeopardized. The case of Egypt regarding Suez verifies this reality. The Environment Law of Egypt adopted in 1994 and amended by the Law No.9 in 2009 strengthens the role of Egyptian Environmental Affairs Agency (EEAA) which is responsible for the coordination and management of environmental affairs (Wahaab 2003). The Law also introduces the environmental impact assessment process even though the process has some limitations such as the lack of technical skills to evaluate site impact or other remedies and the inspections (Wahaab 2003). Nonetheless, Egypt’s environmental policies have been shaped by economic priorities. The National Environmental Action Plan for 2002-2017 reveals that environmental policy is integrated and complemented with economic growth and social development, and improving of the environmental standards is linked to the increase of “the competitiveness of the Egyptian products in the global markets that demand environmentally-friendly products” (EEAA 2001). Wahaab (2003) claims that the main problem related to environmental policies of Egypt is not the lack of environmental plans, but the inefficient application of these plans, weak regulatory compliance and enforcement that deepen the problems.

As can be seen, Egypt could not apply an integrated environmental policy. Even though Egypt adopted certain environmental conventions, the environmental problems in the country could only be handled by the national authorities. So the international cooperation or initiative to mitigate and solve environmental problems remains ineffective or limited. However, the transboundary impacts of ecological problems keep growing and new regulations to cope with interdependent problems are needed.

Concluding remarks The Article 4.3(d) of the Barcelona Convention to which Egypt is a signatory, states that “cooperation between and among States in environmental impact 66

assessment procedures related to activities under their jurisdiction or control which are likely to have a significant adverse effect on the marine environment of other States or areas beyond the limits of national jurisdiction.” (Galil et al.

2015). According to Galil et al. (2017), the successive enlargements of the Suez Canal caused concerns about the introductions of more Erythraean nonindigenous species in the Mediterranean that would lead to degradation and loss of native populations, habitats and ecosystem services. Moreover, the scientists underline that “it is unknown which new species will pass through the Suez Canal and establish themselves and when, and what will be their interaction with the Mediterranean biota.” Unfortunately, they affirm that “it is clear that a larger and deeper Suez Canal allows cohorts of new potentially invasive species to gain admittance to the Mediterranean Sea, where increasing temperatures permit their further expansion westwards and northwards.” They also claim that the States which signed the Barcelona Convention agreed to take all appropriate measures, individually or jointly, to protect and preserve biological diversity; however, they failed completely to manage the introduction of non-indigenous species through the Suez Canal (Galil et al. 2017). In the international law it is commonly accepted not to harm third parties, however in the case environmental damage there is a legal gap.

Transboundary or environmental damage is defined as a harm caused by or originating in one State, and affecting the territory of another. Several international treaties or conventions mention various forms of transboundary damage such as pollution of international waters, long-range air pollution, landsource damage to the ocean and oil pollution. According to Hanquin (2003), “while some of the treaties directly lay down rules on liability and compensation, most contain only general provisions dealing with State responsibility and liability, leaving issues of detailed implementation aside for future action”. A new approach in international law to prevent the damage at source rather than the compensation of the harm (Hanquin 2003) is essential for the protection of the environment especially of the marine life and biodiversity in the Mediterranean Sea. Deepening the global cooperation between states and non-state actors could improve the implementation of ecological regulations. Moreover, the mitigation of ecological problems depends on increasing global awareness and common action.

References Arab Republic of Egypt, Ministry of Environment, Egyptian Environmental Affairs Agency.

Available at http://www.eeaa.gov.eg/enus/laws/conventions.aspx (accessed 20 Sep. 2018).

Bariche, M., Torres, M., Azzurro, E. (2013) The presence of the invasive lionfish Pterois miles in the Mediterranean Sea. Mediterranean Marine Science 14(2): 292-294.

67

Baxter, R.R. (1964) The Law of International Waterways with Particular Regard to Interoceanic Canals. Harvard University Press, Cambridge, 381 pp.

Delson, R. (1957) Nationalization of the Suez Canal Company: Issues of public and private international law. Columbia Law Review 57(6): 755-786.

EEAA (2001) The National Environmental Action Plan of Egypt 2002/17.

Available at http://www.eeaa.gov.eg/portals/0/eeaaReports/neap/Neap_Englast.pdf (accessed 25 Sep. 2018).

Fitzmaurice, M. (2013) The International Court of Justice and International Environmental Law. In: The Development of International Law by the International Court of Justice. (eds., Tams, C.J, J. Sloan), Oxford University Press, Oxford, pp. 353-374.

Galil, B., Boero, F., Fraschetti, S., Piraino, S., Campbell, M., Hewitt, C., Carlton, J., Cook, E., Jelmert, A., Macpherson, E., Marchini, A., Occhipinti-Ambrogi, A., Mckenzie, C., Minchin, D., Ojaveer, H., Olenin, S., Ruiz, G. (2015) The enlargement of the Suez Canal and introduction of non-indigenous species to the Mediterranean Sea. ASLO 24(2): 43-45.

Galil, B., Marchini, A., Occhipinti-Ambrogi, A., Ojaveer, H. (2017) The enlargement of the Suez Canal â&#x20AC;&#x201C; Erythraean introductions and management challenges. Management of Biological Invasions 8(2): 141-152.

Golani, D., Sonin, O. (1992) New records of the Red Sea fishes Pterois miles (Scorpaenidae) and Pteragogus pelycus (Labridae) from the Eastern Mediterranean Sea. Japanese Journal of Ichthyology 39: 167-169.

Hanquin, X. (2003) Transboundary Damage in International Law. Cambridge, Cambridge University Press. pp. 1-2.

Hoskins, H.L. (1943) The Suez Canal as an international waterway. The American Journal of International Law 37(3): 373-385.

Johnson, D.H.N. (1968) Some legal problems of international waterways, with particular reference to the Straits of Tiran and the Suez Canal. Modern Law Review 31: 153-164.

Lapidoth, R. (1976) The reopened Suez Canal in international law. Syracuse Journal of International Law and Commerce 4(1): 1-49.

Malsin, J. (2015) The Guardian. Egypt to open Suez canal expansion two years early. Available at https://www.theguardian.com/world/2015/aug/02/egypt-to68

open-suez-canal-expansion-finished-in-a-third-of-projected-time (accessed 26 Sep. 2018).

PazarcÄą, H. (2004) International Law. Turhan Kitabevi, Ankara, 240 pp. (in Turkish).

Scovazzi, T. (2018) International cooperation as regards protection of the environment and fisheries in the Mediterranean Sea. Anuario Espanol de Derecho Internacional 34: 301-321.

Suez Canal Authority (2018a) Canal Characteristics. Available at https://www.suezcanal.gov.eg/English/About/SuezCanal/Pages/CanalCharacteri stics.aspx (accessed 25 Sep. 2018).

Suez Canal Authority (2018b) New Suez Canal. Available at https://www.suezcanal.gov.eg/English/About/SuezCanal/Pages/NewSuezCanal. aspx (accessed 26 Sep. 2018).

UN (1992) Convention on Biological Diversity. Available https://www.cbd.int/doc/legal/cbd-en.pdf (accessed 20 Sep. 2018).

at

UNEP (2004) Convention for the Protection of the Marine Environment and the Coastal Region of the Mediterranean.

Available at http://wedocs.unep.org/bitstream/handle/20.500.11822/7096/Consolidated_BC9 5_Eng.pdf?sequence=1&isAllowed=y (accessed 20 Sep. 2018).

UNEP and MAP (2015) Mediterranean Action Plan. Barcelona Convention.

Available at https://wedocs.unep.org/rest/bitstreams/1298/retrieve (accessed 20 Sep. 2018).

Wahaab, R.A. (2003) Sustainable development and environmental impact assessment in Egypt: Historical assessment. The Environmentalist 23: 49-70.

69

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

Lionfish envenomation: epidemiology, management and prevention Selin Gamze SÜMEN1*, Bengüsu MİRASOĞLU2, Şamil AKTAŞ2 1 Health

Science University, Kartal Dr Lutfi Kirdar Research and Training Hospital, Department of Underwater and Hyperbaric Medicine, TURKEY 2 Istanbul University, Istanbul Faculty of Medicine, Department of Underwater and Hyperbaric Medicine, TURKEY *Corresponding

author: sgsumen@gmail.com

We are all impressed by the beauty of its colors and feathery rays when we come across with her in the deep blue ocean. She looks like she popped out of a fashion show. She quickly recognises us and keeps on staring to all divers surrounding her. She turns round and round smoothly trying to discover the possible threats.

If we attempt to approach her, she looks more impressive than any other creature by opening her thorns like a feathery fan. Her message is clear: “If you threaten me I can be painful, please do not disturb me”.

Introduction A sea creature is labelled as venomous, if it has a special tool for injecting venom.

Toxic secretions discharged through special body parts such as teeth, stings, nematocysts, or hairs which are essential to defend or catch prey for some animals. Fish spines and venom apparatus are usually protection shields for sea animals in case of threats emerging from their predators (Jung and Bodio 2006).

By fancy and colorful spines, fish attract and hunt other surrounding creatures like small fish and use their venomous spines to incapacitate their prey for feeding. However sometimes humans can be targeted. Fish envenomation may cause severe clinical symptoms and result in the fatality of victims shortly after the injury. The severity of the injury depends on the intensity of the envenomation and the predispositional factors of individual such as allergy, age, immune compromised conditions and other comorbidities.

The lionfish (Pterois volitans and Pterois miles) is a venomous fish from the Scorpaenidae family, which consists of stonefish (synanceia), scorpionfish (scorpaena) and lionfish (pteroinae) in order of venom potency (Diaz 2015; Garyfallou 1996). Although there are records of a few subspecies in Polar Regions, lionfish species mostly prefer tropical, subtropical and temperate regions. Common lionfish is native to Indian Ocean and Red Sea but also inhabit Indo-Pacific, Atlantic, and Australian waters. It has entered the Mediterranean Sea as a Lessepsian species. It is also hypothesized that it was transported via ballast tanks of large vessels from native marine environment through Suez Canal and reproduced rapidly (Maclsaac 2016; Bariche et al. 2017; Zenetos et al. 2012; 70

Por 1971). Other theories regarding spreading of lionfish are release from aquariums or results of global warming. Also, devastating effects of Hurricane Andrew in United States are thought to be important around Atlantic area. Six lionfish were freed when Hurricane Andrew destroyed a large marine aquarium at the edge of bay. These lionfish were seen alive in the sea several days later (Schmitt and de Haro 2013; Courtenay 1995; Diaz 2015; Ruiz-Carus et al. 2006).

Regardless of the way they were introduced to non-native waters, this invasive fish species has become a major predator for other native species and threat to major habitats.

First encounter in Mediterranean Sea was at Haifa Bay in 1991 (Golani and Sonin 1992). In 2014, Turan and et al., reported the first lionfish (identified as Pterois volitans but not confirmed) in Turkey at the southeast part of coastal region of Mediterranean Sea (Turan, et al. 2014). A year later, another lionfish (Pterois miles) occurrence at 11 m depth on sandy bottom was reported in Southwestern coasts of Turkey on the Sea (Turan and Ă&#x2013;ztĂźrk 2015). These records are proofs that lionfish are spreading rapidly and we will encounter lionfish more around our coasts in the near future.

Lionfish sting is extremely painful and systemic symptoms including syncope, agitation, palpitation, muscle weakness may occur. Fortunately, life threating manifestations are rarely seen (Diaz 2015). However case reports indicate lionfish envenomations are increasing nowadays (Resiere et al. 2016; Diaz 2015).

Therefore, it should be a priority to create awareness and prepare strategies related to prompt diagnosis, initial treatment and prevention of the injury. The objective of this chapter is to provide detailed information about lionfish envenomation.

Epidemiology Lionfish population has gradually increased, resulting in emerging new envenomation cases. Lionfish envenomations do not pose a significant problem in their native habitat but they are a potential threat for local fishermen, divers, aquarists and swimmers who intendedly or unintendedly hold the fish. There is no accurate (or estimated) data regarding its prevalence in the World. There are a little more than 360 reported cases of lionfish envenomations which commonly involve swimmers, divers, fishermen, and aquarists. (Forrester 2008; Alfredi et al. 1996; Vetrano et al. 2002; Haddad et al. 2015; Schult et al. 2017). Most accidents take place in the warmer months of the year.

Pathophysiology Lionfish has 12-13 dorsal, 2 pelvic and 3 anal spines each of which is covered with loose integument that contains two grooves on the sides of the spines. Each groove is connected to a venom gland at the base of spine. The gland is a colorless tissue and can secrete about 3 to 10 mg of venom per thorn. The main mechanism of intoxication emerges if the victim handles, touches or steps on the fish. When the spine penetrates the skin and soft tissue, loose sheath is pushed down and a 71

pressure is applied on the gland. This causes the venom to discharge from the glands (Auerbach 1991; de Haro and Pommier 2003). The venom is delivered through the bilateral grooves to the puncture area (Vetrano et al. 2002).

The venom is composed of high molecular weight proteins that have acetylcholine and antigenic character. These proteins are heat-labile and lose their structure at 50-60 °C. Due to high molecular weight antigenic protein property of the toxin, systemic reactions emerge (Cohen and Oleg 1989; Kizer et al. 1985).

Toxins in the venom trigger pain through bradykinin receptors. They cause weakness and transient muscle paralysis by disturbing neuromuscular conduction; muscle contractions, cell necrosis, and serum CPK (Creatine Phosphokinase) and AST (Aspartate Aminotranspherase) elevations by the increase of intracellular calcium levels (Church et al. 2003). Also, toxins are shown to cause alterations in heart rate (tachy and bradycardia) and blood pressure (hypo and hypertension) through adrenergic and muscarinic receptors.

Besides these, it’s thought that they have cytotoxic, proinflammatory and prothrombotic effects (Cohen and Oleg 1989; Church et al. 2003; Church and Hodgson 2002). Acetylcholine is thought to be responsible for muscle fibrillation (Cohen and Oleg 1989). It should be noted that the venom can retain full potency up to 48 hours even after animal’s death (Resiere et al. 2016).

Clinical manifestation Symptoms and findings are divided into two groups; local and systemic clinical characteristics (see Table 1). It is not possible to predict how the symptoms will start and what the prognosis will be. Mostly, severe local pain at the puncture area is the first symptom. Other symptoms develop in time, depending on the amount of venom injected and individual factors. Distribution of clinical presentations and complications are summarized in Table 2 (Resiere et al. 2016).

Local features: After the injury, the first symptom is usually intense local pain which extends proximally. Pain increases in intensity over the next few hours and may continue about 6-12 hours. The victims describe the pain as unbearable and like heating the flesh with a hot iron bar. It usually relieves after a few hours, but rarely may persist for weeks (Haddad et al. 2015; Resiere et al. 2016). While the punctured wound is numb, there is increased sensitivity at the surrounding tissue.

Weakness, paralysis and muscle contraction can occur at the injured extremity.

Pain and tenderness may occur in regional lymph nodes, even disseminating to the central part of the body. Puncture wound may be seen on the affected limb.

Puncture wounds are holes caused by long objects such as needles and spines.

They do not bleed profusely but may carry dirt and foreign material into the body tissues which may cause infection. Puncture site may be encircled by inflammatory edema and sometimes bluish cyanotic zone around. The surrounding tissues become pale and cyanotic with blistering edema. Rarely tissue necrosis is seen. Wounds from the sting of lionfish are graded based on the 72

severity: Grade 1) erythema, cyanosis, pallor, ecchymosis at the puncture site.

These result from increased capillary permeability; Grade 2) vesicle or bullous lesion formation; Grade 3) local necrosis of the site (Fernandez et al. 2011).

Table 1. Local and Systemic Findings, Management of Lionfish envenomation Local Signs and Symptoms Intense pain Erythematous rash Local edema Numbness Bleeding

Systemic Signs and Symptoms Weakness Syncope Dyspnea Hypotension Hallucination Soft tissue infection

Treatment Management

Respiratory arrest Cardiorespiratory collapse Shock

1.Urgent intubation and mechanical ventilation 2. Supportive care 3.Critical care management

73

1.Removal of all spines and foreign materials preferably with gloved hands and forceps 2.Cleaning with clear water 3.Direct pressure to prevent bleeding 4. Immersion of wound site in hot water (42450C) for 30-90 min to relieve acute pain. It can be repeated.

5.Use of oral or parenteral analgesics in case of persistent pain 6.Tetanus prophylaxis 7. Observation of patient for 6â&#x20AC;&#x201C;12 h.

8. Prophylaxis with antibiotics if there is a risk of soft tissue infection and contaminated seawater.

9.Surgical debridement if there are signs of necrosis at the wound

Table 2. Distribution of clinical presentations and complications of the patients Signs and Symptoms

% of cases

Pain and local edema

100

Paraesthesia Abdominal cramps Extensive edema Tachycardia Skin rash Gastrointestinal disorders

90 62 53 34 32 28

Fainting Transient weakness Hypertension Hypotension Hypophosphatemia Elevated liver enzyme aspartate aminotransferase (AST) Hyperthermia Bradycardia Thrombocytopenia

27 24 21 18 12 10

Clinical Complications Local infection Skin abscess Cellulitis Skin necrosis Septic arthritis Hospitalization Requiring surgery

% of cases 18 5 3 3 2 22 8

9 3 3

Puncture wounds can get infected. Local infections may advance rapidly to soft tissue infection such as cellulitis, myositis and necrotizing fasciitis and result with severe sepsis. The infection agents can be marine related bacteria like Vibrio and Aeromonas species which can cause systemic infection and death. It should be noted that risk of serious necrotizing infections are much higher for immunocompromised people (Diaz 2014). Also unspotted spines that remained embedded in the tissue may cause pain, edema, itching and even loss of mobility if located near joints (Diaz and Lopez 2015).

Systemic features: Systemic symptoms are not very common but if present they may vary from mild to severe. The victim may suffer anxiety that may result with hallucinating state due to the intensity of the pain. Mostly, nervous system, cardiovascular system, digestive system and skin are affected. Malaise, nausea, vomiting, and sweating associated with mild fever may be present. Pallor, sweating, hypotension, bradycardia and syncope may occur. Respiratory distress, cardiac dysrhythmias, and cardiac arrest may also develop in severe cases.

Cardiovascular shock and death are very rare but possible (Haddad et al. 2015; Resiere et al. 2016). Hypersensitivity to the venom may develop and anaphylactic reactions can be seen in subsequent envenomations. Hypersensitivity is a strong systemic reaction to a foreign matter entering the body. The extreme response is anaphylaxis, which may result in anaphylactic shock, if untreated, the victim can die. Fish sting may cause severe anaphylaxis, which is a constriction of the air passages and prevents the intake of oxygen at all. It is not clear what triggers 74

the attack but it happens very quickly, within seconds. Signs and symptoms of this extreme allergic reaction include difficulty breathing, pale skin, cyanosis (blue lips or fingernails), sweating, rapid pulse, syncope and cardiac arrest.

The recovery period may vary from several hours to a few days and symptoms regarding can prolong. Generally symptoms regress in a few days but rarely malaise and nausea may persist (Zelaya 2012; AktaĹ&#x; and MirasoÄ&#x;lu 2017).

Medical management Lionfish envenomation requires immediate action. Medical help should be started as soon as the injury is identified. In case of life threatening conditions, appropriate life-saving procedures should be promptly initiated in the prehospital care settings and victims later should be evaluated at the hospital for possible anaphylactic reactions and other serious conditions of the envenomation. In general, medical management can be considered in two steps, pre hospital and hospital care.

Prehospital care The injured person should be removed from the sea and transported to a dry and safe place if the incident takes place in water. The victim preferably should be kept in lying down and reassured. If possible, injured part should be raised as this can help to reduce swelling. The wound should be cleaned with warm saline or antiseptic solutions. Early rinsing of the injured area with warm water will help to flush away the foreign bodies and reduce pain intensity. Bleeding, if present, should be stopped with slight pressure. Visible spines and all other foreign bodies should be removed cautiously. Although it is rare for spines to break in the wound, protective gloves should be worn to avoid self-inoculation during spine removal.

Tweezers are handy for removing spines from the wound, but this should be done with caution as intact venom glands may discharge if pressure applied. Rings, watches, bracelet and other potential constricting items should be removed carefully before edema sets in (Resiere et al. 2016; Atkinson et al. 2006; Vetrano et al. 2002).

Pain control is the mainstay of the management. Foremost important method for pain relief is warm water immersion (Hornbeak and Auerbach 2017). Underlying mechanism of this treatment is unknown. The claim that heat-labile components of the venom would be deactivated (and so the venom) in hot water is questionable (Atkinson et al. 2006). Proteins denaturate over 50-60 0C but humans cannot tolerate water at those temperatures. In addition, it should be kept in mind that burns or scalding may occur with water at 40-45°C. Deterioration of pain when hot water immersion is suspended is a proof that proteins are not deactivated (Haddad et al. 2015). It is thought that heat application provides vasodilatation that reverses the vasoconstriction caused by the venom and pain ceases.

75

There are a few reports stating that hot application may fail to cease intense pain. Hot water immersion can be applied for 30-90 minutes and repeat several times until the pain decreases. If the location of wound is difficult for immersion, both showering and hot compress can also be preferred (Atkinson et al. 2006). Allergic and anaphylactic reactions should always be taken into account and medication with antihistamine, corticosteroid, adrenaline should be implemented rapidly if necessary. Care providers should be prepared for possible cardio pulmonary resuscitation.

Hospital care Once the patient is stabilized, transportation to a well-equipped hospital where further therapy is planned should be provided. Patients with lionfish envenomation should be hospitalized due to the possibility of delayed allergic or systemic reactions. If systemic manifestations develop, adequate treatment should be planned. There is lack of scientific research regarding lionfish envenomation.

It is widely accepted that symptoms and treatments may vary between individuals.

However, there are certain treatment algorithms that should be followed.

Descriptive analysis of case series is shown in Table 3.

The basic vital signs (temperature, pulse, blood pressure, respiration rate and rhythm, central venous pressure, pulse oximeter) should be monitored and recorded in case of deterioration. Recording of the clinical state is mandatory to monitor the treatment procedure. These records should include pulse, respiratory rate and rhythm, blood pressure, electrocardiogram, lung function test, urine output, arterial gases and acid-base balance of the blood (Edmonds 2002; Diaz 2015).

Radiological examinations like soft-tissue X-ray, ultrasound as well as magnetic resonance can be used to disclose bone injury, retained foreign objects or integument of the spine. For serious and extensive lesions, radiological evaluation may help to assess significant tissue damage and necrosis in the wound. In this case, surgical debridement should be performed immediately (Edmonds 2002). If spines or foreign materials are embedded in tissue, surgical removal is a must (Hornbeak and Auerbach 2017). Puncture wound is seen with local edema, mild ecchymosis at the lateral site of the middle finger by sting of lionfish in Figure 1.

Moreover, the radiological imaging of the left hand of the patient shows the spine of fish which was embedded in the soft tissue close to the distal interphalangeal joint in Figure 2.

76

77

1

1

Badillo et al. 2011

33

Alfredi et al. 1996

Vetrano et al. 2002

Number of cases 23

Reference Year Trestrail et al. 1989

Aquarium

Aquarium

Aquarium

Aquarium

Origin

Hand

Hand

Hand

Envenomation sites Hand finger

Pain Edema Bullous lesion Pain

Pain Redness Swelling

Major symptoms Pain Redness Swelling Bleeding

Paralysis of all extremities Hypertension Tachycardia Numbness of both hands

Nausea Dizziness Paresthesias

Nausea Numbness Joint pain Anxiety Headache Disorientation Dizziness Speech impairement (disarthria) Jaw tightness

Systemic signs & findings

Hot water immersion Supportive treatmant

Hot water immersion Supportive treatmant Tetanus vaccination Topical antibiotics Analgesics Bleed out poison Ice water Hot water immersion Analgesic

Hot water immersion Analgesics Antibiotics Tetanus vaccination

Treatments

Table 3. Descriptive analysis of case series of lionfish envenomation

Improvement

Improvement

Improvement

Clinical outcome Improvement

78

15

1

117

Haddad et al. 2015

Schult et al.

2017

Resiere et al. 2016

No information

Aquarium

Aquarium

Upper or lower limb

Forearm

Hand, finger

Pain Erythema Bleeding Edema Puncture wound Pain Redness Swelling

Pain Erythema Edema

Paresthesia Abdominal cramps Extensive edema Tachycardia Skin rash Gastrointestinal symptoms Fainting Transient weakness Hyper/hypotension Hyperthermia Bradicardia Hypophosphatemia

Behavioral changes Sweating Restlessness Nausea Vomiting Diaphoresis Urticaria

Table 3. Continued

Hot water immersion Analgesic Antibiotics Tetanus vaccination

Hot water immersion Analgesics Tetanus vaccination

Hot water immersion Analgesics Antibiotics

Improvement

Improvement

Improvement

Figure 1. Sting site by lionfish, a month after envenomation. Puncture wound is seen with local edema, mild ecchymosis at the lateral site of the middle finger.

Figure 2. Radiologic imaging of the left hand of the patient. The spine of fish was embedded in the soft tissue close to the distal interphalangeal joint.

79

Systemic antibiotics may be recommended if secondary soft tissue infections develop. Antibiotherapy should be planned according to culture-sensitivity tests when there is a wound to collect a culture specimen. In this case, microbiology laboratories should be informed in advance about the possible agents since special procedures are necessary for marine based microorganisms. If empirical therapy is to be given, distinctive properties of these microbes should be considered.

Prophylactic use is not recommended unless the injured person has immunodeficiency disorder (Diaz 2014; Diaz and Lopez 2015).

Systemic analgesics and narcotics are rarely indicated as hot water immersion may help to provide pain relief. Clostridium tetani can exist in coastal shorelines and tidal waters although it is known to be soil based. Therefore, tetanus prophylaxis is recommended for all patients who have encountered traumatic marine injury and is unsure about previous immunization (Diaz 2014; Diaz and Lopez 2015).

Although very rare, health care providers should be prepared for resuscitation (including endotracheal intubation, external cardiac massage, and defibrillation) as allergic reactions, convulsions, cardiovascular shock and as well as respiratory arrest requiring assisted ventilation may develop.

There is no specific antivenom for lionfish envenomation. Stonefish antivenom has been shown to cross-react with lionfish venom but it is rarely indicated since lionfish envenomation is milder and usually responds to conventional treatments.

Antivenom is rarely indicated for lionfish unless symptoms are persistent and unresponsive to hot water immersion as well as adjunctive treatments (Diaz 2015).

Divers also can be injured by lionfish during the dive and it may not easy to deal with the accident. Although basic management is the same, some specific actions may be necessary for underwater accidents. Some recommendations for divers are listed.

1. Remaining calm is important. Alert your dive partner and terminate your dive as soon as possible.

2. Ascend slowly, complying with all decompression stops, and come to the surface immediately.

3. Monitor vital signs such as circulation, airway and breathing.

4. Rinse the wound with clean water or warm saline solution.

5. Immerse the wound in heated, non-scalding water (42-45 °C) from 30 to 90 minutes. Please remember that warm application is effective for only pain relief.

6. Go to a health care center if there is one in close proximity or call emergency hotline 112 (in Turkey) as soon as possible and ask for help from a marine injury specialist who will coordinate the medical procedures necessary for a lionfish envenomation.

80

7. If you are far from a medical center, you could take medication such as antihistaminic and analgesic during transportation to the health care center. This immediate care can reduce the damage to the affected part of the body.

8. You can get additional information and help by calling emergency hotlines in other countries. Once the victim has received the first aid and emergency treatment please contact Turkish Marine Research Foundation (TUDAV) (Email: tudav@tudav.org, Phone: +90 216 424 07 72) for the record.

Prevention The best prevention is not to touch a lionfish even with gloves. It is clearly stated that neoprene gloves, booties and soles are not fully protective in case of touching the fish (AktaĹ&#x; and MirasoÄ&#x;lu 2017). Thick-soled shoes should be worn when entering or leaving in potential areas, and extreme care must be taken when swimming on coral reefs.

When considered generally, the main step in prevention is creating awareness and training. People who can encounter the fish and are at risk (like local fishermen) should be informed about the physical appearance of lionfish, how to handle one, and the fact that fish remains to be venomous for about 48 hours after its death (Resiere et al. 2016). Therefore, holding the fish with bare hands should be avoided and spines should be cut in the proper way immediately after fishing. In the long term, lionfish population control gains importance. Awareness should be raised about over population and solutions should be developed to make lionfish economically significant. Use of venom in medicine can be provided by pharmaceutical industry.

Conclusively, envenomation by lionfish as well as scorpionfish and other exotic animals, can rapidly lead to incapacitating and life-threating complications so health care providers should be trained to manage these injuries. Due to the limited available information regarding envenomation by sea animals, the scientific institutions should share their experience and prepare action plans to record and track these injuries in a yearly period. Involved partners should develop and implement warning mechanisms by means of coordination of scientific research and fruitful collaboration. Nevertheless, since these are infrequent intoxications, the physicians are strongly recommended to consult with the National Poison Control Center by calling 114 and Turkish Marine Research Foundation (TUDAV).

81

Recommendations 

If you see a lionfish in the wild, just admire it from a safe distance.



Do not try to capture this fish.



Do not grab, touch or step on it when diving, swimming, or snorkelling.



Wear protective gloves or clothes that cover all exposed skin.



Please be calm and tell your accompanier that you are stung by the lionfish in case of accident.



Be aware of life-threatening envenomation may occur. First aid, urgent transportation and cardiopulmonary support may be needed.



Tetanus prophylaxis is must in all cases.



Recovery can take place slowly and in a long time, so victims should be followed up.

Case report A 14-year old boy was admitted to hospital with severe pain, numbness, pallor and bleeding complaints and with a puncture wound on his right hand. He was on a sailing boat with his father and accidently stung by lionfish after holding a speargun with a lionfish. The lionfish slid down from the top of harpoon and the boy accidentally touched to the spine of the fish. His complaints were severe pain and puncture wound on the 2nd finger of his right hand. The pain intensified in minutes and he immersed his hand into hot water for 20 minutes to relieve the pain. However, as the water-cooled the pain intensified again. After the boy was admitted to the emergency department at the hospital, physicians were sceptic about the lionfish envenomation and they misdiagnosed as snakebite. The family called us to confirm the diagnosis of lionfish envenomation. His complaints were erythema, edema and blister/bulla formation at the dorsum of the index finger (Figures 3, 4, 5). He was treated with hot water immersion, antibiotic, painkillers, antihistamine drug, wound care and he was hospitalized for a week. The wound healed completely (Figure 6).

82

Figure 3. Sting site by lionfish. Puncture wound with local cyanosis, ecchymosis at the dorsum of the index finger after envenomation

Figure 4. Sting site; Grade 2 wound with bullous lesion formation at the dorsum of the index finger

83

Figure 5. Radiologic imaging of the right hand. There was no spine or foreign body in the tissue

Figure 6. The wound healed without sequela after the treatment

84

References Aktaş, Ş., Mirasoğlu, B. (2017) Lionfish envenomation: clinical aspect and management. J. Black Sea/Mediterranean Environment 23(1): 81-87.

Alfredi, B., Ericksoni, T., Limpscomb, J. (1996) Lionfish envenomations in an urban wilderness. Wilderness and Environmental Medicine 4: 291-296.

Atkinson, P.R.T., Boyle, A., Hartin, D., McAuley, D. (2006) Is hot water immersion an effective treatment for marine envenomation? Emerg Med J 23(7): 503-508.

Auerbach, P.S. (1991) Marine envenomations. N Engl J Med 15: 486-493.

Badillo, R.B., Banner, W., Morris, J.A., Schaeffer, S.E. (2011) A case study of lionfish sting-induced paralysis. Aquaculture, Aquarium, Conservation & Legislation 5(1): 1-3.

Bariche, M., Kleitou, P., Kalogirou, S., Bernardi, G. (2017) Genetics reveal the identity and origin of the lionfish invasion in the Mediterranean Sea. Available at: www. nature.com/scientificreports/7:6782/ (accessed 20 Sep. 2018) doi: 10.1038/s41598-017-07326-1.

Church, J.E., Hodgson, W.C. (2002) Adrenergic and cholinergic activity contributes to the cardiovascular effects of lionfish (Pterois volitans) venom.

Toxicon 40: 787-779.

Church, J.E., Moldrich, R.X., Beart, P.M., Hodgson, W.C. (2003) Modulation of intracellular Ca+2 levels by Scorpaenidae venoms. Toxicon 41: 679-689.

Cohen, A.S., Oleg, A.J. (1989) An extract of lionfish (Pterois volitans) spine tissue contains acetylcholine and a toxin that affects neuromuscular transmission.

Toxicon 27:1367-1376.

Courtenay, W.R. (1995) Marine fish introductions in southeastern Florida.

American Fisheries Society Introduced Fish Section Newsletter 14(1): 2-3.

De Haro, L., Pommier, P. (2003) Envenomation: a real risk of keeping exotic house pets. Vet Hum Toxicol 45(4): 214-6.

Diaz, J.H. (2014) Skin and soft tissue infections following marine injuries and exposures in travellers. J Travel Med 21(3): 207-213.

Diaz, J.H. (2015) Marine Scorpaenidae envenomation in travelers: Epidemiology, management, and prevention. J Travel Med 22(4): 251-258.

85

Diaz, J.H., Lopez, F.A. (2015) Skin, soft tissue and systemic bacterial infections following aquatic injuries and exposures. Am J Med Sci 349(3): 269-275.

Edmonds, C. (2002) Venomous marine animals. In: Diving and Subaquatic Medicine, Fourth Edition. (eds., Edmonds, C. Lowry, C., Pennefather, J., Walker, R.) Edward Arnold, London, pp. 335-351.

Forrester, M.B. (2008) Pattern of lionfish envenomations reported to Texas poison control centers, 1998-2006. Toxicological & Environmental Chemistry 90(2): 385-391.

Garyfallou, G.T., Madden, J.F. (1996) Lionfish envenomation. Ann Emerg Med 28(4): 456-7.

Golani, D., Sonin, O. (1992) New records of the Red Sea fishes, Pterois miles (Scorpaenidae) and Pteragogus pelycus (Labridae) from the eastern Mediterranean Sea. Jpn J Ichthyol 39(2): 167-169.

Haddad, V.Jr., Stolf, H.O., Risk, J.Y., França, F.O., Cardoso, J.L. (2015) Report of 15 injuries caused by lionfish (Pterois volitans) in aquarist in Brazil: a critical assessment of the severity of envenomations. J Venom Anim Toxins Incl Trop Dis 21: 8 doi: 10.1186/s40409-015-0007-x.

Hornbeak, K.B., Auerbach, P.S. (2017) Marine envenomation. Emerg Med Clin N Am 35: 321-337.

Fernandez, I., Valladolid, G., Varon, J., Sternbach G. (2011) Encounters with venomous sea-life. The Journal of Emergency Medicine 40 (1):103-112.

Jung Hanss, T., Bodio, M. (2006) Medically important venomous animals: Biology, prevention, first aid, and clinical management. Clinical Infectious Diseases 43: 1309-1317.

Kizer, K.W., McKinney, H.E., Auerbach, P.S. (1985) Scorpaenidae envenomation. A five- year poison center experience. JAMA 253(6): 807-10.

Maclsaac, H.J., De Roy, E.M., Leung, B., Grgicak-Mannion, A., Ruiz, G.M. (2016) Possible ballast water transfer of lionfish to the eastern Pacific Ocean.

PLos One 11: e0165584.

Por, F.D. (1971) One hundred years of the Suez Canal-a century of Lessepsian migration: Retrospects and viewpoints. Syst Zool 20(2): 138-195.

Resiere, D., Cerland, L., De Haro, L., Valentino, R., Criquet-Hayot, A., Chabartier, C., Kaidomar, S., Brouste, Y., MĂŠgarbane, B., Mehdaoui, H. (2016) 86

Envenomation by the invasive Pterois volitans species (lionfish) in the French West Indies--a two-year prospective study in Martinique. Clin Toxicol (Phila) 54(4): 313-318.

Ruiz-Carus, R., Matheson, R.E., Roberts, D.E., Whitfield, P.E. (2006) The western Pasific red lionfish, Pterois volitans (Scorpaenidae), in Florida: Evidence for reproduction and parasitism in the first exotic marine fish established in state waters. Biological Conservation 128: 384-390.

Schmitt, C., de Haro, L. (2013) Clinical marine toxicology: A European perspective for clinical toxicologists and poison centers. Toxins 5: 1343-1352.

Schult, R.F, Acquisto, N.M., Stair, C.K. Wiegand, T.J. (2017) A case of lionfish envenomation presenting to an inland emergency department. Case Reports in Emergency Medicine doi: 10.1155/2017/5893563.

Trestrail, J.H., al-Mahasneh, Q.M. (1989) Lionfish string experiences of an inland poison center: a retrospective study of 23 cases. Vet Hum Toxicol 31(2): 173-175.

Turan, C., Ergüden, D., Gürlek, M., Yağlıoğlu, D., Uyan, A., Uygur, N. (2014) First record of the Indo-Pacific lionfish Pterois miles (Bennett, 1828) (Osteichthyes: Scorpaenidae) for the Turkish marine waters. J Black Sea/Medit Environ 20(2): 158˗163.

Turan, C., Öztürk, B. (2015) First record of the lionfish Pterois miles (Bennett 1828) from the Aegean Sea. J Black Sea/Medit Environ 21(3): 334˗338.

Vetrano, S.J., Lebowitz, J.B., Marcus, S. (2002) Lionfish envenomation. J Emerg Med 23(4): 379-382.

Zelaya, M.A.M. (2012) Toxic effects and management of injuries caused by the lion fish (Pterois volitans, P. miles). Rev Fac Cienc Méd 9-17.

Zenetos, A., Gofas, S., Morri, C., Rosso, A., Violanti, D., Garcia Raso, J.E., Çınar, M.E., Almogi-Labin, A., Ates, A.S., Azzurro, E., Ballesteros, E., Bianchi, C.N., Bilecenoğlu, M., Gambi, M.C., Giangrande, A., Gravili, C., HyamsKaphzan, O., Karachle, P.K., Katsanevakis, S., Lipej, L., Mastrototaro, F., Mineur, F., Pancucci-Papadopoulou, M.A., Ramos Espla, A., Salas, C., San Martin, G., Sfriso, A., Streftaris, N., Verlaque, M. (2012) Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trenda and pathways. Mediterr Mar Sci 13: 328-352.

87

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

Marine aquariums and lionfish trade in Turkey Zeynep GÜLENÇ Turkish Marine Research Foundation (TUDAV), P.O. Box: 10, Beykoz, Istanbul, TURKEY Corresponding author: zeynepgulenc@hotmail.com

Introduction Public aquariums are creating artificial environments that are mimicking the actual habitats of aquatic creatures. This activity has attracted a great deal of audience worldwide as well as in Turkey. With a commercialized perspective, these aquariums focus only on the species that they think will attract attention and are visually rich. The lionfishes (Pterois miles, Pterois volitans), classified as invasive species, have taken a place in the aforementioned aquariums, due to their attractive appearances.

The displaying of freshwater fishes in glass aquariums in a modern sense began in the 19th century England and Germany. Following the Second World War, the freshwater aquarium industry has developed rapidly in parallel with the air transport industry, but the interest in marine aquariums did not start to increase before 1990 (Türkmen and Aktuğ 2011). Turkey's interest in the marine aquarium began particularly in the early 2000s and displayed a gradual increasing. The income from marine aquariums in Turkey was approximately $3,500,000 in 2011 (Gültekin et al. 2014).

The marine fish invasions can occur via several methods including but not limited to: natural range extensions, deliberate introductions in order to improve fisheries, fish movements through canals, ballast water transportation, and aquarium or aquaculture releases, either intentional or unintentional (Hare and Whitfield 2003). Semmens et al. (2004) pointed out a substantial threat to the coastal ecosystems and presented an opportunity rarely seen for proactive management of marine-species introductions, under the condition where managers and scientists act with haste.

The presence and likely establishment of the lionfish P. volitans of Indo-Pacific origin in the Atlantic seaboard was documented by Whitfield et al. (2002). The assumption is that the marine aquarium trade was the source of the introduction.

Lionfish are now found in West Atlantic waters, where they are one of the many species of non-native aquarium fish (Padilla and Williams 2004). Randall (1987) noted that aquarium releases have been identified as the probable source of marine fish introductions before, it is the first time that the likely source of a successfully

88

established non-native marine fish have been identified as aquarium releases (Semmens et al. 2004).

Aquarium species, on the other hand, are large and generally traded as adults, which gives them a greater probability of surviving to reproduce (Padilla and Williams 2004). The aquarium or ornamental species are a third of the worldâ&#x20AC;&#x2122;s worst aquatic invasive species (Padilla and Williams 2004). When released, they displace and prey on native species, carry pathogens, block waterways, while others are seen as considerable agricultural pests, and some of them are a direct danger to humans, like the lionfish.

The lionfish species Pterois miles (Bennett, 1828) and Pterois volitans (Linnaeus, 1758) of Indo-Pacific origin, are the Lesepsian species which settled in the Mediterranean through the Suez Canal and considered the most successful invasive species in the history of aquatic invasion (Bariche et al. 2013). The review of the recent development of lionfish trade in Turkish aquariums may help to better understand the introduction of this fish to the Turkish seas. The aim of this study is to collect and present the information regarding living conditions of the lionfish in the aquariums and its trade in Turkey.

Materials and methods In this study, aquariums located in Istanbul and outside of Istanbul were visited and interviewed (Figure 1).

Figure 1. Location of interviewed aquariums

89

On some occasions they were reached via mail and telephone. Written and verbal information about lionfish were obtained through asurvey consisting of eleven question. The questions were open-ended questions focused on understanding the possible effects of lionfish keeping. The authorities that were contacted were asked questions about the supplying process of lionfish to aquariums, permitting procedures for the supplying process and living conditions of the lionfish in aquariums (Table 1).

Table 1. Questions given to the attendees No. 1 2 3 4 5 6 7 8 9 10 11

Questions Are there any lionfish in your aquarium? If yes, how many individuals?

How many years have you had lionfish in your aquarium? Have you observed any decrease or increase in the number of individuals? What is the increase or decrease rate?

Where do you supply lionfish?

What is the permission procedure?

Is lionfish among the favourite animals in your aquarium? Does it attract visitors? Why? What are the favourite species in your aquarium?

What is the procedure for acquiring the lionfish to the aquarium?

What are the living conditions? (Salinity, temperature, nutrition, other species which are living together) Have you ever experienced any injuries?

What are the procedures applied to deceased individuals?

Are there any individuals who run away or released to the sea from your aquarium?

What is the cost of acquiring the lionfish for the aquarium? (taxation, customs, expenses etc.)

Results and discussion A total 9 aquariums, four in Istanbul, and the rest in other parts of Turkey such as Ankara, Antalya, Bursa, EskiĹ&#x;ehir and DiyarbakÄąr have been investigated. The aquariums where the questions are asked and the number of lionfish individuals are shown in Table 2.

Although the aquariums provide optimum conditions for the survival of animals, their natural cycles such as reproduction are interrupted due to the use of synthetic water and reproductive potential of animals is very low as their natural habitat is reef ecosystem. As a result of the questionnaire, no increase was observed in the number of individuals in any aquarium.

90

Table 2. Interviewed aquariums, –There is no lionfish Name of Aquariums

Sea Life Istanbul Istanbul Aquarium Emaar Aquarium ViaSea Aquarium Aqua Vega Aquarium Antalya Aquarium ETI Underwater World Bursa Tunnel Aquarium Aqua Diyarbakır Total

Private/ Public

Province

Number of lionfish (P. miles/ P. volitans)

Private Private Private Private Private Private Public Public Private

Istanbul Istanbul Istanbul İstanbul Ankara Antalya Eskişehir Bursa Diyarbakır

20 3 15 7 13 8 66

The lionfish are quite durable and there are not many casualties in aquariums.

Antalya aquarium informed that they report max. 1 individual loss in a year. As for Sea Life Aquarium, they informed that the cause of the individual losses were varied. They experienced individual losses due to the following causes; lionfish could not adapt the bait when they come to aquariums in the early period, environmental and systematic problems (such as the inaccurate water temperature adjustment or accidental supplement of freshwater) and the fish were infected with Cryptocaryon irritans which is holotrichous ciliate parasite of marine fishes (Colorni and Bugers 1997). Cryptocaryon irritans is among the main marine fish diseases and observed in sea bass (Dicentrarchus labrax) and sea bream (Sparus aurata) in Turkish seas (Çağırgan 2009). On the other side, ViaSea Aquarium had 3 individual losses since 2016. One of the individuals loss was caused by a combat with another lionfish, the other individual death was due to an undetermined problem in its air bladder. As for the third individual’s loss, it was caused by copper exposure. In ViaSea Aquarium, 0,1 ppm of copper is added to the tanks once a week to prevent the growth of Cyrptocaryon irritans. If the fish is close to pump during the copper intake, it is intensely exposed to copper. As a result of this exposure, symptoms such as the loss of coordination, whirling around, respiration through water surface and jumping out of water were observed. This was the reason for loss of the third lionfish in the aquarium.

The origin of a large part of marine aquarium livestock is found in tropical oceans in the archipelago of Indonesia, the Philippines, Sri Lanka, the Maldives and the Central Pacific Islands (e.g., Hawaii). Importation of the other species are made from the Caribbean (e.g., Puerto Rico) and the Red Sea region (Livengood and Chapman 2007). As for supplying of lionfish the aquariums in Turkey who reported that they supply it either through direct importation or companies that import from Indonesia and Kenya. Additionally, recently aquariums started to exhibit the lionfish caught in the southeast part of Turkey.

91

It is also noted that in the procedures of supplying the lionfish, there is no need for permission to exhibit the lionfish in the aquariums since the lionfish is not subject to CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora). The Ministry of Agriculture and Forestry of Turkey requires the pro-forma invoice and the filled out health certificate for the import permission. Since the packages carrying the lionfishes are taxed according to their weight, the lionfishes are packed in the plastic bags or transparent containers filled with sufficient amount of water and oxygen, but they are impenetrable by their spines. On the plastic bags that contain lionfish, amount and species of the fishes (Pterois volitans/ Pterois miles) are written which is called packing list.

For each fish, veterinary approved entry certificate, pro-forma and commercial invoice, customs declaration and freight invoice have to be submitted to the customs office of the country of importation. Following the exit permit, the importer will have the permission to import the lionfish through customs office.

After the customs control, the veterinarian confirms the amount of the animals and the number of bags. If the lionfish survives the 21 days of quarantine, the process will be completed and the animal will be legally aquarium's fish.

After passing through customs, the lionfish preferably between 5-7 cm (small individual) will packed in bags with minimum amount of water so as not to increase the import tax. Then the bags are placed in the ice filled styrofoam and they are brought in the aquarium preferably with the refrigerated vehicle.

Afterwards, the bags would be checked to confirm the species, amount of the fish, individual losses and would be reported to the exporter company.

Before the shipment, the loading parameters of the animals would be requested from the exporter. According to these parameters, the tanks in which the animals will be kept in quarantine would be prepared. The bags which contain the animals that are unfed for 48-72 hours with ammonia remover supplement, would go through the measurements of salinity, temperature and pH. As the pH can reduce from 8 to 2-4 values during the shipment, re-adjustments of the parameter are made in the tanks. Once the differences of parameters between the quarantine and the adaptation tanks equalize, then the fish would be moved to quarantine tank with the help of a suitable rubber scoop. Quarantine is a process that is applied to the tank to prevent infections, to get the animals to eat and to grow in case the fish is small (Table 3). The duration of quarantine, medications and dosages differ depending on species, and usually it takes a month. After the quarantine process is completed, the fish is taken to the tank where it will be exhibited.

92

Table 3. The treatment process of the Sea Life aquarium on lionfish during the quarantine period. Formaldehyde is used for bacterial infections, fungi and parasites.

Copper, to increase the resistance of the organism and to prevent the growth of microorganisms. As for Flukesolve, it's used for internal parasites.

Day 1 Day 2 Day 3 Day 6 Day 10 Day 21*

Fish arrives Formalin bath 0.5ml/l (of formaldehyde 35-40%) or 0.6ml/l (of formaldeyde 30%) for 6 hours, at least 50% water changes after treatment Start bringing up copper over 3 days to 0.15ml/l, Flukesolve bath at 1g/250l for 24 hours (of Cestocur at 1ml/25l), at least 50% water changes at end of the treatment, maintain copper level during this treatment Full strength copper for 21 days Flukesolve bath at 1g/250l for 24 hours (or Cestocur at 1ml/25l), at least 50% waterchange at end of treatment, maintain copper levels during this treatment Flukesolve bath at 1g/250l for 24 hours (or Cestocurat 1ml/25l) at least 50% water change at end of treatment

*Day 21 or day before going onto display

Aquariums tend to have a commercial perspective, in order to attract more customers in which they endeavour to make customer-oriented advertising. The Lionfish attracts the attention of people as a result of their rich visuality with vivid colours, long pectoral fins, and venomous spines, nevertheless they are not particularly in demand as a species. When they are exhibited alone as poisonous fish, people are more interested in them. There are also people who know the fact that they are a lessepsian and poisonous species, and they especially want to see them. Among all the species that are exhibited in aquariums, sharks, octopus, crabs and starfish are the centre of the attention.

When living conditions are considered, they are kept at a range of 30-39 â&#x20AC;° salinity, 24-26 °C temperature, and at a pH value of 8. They feed on frozen bait such as shrimps, mussels, whitings, mackerels, silverfish and squids. It's reported that frozen food is preferred because of the absence of parasites. When the fish caught in the wild first come to the aquarium, they do not want to consume the frozen bait because they are accustomed to eat live bait, as a result, in the adaptation process, they are first given live bait and then gradually get familiarized with the frozen bait. During the familiarization process, the end of a stick is fitted with a bait, and this bait is moved in the water in order to allow the fish to eat it. Duration of the process of getting accustomed to the frozen bait varies between 2 days and 1 week.

Because the more you feed the lionfish, the more they eat, so they are fed on regular intervals in order to give their gastrointestinal tract the opportunity to rest.

For example, in ViaSea Aquarium, the fish are fed 5% of their body mass for 3 days a week, 2.5% of their body mass for another 3 days, and followed by no feeding on Sundays. The adult individuals in Sea Life Aquarium (Figure 2) on the other hand, are fed two to three times a week, according to their condition. The 93

reason behind this treatment is to prevent the accumulation fat on the liver tissue of the animal.

Figure 2. Pterois volitans in the Sea Life Aquarium (by Barış Gül)

Whereas in the nature, the effects of Cryptocaryon irritans are rare due to the low density of its hosts, however in the aquarium environments this parasite can overwhelm the whole fish population of the aquarium. Invasion of the skin, eyes and gills, and also impairing the physiological function of these organs are the effects of this parasite (Colorni and Bugers 1997). Lionfishes are also susceptible to C. irritans. In case of C. irritans infection, hyposalinity therapy is applied by aquariums. Salinity is reduced to 14-16 ppm, and the duration varies depending on the expiration of the parasite, but it generally lasts for 2 weeks.

Lionfish captured from the natural habitat can attack the smaller fish in tank that they are located because they cannot suppress their hunting instinct. That is why they are sharing the same tank with their own size group so they cannot prey on them, or they are exhibited alone. While in Sea Life Aquarium, lionfish lives with Cromileptes altivelis, Grammistes sexlineatus, Echidna nebulosa, Gymnothorax fimbriatus, Gymnothorax thyrsoideus, Siganus vulpinus, Scuticaria tigrina; in ViaSea Aquarium, it lives with Acanthurus sohal, Chaetodon falcula, Chaetodon semilarvatus, Pomacentrus sulfureus, Zebrasoma xanthurum, Dascyllus aruanus. In Aqua Diyarbakır Aquarium, lionfish lives with Gymnomuraena zebra and Balistoides conspicillum and in Emaar Aquarium it lives with Taeniura lymma. (Figure 3) Finally, lionfish is exhibited alone in Antalya and İstanbul Aquarium. According to the Sea Life Aquarium, lionfish 94

can live together with Labroides dimidiatus (cleaner wrasse) in a mutualistic relationship which is a species that could be eaten by lionfish depending on its size. Cleaner wrasse can feed on the parasites on lionfish skin and gills and that way lionfish can get rid of its own parasites. Another information on the relationship of cleaner wrasse and lionfish is that if the cleaner wrasses are released into the tank directly then the lionfish would prey on them. However, if the cleaner wrasses are released slowly into tank while the lionfish is fed at the same time, the lionfish would not prey on cleaner wrasses.

Figure 3. Exhibition tank and information board of lionfish in Emaar Aquarium (by Fulya Güçlüer)

Interviewed aquariums reported that they had not reported an injury incident until now. In addition, it was reported that ViaSea Aquarium made their employees sign a document titled “Safe Working Practice and Maintenance Protocol for Lionfish” (Figure 4).

95

Figure 4. Safe working practice and maintenance protocol for lion fish from ViaSea Aquarium

According to the Antalya Aquarium, after the autopsy of the deceased individuals are photographed, a deceased individual report is prepared. After that, the record of the mentioned deceased individual would be taken out from the list of "alive individual species" and from the list of "species and alive individuals of the other forms" which would be given to the zoo every year. The individual loss would be recorded in the deceased individual list which is again given to the zoo from time to time. The deceased individuals are taken by the company after being stored in the medical waste area by providing the necessary conditions. In Emaar Aquarium, big fish are sent to Istanbul University, Faculty of Veterinary Medicine for an autopsy and after the autopsy they are incinerated. Autopsy results are reported to the aquarium as a report. Small fish are bagged and thrown in the refrigerated waste container. As lionfish is not subject to CITES, they do not need to be notified to the Ministry of Agriculture and Forestry when they decease. ViaSea Aquarium stated that it is mandatory to obtain skin residue and gill sample from the deceased individuals. If the size of the animal is greater than 20 cm, necropsy is performed. The size of the gonad, the macroscopic structure of the stomach and intestine wall, the fat rate of the liver and the color of the bile are examined. If the fish is smaller than 20 cm, skin and gill sample is taken for external parasites and fecal froti samples are taken for internal parasites. In Sea Life aquarium, if the animal died for no identified reason, their organs are fixed with formaldehyde and sent abroad. Based on the report after the pathological examinations, other animals in the tank are examined and treated. If the cause of

96

the death of the fish is clear, it would be reported and the animal would be properly disposed.

Interviewed aquariums stated that no lionfish of their own would be released to the sea and a situation such as an escape was impossible. Emaar Aquarium and the Sea Life Aquarium gave some animals the rehabilitation treatment and then released them to the sea, but the lionfish was not subject to it.

ViaSea Aquarium reported that the lionfish cost them around 63 USD with 18 USD fee of an individual and the 45 USD of freight cost. On the other hand, Sea Life Aquarium reported that a lionfish of 15-20 cm (XL individual) was about 10 USD in 2018. As fish comes in at least 5 liters of water, the additional cost, excluding the cost of fish, would be 16-17 USD with tax included. Additionally, Okyanus Aquarium reported that in the recent years, some suppliers caught the lionfish at a cost of 250 Turkish Liras (44 USD) as of 2018. And also they said that the cost of the packages containing lionfish, including taxes from abroad, is about approximately 400 USD. It is reported that the packages can optionally contain a small amount of large size lionfish or large amount of small size lionfish.

Discussion As a result, lionfish are exhibited in aquariums due to their attractive morphological features, poisonous spines and high tolerance to variable environmental conditions. In August 1992, after the damage of the Hurricane Andrew to a large sea-side aquarium which was at the Biscayne Bay of Florida, six alive specimen of lionfish were spotted few days later. Hence, this incident is widely accepted as the beginning of the introduction of lionfish into the Atlantic coast of mainland USA (Schofield 2009; Ocean Health Index 2012).

For the moment, Florida is the only place to prohibit the importing of lionfish (Farquhar 2017). On 18 June 2014, a number of measurements was approved by The Florida Fish and Wildlife Conservation Commission (FWC) to combat invasive lionfish which also included ban on importation of lionfish for aquariums and other purposes. These regulations include; afore-mentioned ban on importing lionfish, permission to harvest lionfish with a rebreather when diving and allowing participants to spear lionfish or other invasive species during the organized tournaments and events where spearfishing is not allowed. According to the spokesperson of FWC, any person can have lionfish in their aquariums however this lionfish has to come from Florida waters (Pillion 2014). If we consider to apply this importing ban, it can be helpful to control and monitor the present population of lionfish in Turkish waters.

Even though interviewed aquariums does not consider the possibility of lionfish being released to the sea, activities of public aquariums and also the individuals who looks after lionfish as hobby should be tracked. After all, people can take 97

lionfish into their aquariums without any approval certificate or any tracking record which could mean there is a high chance of them intentionally or unintentionally releasing the lionfish into the sea. With the conduct of the species monitoring activities, it is necessary to identify the invasive species, to take into account of the damages they cause or could cause. And it's also necessary to monitor the lionfish after its procurement to keep the population in control.

Lionfish which is known as a lessepsian species and also known as destructive for the natural ecosystem had spread in Turkish seas. Reducing the tariffs on the exportation of lionfish and public awareness is important about lionfish could be one of the way to mitigate negative impacts of its population in Turkish seas.

Acknowledgement I would like to thank Prof. Bayram Öztürk to encourage me to write this paper and also aquarium’s authorities which provided me information about lionfish.

References Bariche, M., Torres, M., Azurro, E. (2013), The presence of the invasive lionfish Pterois miles in Mediterranean Sea. Mediterranean Marine Science 14(2): 292294.

Colorni, A., Burgess, P. (1997) Cryptocaryon irritans Brown 1951, The cause of ‘white spot disease’ in marine fish: an update. Aquarium Sciences and Conservation 1: 217-238. Çağırgan, H. (2009) The use of veterinary drugs and vaccines in Turkey. Options Méditerranéennes, Série A, Séminaires Méditerranéens (86): 29-34.

Farquhar, S.D. (2017) Back to the Source: Lionfish imported into the United States via the ornamental aquarium trade. Journal of Environment and Ecology 8(2): 23-31.

Gültekin, K. B., Karadal, O., Türkmen, G., Özaydın, O. (2014) The marine fish species belongs to Turkish fauna exhibited in public aquariums. Ege J Fish Aqua Sci 31(3): 127-132.

Hare, J.A., Whitfield, P.E. (2003) An integrated assessment of the introduction of lionfish (Pterois volitans/miles complex) to the western Atlantic Ocean. NOAA Technical Memorandum NOS NCCOS 2. pp. 21.

Livengood, E.J., Chapman, F.A. (2007) The ornamental fish trade: An introduction with perspectives for responsible aquarium fish ownership Department of Fisheries and Aquatic Sciences, Institute of Food and Agricultural Sciences: University of Florida, Publication FA124.

98

Ocean Health Index (2012) The invasion of the lionfish. Available at http://www.oceanhealthindex.org/news/StoriesInvasion_of_the_Lionfish (accessed 29 Oct. 2018) Padilla, D.K., Williams, S.L. (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in Ecology and the Environmen 2(3): 131-138.

Pillion, D. (2014) Florida bans importing live lionfish in aquarium trade, allows more spearfishing to combat invasive species.

Available at https://www.al.com/news/beaches/index.ssf/2014/06/florida_bans_importing_li ve_li.html (accessed 26 Oct. 2018).

Randall, J.E. (1987) Introductions of marine fishes to the Hawaiian Islands. Bull Mar Sci 41: 490-502.

Schofield, P.J. (2009) Geographic extent and chronology of the invasion of nonnative lionfish (Pterois volitans [Linnaeus 1758] and P. miles [Bennett 1828]) in the Western North Atlantic and Caribbean Sea. Aquatic Invasions 4(3): 473-479.

Semmens, B.X., Buhle, E.R., Salomon, A.K., Pattengill-Semmens, C.V. (2004) A hotspot of non-native marine fishes: evidence for the aquarium trade as an invasion pathway. Marine Ecology Progress Series 266: 239-244.

Türkmen, G., Aktuğ, A.M. (2011) The investigation on marine aquarium sector and imported fish species exhibiting in İzmir province. Ege J Fish Aqua Sci 20(2): 59-64.

Whitfield, P.E., Gardner, T., Vives, S.P., Gilligan M.R., Courtenay, W.R., Carleton, R., Hare, J.A. (2002) Biological invasions of the Indo- Pacific lionfish (Pterois volitans) along the Atlantic coast North America. Marine Ecology Progress Series 235: 289-297.

99

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

Lionfish and scuba diving Murat DRAMAN KASAD (Kaş Sualtı Derneği - Kaş Underwater Association) Corresponding author: murat@dragoman-turkey.com

Introduction As professional dive-centre operators, we were quite surprised, in the summer of 2014, to discover the first specimen of the lionfish Pterois miles (Figure 1), in Kaş-Kekova Marine Protected Area. One single specimen was observed on a single dive site. This was quite an attraction for divers: dive guides, when on this site, would look for this animal specifically to show it to divers, who were amazed by this very unusual discovery. A new, beautiful fish, that would always stay around the same rock and would hardly get away from divers when approached: a novel attraction.

Figure 1. Pterois miles by Murat Draman - The Diving Guide: Kaş

100

Being in Eastern Mediterranean, in southern Turkey, not too far from the Suez Canal, we were quite used to sighting new species arriving from the Red Sea: the area is greatly affected by the ”Lessepsian migration”. We had so far observed the desertifying effect of rabbit-fishes Siganus luridus and Siganus rivulatus on the local flora. They have been present in the region for as far as local fishermen can remember and have become the dominant herbivore fish species in the area.

They consume the algae and grass cover relentlessly above the thermocline.

Water temperatures rising and the thermocline going deeper, their effect is devastating. The minuscule but overwhelming seashells Ceritium scabridum and crowned sea-urchins Diadema setosum scrape the surface of shallow rocks for the remaining traces of algae. On the other hand, elusive silverside toadfishes Lagocephalus sceleratus do excessive damage on the fishermen’s takes and small but omnipresent and stubborn Torquigener flavimaculosus are on the constant search for small crustaceans on the sandy bottom (Draman 2016).

Being used to all these new arrivals, the lionfish seemed like another predator that would share the resources of the sea. Still, knowing the fate of the Caribbean under the lionfish invasion, and the exceptional reproduction behaviour of the fish (a capacity of 4-30,000 eggs every 4 days, for more than 2,000,000 eggs a year) (Brylske 2018), we were quite nervous.

While warnings about the need of eradication by trained professionals went unheard or faced resistance by some divers (“impossible to stop the invasion, should not stop the course of nature, should not intervene nor kill animals” etc.).

Their numbers kept on increasing: from a few individuals on some of the dive sites in 2016 and a few on each site in 2017, to 10-15 observations on each site in 2018 (Draman 2018) (Figure 2). If nothing is done, their numbers will surely increase and, the results may be much more devastating than what was experienced in the Caribbean, as the Mediterranean fauna is much less abundant.

The scientific community unanimously agrees that lionfish are a menace to the environment, but they also agree that their invasion cannot be stopped.

We already see the effects of this invasion: as of 2018, there seems to be a serious decline in Thalassoma pavo and Coris julis populations, typical small Mediterranean fish that feed on Chromis chromis damsels’ eggs among others, and as expected, there is a remarkable increase on juvenile damsels hiding in the spines of crowned sea-urchins Diadema setosum.

We predict that the increasing numbers of lionfish will affect diving activities, and some basic tourism activities such as restaurants as well, slowly but surely.

As seen in the Caribbean experience, some new activities/products emerge, associated with the lionfish. These will be discussed below.

101

Figure 2. Diver and lionfish by Veysel Kureyş

Supporting protected areas with environmental fees Studies show that tourists, that may or may not be associated with diving/snorkelling, who consider themselves to be environmentally-sensitive (60% in a survey in Cayman Islands), are willing to pay extra environmental fees, if there are enough information that these resources are used for controlling the expansion of invasive species and the conservation of biodiversity (van Beukering et al. 2014). These ratios are higher in the diver community that experiences firsthand the damage caused by the lionfish. Communication efforts could increase the support by tourists, and improve the consumption on invasive species such as the lionfish. Involving the visitors in the invasion prevention efforts could constitute a major contribution to their financing.

Lionfish diving As a positive point to enhance the diving/snorkelling industry, “lionfish diving” (Figure 3) may be available as a new activity offered to the diving tourist. A beautiful, photogenic, slow and self-confident animal, the lionfish is easy to observe. It displays its magnificent wings when it feels threatened and also when it maneuvers to block its prey. It lives at all depths from the surface to over 100m, therefore it is widely available in recreational diving depths. While its dorsal spines may deliver a potent venom, painful but usually not mortal for humans, the animal is not aggressive and a safe distance keeps the divers away easily. The fish gets used to the presence of divers and is even known to follow divers during night dives to hunt prey under their torches’ lights.

102

Divers enjoy this discovery experience and encounters become memorable moments for a diver. Potential problems are easily avoided with a standard “no touching” policy: nevertheless, dive-centres that offer this recreational dive must be properly prepared for accidents.

Figure 3. Diver and lionfish by Çagatay Arıcan

Citizen science activities The willingness of divers to participate in citizen science activities for the conservation of biodiversity and monitoring of the invasive fishes is an activity that motivates environment-conscientious divers (Carballo-Cardenas and Tobi 2016) (Figure 4). Properly guided surveys turn their dives into useful datagathering activities: this may be an additional market for the diving industry and

103

at the same time, it is costless labor that helps collect important information that is needed by scientists to monitor the health of marine ecosystems.

Figure 4. Underwater survey © www.leibniz-zmt.de/en/research/expeditions/

Lionfish hunting / removal While complete eradication seems impossible, some, including the author of this article, still believe in removal efforts’ necessity, specifically in marine protected areas (in our case the Kaş-Kekova Marine Protected Area). Our belief is in the same direction as in the final report of the “Workshop on marine invasive species management in Mediterranean MPAs” (24-26 April 2018) (IUCN Med 2018), that states: … Nonetheless, more science-based research is needed to prove these impacts and to further increase the understanding on connectivity among invasive species’ populations. This lack of knowledge, however, shouldn’t delay actions by decision makers and managers to control their populations and mitigate their effects. It is paramount that all the MPAs should therefore develop monitoring programmes in their sites to evaluate the presence of invasive species (early 104

detection), examine trends, and evaluate the impacts.

Management needs to be proactive, working not only on monitoring but also on prevention measures and on the initial stages of invasion with fast removal actions. As the knowledge on basic ecological traits of many invasive species is not sufficient (or absent), it is difficult to find or propose mitigation measures once the invasion has spread. â&#x20AC;Ś To be proactive, MPAs need to have flexibility in their conservation status and be able to change their management regime and measures to allow, for example, conducting quick removal actions within the marine protected sites. These actions should be seen as a way in achieving the objectives of the MPAs to maintain native biodiversity (with its no-take zones and social implications) and reducing as much as possible the biomass of the non-natives and their impact on the ecosystem. Protecting large native predators (e.g. groupers) could be a solution to further explore as it was suggested from observations in Turkeyâ&#x20AC;&#x2122;s MPAs. Dives for lionfish removal are very popular in the Caribbean and marketed to divers from all around the world (Figure 5). Divers are attracted by this activity, as they feel that it serves a purpose and helps preserve environments where the lionfish decimates local fish populations and drastically reduces biodiversity.

Lionfishes are voracious eaters: they suck and swallow whole, any fish that fits in their mouth. Juvenile lionfishes feed extensively on small crustaceans. Not only they decimate the reefs by eating all fish that are up to halt their size, they also finish off the food source that would normally feed local top predators, therefore also causing their disappearance (www.dive-the-world.com).

Fish removal requires the mastery of basic techniques and the use of specialised equipment that will help divers stay away from venomous spines and not to get stung. This training is quite easy and any diver with proper buoyancy control may be a candidate for this activity, but the risk of getting stung would increase: caution must be used and divers must be organised and briefed properly.

105

Figure 5. Lionfish hunting marketing on the web (by With ReefCi in Placencia, Belize)

Feeding lionfish to top predators It seemed logical to train top predator fishes (groupers, barracudas, sharks, eels, amberjacks etc.) to eat lionfish, by feeding them killed specimens, especially in environments where predators do not know them and therefore are not used to prey on them. This was common practice in the Caribbean after lionfish removal activities with spearguns and was also marketed as a recreational diving activity.

Fish feeding modifies the behaviour of these carnivorous fish as they become aggressively demanding and harassing, putting the divers in danger and often causing injury (McArthur 2016) (Figure 6). This activity was consequently abandoned in the Caribbean, going back to another standard norm in scuba diving: â&#x20AC;&#x153;do not feed marine animalsâ&#x20AC;?.

106

Figure 6. Aggressive predator behaviour when feeding Š www.forscubadivers.com/photosvideos/unintended-consequences-with-marine-lifevideo/

Offering lionfish in restaurants The lionfish venom is a protein-based neurotoxin deactivated by heat (www.scubadiving.com), and the flesh is not poisonous but tasty and fatty, very similar to that of any scorpion fish. Motivating local fishermen to catch these fishes and to sell them to restaurants could generate substantial income, and therefore compensate for the lack of other commercial fish. As the customer reaction is positive, restaurants are eager to put them in their menus. Attention must be given not to get stung by the spines while cleaning the fish, as the venom is active even if the fish is dead.

Marketing this fish to tourists in restaurants had enormous success. Lionfish recipes abound anywhere the fish is present (Figure 7). Local consumption of lionfish is starting slowly in the Mediterranean, and more and more, seafood restaurants are planning to offer them.

107

Figure 7. Lionfish cookbook Š www.scubadiving.com

Conclusion As the recreational and commercial value of lionfish is increasing, is usually ceases to be viewed as a threat (Carballo-Cardenas and Tobi 2016), but becomes a tourism asset. We should not forget that it may still present a great danger for the marine environment.

It generates additional income for local dive operations, fishermen and restaurants alike. We believe that allowing local fishermen to remove them by all means would serve both the local economy and the preservation of biodiversity in marine protected areas.

108

References Brylske, A. (2018) Lionfish invasion: The Saga Continues. Available at: https://dtmag.com/thelibrary/lionfish-invasion/ (accessed 10 Oct. 2018).

Carballo-Cardenas, E.C., Tobi, H., (2016) Citizen science regarding invasive lionfish in Dutch Caribbean MPAs: Drivers and barriers to participation. Ocean and Coastal Management 133: 114-127 Dive the world (2018) Diving with lionfish. Available at: http://www.dive-theworld.com/creatures-lionfish.php (accessed 2 Oct. 2018).

Draman, M. (2016) Red Sea in the Med. A4 Editions, İstanbul, 132 pp.

Draman, M. (2018) The Driving Guide: Kaş, Extended 3rd Edition. (www.thedivingguidekas.com). A4 Editions, İstanbul, 352 pp.

IUCN Med (2018) Workshop on marine invasive species management in Mediterranean Marine Protected Areas, April 2018 (2018) IUCN Center for Mediterranean Cooperation (IUCN Med) in cooperation with Enalia Physis Environmental Research Centre (ENALIA), Cyprus.

McArthur, D. (2016) Unintended Consequences of Lionfish Culling [video].

Available at: http://forscubadivers.com/photosvideos/unintended-consequenceswith-marine-life-video/ (accessed 9 Oct. 2018).

Scuba Diving (2016) The truth about invasive lionfish. Availavle at: www.scubadiving.com/photos/divers-guide-marine-life-lionfish (accessed 12 Oct. 2018). van Beukering, P., Brouwer, R., Schep, S., Wolfs, E., Brander, L., Ebanks-Petrie, G., Austin, T. (2014) The impact of invasive species on tourism: The case of lionfish in the Cayman Islands. (www.wolfscompany.com/wpcontent/uploads/2016/02/R14-32-Tourism-value-and-lionfish-final-report.pdf) IVM Institute for Environmental Studies, Amsterdam, pp. 53.

109

Hüseyinoğlu, M.F., Öztürk, B. (Eds.) 2018. Lionfish Invasion and Its Management in the Mediterranean Sea. Turkish Marine Research Foundation (TUDAV) Publication no: 49, Istanbul, Turkey.

Lionfish preparation for cooking in Turkey Tolga MANACIOĞLU*, Simge MANACIOĞLU Mezetaryen wine / meze (Muskat Meze Bar), Kaş, Antalya, TURKEY *Corresponding

author: dtolgamanacioglu@gmail.com

Lionfish is an invasive Lessepsian species which migrated through the Suez Canal from the Red Sea to the relatively warm waters of the Mediterrenean and recently to the Aegean Sea. Since the lionfish is a species which is not harvested commercially in great amounts or does not have many predators because of its spines, the number in our seas is increasing. Hence, to produce recipes that will add to the wide range of our gastronomy will boost the commercial value of the lionfish.

One should consider a few important points before starting to cook a lionfish.

Paying some attention to these, you can clean the lionfish without hurting yourself and encourage the consumption with the right zesting.

It is widely known that lionfish has spines on dorsal, pelvic, anal and pectoral fins and on the tail. Clipping off these spines prior to cleaning the bones, the fish can be safely and easily filleted. Good kitchen scissors or garden scissors will do the job. Holding the fish carefully, it is advised to clip the spines starting with the pectoral and dorsal fins (Figure 1).

After getting rid of spines, get a sharp fillet knife and cut deeply behind the head towards the abdomen with a 60 degree angle. Do this on each side of the fish.

What is important here is to spot the end of abdomen right and to get the cleanest fillet without damaging the internal organs of the fish. Giving these deep cuts to each side of the fish, you can start the process of filleting with the help of two small cuts on each side of the tail (Figure 2).

Another important matter is that you get rather small portions from lionfish.

Considering you can only get 160-180 gr fillets from a big lionfish, you should be cleaning at least two of them to cook a meal for two.

Apart from the cleaning tips, one should also consider the gastronomical characteristics of the lionfish in order to cook a nice fish meal. The lionfish that we obtain from the Mediterranean has very low fat and is very poor in flavor. It needs a good deal of fat and acidity for zesting although its white, soft and almost boneless fillets look very satisfactory. Flavoring aromatics, lots of butter or olive oil, and supplements that provide acidity will help you prepare delicious lionfish meals.

110

Figure 1. Clipping of venomous spines of lionfish

111

Figure 2. Preparetion of lionfish for cooking

112

Mediterranean style lionfish

Ingredients (for 2 pax) 4 lionfish fillets (around 300-350gr) 8 cherry tomatos 1 tablespoon of capers 10 olives 2 cloves of garlic 1 tea spoon red peppercorn 5 table spoons olive oil 2 table spoons white wine salt Method 1- Heat the olive oil in a pan over medium heat. Add tomatos and sauté 5 minutes.

2- Add capers, olives, sliced garlic and peppercorns, and sauté 3 minutes more.

3- Add fish fillets, cook one side for 3 minutes, then turn the other side and add white wine.

4- Add salt and cook for 4 minutes more. It’s ready to serve.

113

Lionfish ceviche

Ingredients (for 2 pax) 100-120 gr lionfish fillet 1 big lemon ½ table spoon olive oil ½ peach ½ red onion ½ red bell pepper Fresh basil 1 teaspoon cream cheese salt Method 1- Chop the fish fillet like small squares and put them in a cup.

2- Squeze the lemon and cover the chopped fish with lemon juice. It has to wait min. 1 max. 1.5 hours in the fridge.

3- Finely chop red onion, peach, basil and red bell peppers.

4- After 1 hour remove the fish from lemon juice and mix with the other ingredients including salt, cream cheese and olive oil.

You can serve the ceviche with nachos.

114

Lionfish pilaki

Ingredients (for 2 pax) 300 -350 gr lionfish fillet 1 big onion 2 gloves of garlic 2 plums 1 red bell pepper 4 table spoons olive oil 1 table spoon white wine 1 table spoon malt vinegar 1 tea spoon coriander seeds parsley salt Method 1- Thinly slice the onion lengthwise.

2- Heat the olive oil in a pan over medium heat and add onion, sautĂŠ for 5 minutes.

3- Thinly slice garlic and plums.

4- Chop the red bell pepper.

5- Julienne the fish fillets.

6- After the onion is sautĂŠed for 5 minutes, add garlic, red bell pepper and sautĂŠ for 2 more minutes.

7- Add white wine and coriander seeds and simmer for 2 minutes.

115

8- Add jullienned fish fillets and sautĂŠ for 4 minutes and add salt.

9- Add plums, vinegar and parsley, and turn off the heat.

Itâ&#x20AC;&#x2122;s better to eat this dish when it is cold.

Lionfish cakes Ingredients (for 2 pax) 500 gr lionfish fillet 2 middle-sized potatoes 2 gloves of garlic 1 tea spoon ground coriander A pinch of ground nutmeg 4 table spoons flour 1 tea spoon baking soda 2 table spoons mixed fresh green herbs, such as dill, chives, basil or parsley 5 table spoons sweet chilli sauce 3 table spoons vegetable oil Salt and pepper Method 1- Roughly chop the fish, then peel and grate the potato.

2- Combine with the flour in a bowl, then season with sea salt and black pepper.

3- Chopped all green herb together and add to the bowl.

4- Add spices like nutmeg and coriander, and combine well.

116

5- Bring together with your hands and shape it into 12 flat patties, then leave to chill in the fridge.

6- Heat 3 table spoons of oil over a medium-high heat.

7- Cook the fish cakes for 3 minutes on each side, until golden and crisp, then put them on the kitchen paper to drain.

8- Serve with sweet chilli sauce.

Lionfish the Lady Gaga (by Bayram Ă&#x2013;ztĂźrk) Ingredients (for 2 pax) 3 Lionfish (each 500 gr) - filleted Salt and black pepper Olive oil for frying Tomato sauce Flour Garlic Method 1234-

Season the fish fillets with salt and pepper.

Put a little bit of flour on them.

Fry in olive oil.

Put the tomato sauce and garlic when served.

117