1. Introduction
The Mediterranean Sea is a key hotspot for marine biological invasions, hosting approximately 1000 non-indigenous species to date [
1]. Among these, ~13.5% have been characterized as invasive due to their adverse effects on human health, the economy of coastal communities and the structure, function and services of native ecosystems [
2,
3]. The economic impacts of marine invasive species relate to monetary losses to coastal human activities such as fisheries, aquaculture, tourism and marine infrastructure [
4], resulting in a potential decline in living standards. Regarding fisheries, invasive species inflict losses by depleting native commercial stocks (through predation, competition, habitat degradation and disease transmission), by fouling gear and equipment and by damaging fishing gear and catches [
5].
Small-scale fisheries hold substantial socio-economic importance for Mediterranean fishers, contributing significantly to sustainable livelihoods, employment and income within fishing communities, as acknowledged by the FAO [
6]. In Greece (eastern Mediterranean), the small-scale fishing fleet numbers approximately 11,000 active vessels comprising >90% of the fishing fleet. Small-scale fisheries produce 35–40% of total landings, although they contribute 55% to total fish value, as they mainly target high-valued species [
7]. The regions on which the present study focused were coastal areas of the Ionian Sea, the Cretan Sea and the Libyan Sea (
Figure 1), where 1317, 501 and 108 active small-scale fishing vessels are registered [
8]. In these regions, the most commonly used gear types are nets (mainly gillnets and trammel nets) and bottom longlines, with combined nets also used to a lesser extent [
9,
10,
11]. In the Ionian Sea, net fishers mainly target the European hake
Merluccius merluccius, the common sole
Solea solea, the common dentex
Dentex dentex and members of the family Mullidae (striped red mullet
Mullus surmuletus and red mullet
Mullus barbatus) [
9,
10]. In seas around Crete, net fishers mainly target members of the family Mullidae, the common cuttlefish
Sepia officinalis, the Mediterranean parrotfish
Sparisoma cretense and the European barracuda
Sphyraena spyraena [
11]. Longline fisheries in all regions mainly target the red porgy
Pagrus Pagrus and species of the genera
Diplodus and
Epinephelus [
9,
10,
11].
Depredation by marine fauna is a significant source of economic loss for small-scale fisheries in the Mediterranean Sea. To date, the most well-studied species that cause damages in the Mediterranean small-scale fisheries are dolphins and seals [
12,
13]. To a lesser extent, sea turtles, large fish (e.g., sharks, amberjacks, eels) and sea birds are also reported by fishers to inflict gear and catch damages [
14,
15]. Over the last few decades, however, the rising rate of biological invasions of Indo-Pacific marine species from the Red Sea to the Mediterranean Sea has increased the number of species negatively affecting small-scale fisheries [
16]. The blue crab
Portunus segnis [
17] and pufferfish species [
18] are now reported as the new gear-damaging invaders of the eastern Mediterranean.
Lagocephalus sceleratus (Gmelin, 1789), commonly known as the silver-cheeked toadfish, is the largest among the tetraodontid pufferfish introduced in the Mediterranean [
19]. The species was first recorded in the Mediterranean Sea on the southwestern coast of Turkey, in 2003 [
20]. In the Basin,
L. sceleratus is found in depths ranging from 0 to 170 m and on various substrate types, including sandy, rocky and muddy areas and
Posidonia oceanica meadows [
21,
22]. However, the species shows a preference for shallower waters at depths 0–50 m and sandy bottoms with patches of
Posidonia oceanica, as stated in previous studies [
23,
24].
Shortly after its introduction,
L. sceleratus gained notoriety as one of the “worst” invasive species in the Mediterranean Sea [
25], primarily due to the high levels of the neurotoxin tetrodotoxin (TTX) contained in its internal organs, muscles and skin. The high toxicity of silver-cheeked toadfish has raised significant public health concerns in eastern Mediterranean countries, as several cases of TTX poisoning, including some fatalities, were linked to the consumption of this pufferfish [
26,
27,
28,
29,
30]. In response to these health risks, the European Union, Turkey and Egypt have enacted legislation prohibiting the commercial exploitation and consumption of
L. sceleratus along with other pufferfish species [
31,
32,
33]. Additionally,
L. sceleratus adversely affects small-scale fisheries, which is attributable to two main factors: Firstly, as consistently emphasized by numerous reports of eastern Mediterranean fishers, the species depredates on fishing gears causing damage to nets, longlines and catches due to its formidably sharp teeth [
27]. Secondly, its inherent toxicity makes it a common discarded catch, rendering it commercially worthless.
In contrast to the extensive research on the toxicity of the species in the Mediterranean Sea [
34,
35,
36,
37,
38], quantitative assessments of its economic impact remain limited. Such assessments originate exclusively from the Mediterranean coasts of Turkey, where total losses due to
L. sceleratus were estimated at around EUR 4.5 million per year [
39,
40]. Another review provides semi-quantitative data, ranking the socio-economic impact of this species in the Mediterranean Sea as moderate, albeit higher compared to other invasive fish with management priority [
28]. In the Greek seas, data are even more scarce and fragmentary, with only one study ranking silver-cheeked toadfish as the second most damaging species for the Cretan small-scale fisheries after dolphins, based on local fishers’ perceptions [
15]
The present study aims to investigate for the first time the magnitude of the economic impacts of L. sceleratus on small-scale fisheries in Greece and to assess how fishers adapt to this emerging economic challenge. Predictive models were also constructed to elucidate the factors affecting L. sceleratus by-catch, in terms of biomass and abundance, as well as the depredation by this species on fishing gears during fishing trips.
4. Discussion
In the present study, we evaluated the magnitude of
L. sceleratus impacts on small-scale fisheries in the Greek seas through interviews with local fishers. A multitude of economic impacts were reported (
Table 3), marking the first quantitative assessment of monetary losses suffered by Greek fishers due to this invasive species. In response to
L. sceleratus depredation on gears, fishers reported several fishing tactic adjustments (
Figure 3), particularly in Crete, where the species was more prevalent. Additionally, in order to disentangle the factors influencing the interaction of
L. sceleratus with small-scale fisheries, generalized additive models were applied to data collected through onboard sampling on Cretan vessels.
Our study contributes to the limited literature on the impacts of
L. sceleratus in Mediterranean small-scale fisheries (
Supplementary Table S1) and, on a broader scale, to the poorly assessed economic impacts of marine invasive species in European seas [
47]. It is the first to examine all sources of monetary losses due to interactions with this pufferfish (gear-, catch- and labor-related losses), thereby providing a more accurate estimation of the overall economic impact of this damaging species. In contrast, previous studies focusing on the economic impacts of
L. sceleratus, conducted along the coasts of Turkey, mainly addressed the economic losses associated with gear damages, with limited information on labor and catch losses provided [
18,
39,
40].
We found that the silver-cheeked toadfish adds substantial extra economic pressure to small-scale fisheries, a sector already considered marginalized and vulnerable [
48]. The mean annual income of Greek small-scale fishers for the period 2012–2019 was 17,518 EUR/vessel, with little variability recorded across different years (range = 15,896–20,168 EUR/vessel) [
49]. This implies that fishers in Crete experience approximately 36% losses in their total income, while those in the Ionian region experience a comparatively minor 1% reduction due to
L. sceleratus impacts. The annual economic losses resulting from
L. sceleratus depredation were comparable to those caused by marine mammals in Greek small-scale fisheries [
50,
51,
52,
53] (
Supplementary Table S2). According to a previous study conducted in Crete in 2013, fishers had already identified
L. sceleratus as the second most gear-damaging species after dolphins, followed by seals and turtles [
15]. Additionally, the species was also reported to have a higher impact on catch compared to marine megafauna species. However, since then, the abundance of this species has substantially increased, and the impacts found are presumed to be more severe than in previous years.
Variations in the economic impact of
L. sceleratus were observed across study areas and fishing gears. Specifically, the highest economic losses were reported by the Libyan Sea fishers operating both nets and longlines, while the lowest were reported by Ionian netters. The magnitude of the impact in each fishing region appeared to align with the reported
L. sceleratus catch frequency and annual by-catch, which were higher in the Libyan Sea (southeastern region of this study) and markedly lower in the Ionian Sea (northwestern region of this study) (
Table 3). These regional trends may be linked to the westward expansion of the species in the Mediterranean Sea, suggesting higher occurrence and population size in the southeastern regions compared to the northwestern ones. Indeed, Coro et al. [
54] found that the probability of
L. sceleratus occurrence is higher in South Turkey and South Greece (>0.8) compared to the Aegean and Ionian seas (0.4–0.6).
In Crete, the interview results agreed with findings from the onboard sampling and indicated that L. sceleratus is more frequent and abundant in the Libyan Sea, contributing more to the total catch compared to the Cretan Sea. However, the higher L. sceleratus BPUE recorded in the Cretan Sea is an indication that the species populations in south Crete included a relatively higher number of smaller individuals than those in the north. This finding is also supported by the mean total length of specimens caught, which was higher in the Cretan compared to the Libyan Sea. The potential increased presence of small-sized L. sceleratus in the Libyan Sea may suggest that nursery grounds of the species are mostly located in southern regions of Crete rather than in northern regions of the island.
In order to mitigate the impacts of silver-cheeked toadfish, fishers adjusted their fishing tactic to avoid interaction with this pufferfish. Fishers’ tactical responses to
L. sceleratus depredation reflect well-established knowledge regarding the species ecology (e.g., depth and substrate preferences, daily activity). Regionally, the highest percentage of fishers who changed their tactic was recorded in the Libyan Sea, where the higher abundance indices of
L. sceleratus (annual by-catch, NPUE, catch frequency) and the higher depredation probability were estimated. The shift of fishing activity to deeper waters (>50 m) was the most frequently reported tactic adjustment of fishers operating in seas around Crete, which is justified by the fact that operations conducted in shallow waters (<40 m) are more likely to be impacted by this species (see Results
Section 3.5). Similar changes in fishing tactics have also been reported for Cyprus small-scale fisheries [
55], as well as for long- and handline fishers in the island of Rhodes (southeast Aegean), who shifted their effort to depths greater than 60 m [
24].
The GAMs fitted in the present study revealed that interactions of
L. sceleratus with small-scale fisheries, in terms of the species by-catch and depredation, were influenced by depth, gear, region and temperature. All dependent variables tested presented a decreasing trend with the increase in fishing depth. Specifically, depredation probability, biomass and abundance of
L. sceleratus were higher between 0–40 m and started to steadily decrease as the fishing depth exceeded 40 m. These findings agree with the results from the interviews; the lowest catch frequencies were reported in the depth zone 65–100 m (
Table 2). In a previous study in Cyprus, the highest numbers of
L. sceleratus caught during small-scale fisheries operations were also recorded in the 10–40 m depth zone [
21]. Similarly, in trawl operations conducted on the Turkish coasts, the highest catches of
L. sceleratus were reported in the depth zone 0–25 m [
56,
57]. Concerning the fishing gear,
L. sceleratus biomass and abundance were higher in nets than loglines, whereas the opposite was true for depredation probability. These findings are explained by the fact that
L. sceleratus easily escapes when caught on longlines, as it cuts off the branch lines with its sharp teeth. Moreover, the damages may be more frequent for longlines due to the appeal of the bait used.
The effect of region indicated that depredation probability and L. sceleratus abundance were higher in the Libyan Sea compared to the Cretan Sea. Interestingly, region was significant in the abundance model but not in the biomass model. This is an additional indication of the presence of more and smaller specimens in the Libyan Sea and fewer and larger specimens in the Cretan Sea (see above). Conclusively, the higher abundance of L. sceleratus in the Libyan Sea may also justify the higher depredation probability found in this region.
Lastly, the increase in temperature positively influenced the depredation probability during a fishing trip. This trend may be driven by the increase in
L. sceleratus metabolic rate caused by the sea temperature rise [
58]. However, a drop is presented in this general increasing trend in temperatures between 21 and 23 °C (period from early to late June). This period corresponds to the peak of the spawning activity of
L. sceleratus in Crete [
59], when lower depredation on fishing gears may be related to a general restriction of food intake by the species. Such limitation of feeding activity may occur due to investment in accessory spawning activities, such as nest building, which is observed in other pufferfish species [
60] but has not been confirmed yet for
L. sceleratus.
Up to now, specific management actions for the control of
L. sceleratus populations in the eastern Mediterranean have only been applied in Turkey and Cyprus. These actions involved the initiation of bounty programs which compensated the fishers for each specimen of
L. sceleratus caught [
61,
62,
63]. Other than the small monetary benefit for the fishers, these bounty programs have, so far, been ineffective in controlling
L. sceleratus populations, as no evident declining trends have been observed yet [
61,
62]. Moreover, prior experience with the management of lionfish (
Pterois miles/
Pterois volitans) in the western Atlantic has shown that bounty programs are not a self-sustaining measure, as they usually do not run on a consistent basis due to their dependence on fund availability [
64].
According to Giakoumi et al. [
65], the most applicable and highly prioritized management actions in order to control a widely spread marine invader (such as
L. sceleratus) are (a) raising public awareness regarding the species impacts, (b) encouraging the targeted removal of the species from commercial and/or recreational fisheries (i.e., increasing the fishing pressure on the species), and (c) promoting the commercialization of the species. A successful management example is the control of lionfish populations in the western Atlantic [
64], but for the case of
L. sceleratus, the non-edibility of the species necessitates exploring commercial applications other than human consumption.
Currently, there are no available market products from
L. sceleratus; however, some promising advances towards the potential commercial use of this invasive species have been made. Bioactive compounds, such as collagen and TTX, have been successfully extracted from
L. sceleratus tissues, and, moreover, successful detoxification methods have been developed [
66,
67]. TTX, which is predominantly extracted from pufferfish, can be used in various medical and pharmaceutical applications [
68]. Additionally, the extracted collagen and TTX can have applications in the production of cosmetics, and the detoxified
L. sceleratus tissues can be used as a fish-oil source in nutraceuticals [
65,
66]. The processed skin of
L. sceleratus is also available for the production of “eco-friendly” clothing and accessories [
69]. In conclusion, there is much scope for the commercial exploitation of
L. sceleratus, which would be essential for a long-term, self-sustaining management plan.
In summary, our research significantly advances our understanding of biological invasions, particularly in the context of marine invasive species interacting with fisheries. The investigation of spatial variations in the distribution and impact of such species emerged as a crucial aspect. Region-based approaches are recommended for future studies in the field of invasion biology, as they are essential for targeted and cost-effective management schemes. The combination of fishers’ perspectives, onboard sampling and the application of predictive models was proven to be a robust approach. Similar approaches can provide insights that can guide stakeholders in regions where the arrival or population growth of an invasive species, interacting with fisheries, is imminent.