New records of the silver-cheeked toadfish Lagocephalus sceleratus (Gmelin, 1789) in the Tyrrhenian and Ionian Seas: early detection and participatory monitoring in practice

The silver-cheeked toadfish Lagocephalus sceleratus (Gmelin, 1789)an invasive toxic species well established in the eastern Mediterraneanis rapidly expanding through the western Basin and a public campaign was set to inform Italian citizens on the risks associated with its consumption. Both news media and local communities responded rapidly to the initiative generating an increasing flow of information. On 15 April 2016, a new capture of this species (off Briatico, Calabria, Italy at 25 m of depth), was promptly reported to the authors, representing the first documented record of L. sceleratus from the Tyrrhenian Sea. On 7 June 2016, a second specimen was captured at Montebello Ionico in Calabria. This case of early detection is here presented as a successful example of interplay among citizens, researchers, and policy makers: a powerful approach for monitoring the spread of invasive species and reducing their potential impacts through increasing awareness.


Introduction
Early detection and rapid response (EDRR) is recognized as a key aspect for invasive species management (Genovesi and Shine 2004) and acknowledged by the European Commission (COM 2008).These principles, today included in the new European regulation (EU) No 1143/2014 on the prevention and management of the introduction and spread of invasive alien species, are deemed to be crucial for tackling unwanted invasions.Promoting public awareness and disseminating information to the local communities, even through specific alerts, is a key driver to promptly detect unwanted invasive species and in the last few years several theoretical frameworks have been developed through formalised early warning systems (Genovesi et al. 2010).Besides these theoretical efforts, mostly elaborated at the policy level, members of the public are increasingly participating in scientific research (Shirk et al. 2012) opening new potential for tracking biodiversity changes in both terrestrial and marine environments (Simpson et al. 2009 The silver-cheeked toadfish Lagocephalus sceleratus (Gmelin, 1789) (Tetraodontidae), one of the worst invaders of the Mediterranean Sea (Streftaris and Zenetos 2006), is expanding rapidly through the western Mediterranean Sea.Due to its toxicity, many Mediterranean countries have promptly responded by informing the general public about the risks associated to the consumption of this species.These awareness initiatives, necessary to limit the impacts of this invasion (Nader et al. 2012), have been carried out in countries such as Egypt, Turkey, Lebanon, Cyprus, Greece and Tunisia (see Ben Souissi et al. 2014 and references therein).Today, the consumption of the silver-cheeked toadfish is illegal in many nations, including Japan and Malaysia where other pufferfish are traditionally (and legally) consumed.At the European level, European Regulations Directive 91/493/CEE, 853/2004/EC and 854/2004/EC have issued a ban on the fishery, marketing, and consumption of L. sceleratus and Italy bans the commercialization of all Tetraodontidae (Art.5 DL n. 531/1992).
Due to the rapid expansion of the silver-cheeked toadfish through the Strait of Sicily (Jribi and Bradai 2012), Italian researcher, at the Institute for Environmental Protection and Research (ISPRA) initiated information gathering activities among southern Sicilian fisheries but no further observations of this species were recorded until 2013.The first documented record of L. sceleratus from Italian waters is dated 7 October 2013 from Lampedusa Island (Azzurro et al. 2014) and prompted a series of initiatives at both the national and local scale.Other observations indicating rapid expansions of this species distribution were documented in Algeria (Kara et al. 2015), Malta (Deidun et al. 2015), Spain (Katsanevakis et al. 2014), and in the Eastern Adriatic Sea ( prem et al. 2014).

Material and methods
On 22 December 2015, a national awareness campaign was launched by ISPRA in collaboration with the Ministry for Agricultural and Forestry Policies, the Italian Harbour-master's Office, and the web platform http://www.seawatchers.orghosted by the Institute of Marine Sciences Consejo Superior de Investigaciones Científicas ICM-CSIC of Barcelona (Spain).This campaign reinforced those initiatives undertaken soon after the first record of L. sceleratus in Italian waters (Andaloro et al. 2016).The communication with the public (ongoing) is mostly set through the dissemination of a fact sheet (Figure 1), written in Italian, which warns of the risks associated with the consumption of this species.The first section of the factsheet contains a description of L. sceleratus, an update on its geographical spread in the Mediterranean Sea, and warnings about its toxicity specifying that tetrodotoxin is resistant to cooking.The second section of the factsheet explains how to recognize L. sceleratus from other co-occurring pufferfish [i.e., L. lagocephalus (Linnaeus, 1758) and Sphoeroides pachigaster (Müller and Troschel, 1848)].In case of capture/observation of the silver-cheeked toadfish, fishermen were invited to immediately contact ISPRA.A dedicated email pescepalla@ispra mbiente.itplus three telephone numbers were made public to receive such information.The campaign was advertised by different media sources ranging from popular TV programmes to online articles and local newspapers.Here we present two new Mediterranean records of L. sceleratus.In both cases, researcher made direct contacts with the fisherman to verify the observation and acquire specific details.

Results and discussion
On 15 April 2016, an adult specimen of L. sceleratus (Figure 2) was captured by purse seine targeting the European pilchard (Sardina pilchardus), 1.85 km off the Briatico coasts (Calabria, Italy) (Lat 38.742;Long 16.033), at 25 m of depth.This unusual capture, which represents the first documented occurrence of silver-cheeked toadfish in the Tyrrhenian Sea, was documented through a video recording by a local newspaper and communicated to ISPRA researchers the same day as the capture.Then, researchers validated the record and immediately alerted the local harbour officer who traced the fisherman.The specimen, kept frozen by the same fishermen and then shipped to the ISPRA laboratories, weighed 2.463 kg and was 58 cm total length (TL).At the same time, ISPRA launched a press release and published a short video (http://www.youtube.com/watch?v=c2fjI7pYGIg) to promote the alert.On 7 June 2016, a second specimen was recorded from Montebello Ionico, Calabria at Saline Ioniche (Lat 37.925; Long 15.754) and promptly posted to seawatchers.org(http://www.observadoresdelmar.es/obser vacio-detall.php?projecte_id=9&id=5549).The specimen, of an estimated weight of 4 Kg, was captured by surfcasting at a depth of 4 meters on a sandy bottom and then released alive.This latter stands for the second record of L. sceleratus in the Ionian Sea, the   first capture being reported in January 2014 near Syracuse (south-east Ionian Sea) by Kapiris et al. (2014).Similarly to the case reported by Azzurro et al. (2014) and dealing with the first Italian record of L. sceleratus, this new capture generated a great deal of interest among the media and social networks.The number of Italian articles and web pages providing information on Lagocephalus sceleratus and published online, jumped from 39 (in 2015) to 215 (in May 2016) (Source: Google news retrieval engine).As often happens for toxic or venomous species (e.g., Hayes and Mackessy 2010), it must be noted that the alert campaign also stimulated a series of sensationalistic reports in the lay press, some of them providing incorrect identifications.This is for example the case of the oceanic puffer Lagocephalus lagocephalus (Il Tirreno 2016) and the brown trout Salmo trutta (Leccesette 2015), misidentified with the highly venomous silver-cheeked toadfish.Notwithstanding these inaccurate new reports, it must be admitted that the clamour raised about a toxic invasive species probably triggered intense interest in local communities and encouraged a spontaneous exchange of information based on mutual benefit and interest.Outcomes of this entire process are not limited to the (early) detection of invasive species in new locations but must be also related to social aspects, such as an increased awareness on this issue of public concern.These activities are also expected to ameliorate the willing of local communities to be engaged in participatory monitoring and improve the relationships between local communities and public research and management, which are very desirable aspects of every social-ecological system.

Figure 1 .
Figure 1.Poster advertising the toxicity of the Lagocephalus sceleratus, as part of the information campaign carried out in Italy, with information on other pufferfish occurring in the area.Drawings of A. Lombarte.The high resolution version of the poster can be downloaded at http://www.isprambiente.gov.it/files/comunicati-stampa/2015/Locandina_pesce_palla.pdf .

Figure 2 .
Figure 2. On the left, the silver-cheeked toadfish captured off Briatico, Italy, Southern Tyrrhenian Sea (Photo credits: Lieutenant O Iemma); on the right the specimen captured at Saline Ioniche (Ionian Sea).Photo credits: P Romeo.

Figure 3 .
Figure 3. Two new occurrences of Lagocephalus sceleratus in the Tyrrhenian and Ionian Seas according to the present study.
Azzurro et al. 2013 2013for exotic fish species in the Mediterranean Sea).These contributory projects (sensu Shirk et al. 2012), which are generally designed by scientists and for which members of the public primarily contribute data, have great potential for tackling the issue of invasive species.They may provide early detection, generate large data sets, and ultimately contribute to management actions.