Our Mediterranean-level analysis provides solid correlative evidence that landings of seabream, an iconic fish species, are now driven by aquaculture. A landings-per-unit-of-effort (LPUE) proxy, using data from six Mediterranean EU member states, also showed significant correlations with seabream escapes, suggesting that aquaculture continues to influence landings after accounting for fishing effort. However, despite a similar pattern being evident for seabass until 2005, the relationship between landings and escapes for this species was not significant, mainly due to a large drop in landings in the last five years. We argue that relatively higher mortality rates post-escape, lower capturability by the artisanal fleet, and minor 'leakage' of farmed seabass compared to seabream may prevent the detection of escapees’ effect on landings for this species. Given the substantial declines (30%) in fisheries landings across all species in the Mediterranean (FAO 2020, 2022) and the downward trend in the number of fishing vessels across the Mediterranean and the Black Sea area over the last decades (-37% for the studied fleets since 1990), the most parsimonious explanation for the recent and rapid increase in seabass and sea bream landings is that escaped fish from aquaculture boost wild populations. Our results have significant implications for fisheries stock assessments, which escapees will continuously confound, and the genetic diversity of these species in the wild. High connectivity levels between wild and farmed populations may also contribute to epidemics of pathogens or parasites and competition for food and habitat (Arechavala-Lopez et al. 2013b, Arechavala-Lopez et al. 2018).
Globally, fish escapes are common in farming regions, including the Mediterranean Sea and the Black Sea, two of the ecoregions at most risk from farmed fish escapes (Atalah & Sanchez-Jerez 2020). Every year millions of fish escape from fish farms into Mediterranean natural coastal habitats, and the leading cause of escape incidents (> 90%) is farm structural failure due to extreme weather events (Jackson et al. 2015). The situation has worsened over recent years due to record-breaking storms that hit the Mediterranean (Amores et al. 2020), and escapees continue to be one of the main concerns of both farmers and fishermen (Akyol et al. 2019).
Available evidence suggests that seabream are more prone to escape than seabass (Glaropoulos et al. 2012). Seabream actively bite farm nets when visually attracted by worn and loose threads or even biofouling organisms (Papadakis et al. 2013, Glaropoulos et al. 2014). At the same time, seabass do not display a net-biting or induced-escape behaviour as marked as seabream (Glaropoulos et al. 2014). In addition, recapturing escaped seabass is more challenging than seabream because of their better swimming and dispersion abilities and more pelagic behaviour, which would hinder recapture by artisanal fisheries using bottom gillnets and trammel nets (Arechavala-Lopez et al. 2013c, Toledo-Guedes et al. 2014). There is little data on escaped fish survival in natural coastal habitats, but seabass escapees are more susceptible to stress due to reduced food intake and growth, resulting in a higher mortality rate in acute stress moments (e.g. escape events) compared to seabream (Samaras et al. 2018). Additionally, ‘escape through spawning’, where farmed fish reach sexual maturity and spawn in sea cages, is an additional route of escape (Uglem et al. 2012). One million 1-year-old seabream were estimated to recruit to wild populations in Greece via this escape route in 2012 (‘escape through spawning’, Somarakis et al. 2013), although the wider extent of this process through space and time in the Mediterranean is unknown. Thus, different pre- and post-escape behaviours among the two species and seabream ‘escape through spawning’ may explain the differences in the relationship between escaped biomass and landings.
Theoretically, aquaculture could alter fisheries captures in two ways: (1) fish escapes enhance conspecific wild stocks, thus maintaining and increasing captures; and (2) cheaper farmed fish flood the market, rendering wild fisheries non-profitable and thus relaxing fishing pressure (Villasante et al. 2013). However, wild and farmed fish behave as two different, unrelated products (Villasante et al. 2013). The latter together with the multi-specific nature of Mediterranean fisheries (Lleonart & Maynou 2003), prevent the flooding effect. However, the evidence points that aquaculture escapees increase landings at a regional scale (Dimitriou et al. 2007b, Glamuzina et al. 2014, Toledo-Guedes et al. 2014, Arechavala‐Lopez et al. 2015, Izquierdo‐Gómez et al. 2017). Our analysis reflects the additive effect of many local cases across the Mediterranean Sea. Although seabream and seabass stocks are currently not formally assessed in the Mediterranean and the Black Sea area, they are essential demersal fisheries, highly vulnerable and heavily exploited (Osio et al. 2015, Froese et al. 2018). Before the introduction of aquaculture, seabream stocks were fished at levels above sustainable yield (Farrugio et al. 1994), and it is unlikely that this situation has improved (FAO 2020, 2022). In this context, escapees could mask the overexploitation of wild stocks (Hansen et al. 1999, Tsikliras et al. 2015), promoting misleading stock assessments.
The biomass of species reared in floating cages in the Mediterranean massively surpasses that of wild populations, and estimated escapees are well above fisheries’ landings. This also happens, for instance, with Atlantic salmon (Salmo salar) but at a scale several orders of magnitude larger (Naylor et al. 2005). Positive regime shifts in landings were detected in the early 1980s and 2000s, matching the onset of aquaculture in the Mediterranean and when estimated escapees vastly surpassed landings of both species, respectively (Fig. 3). Stock assessments of Atlantic salmon are reliable because it is relatively easy and accurate to distinguish between wild and escaped fish (Fiske et al. 2005). However, since the available tools for identifying the origin of seabream and seabass are not implemented, escapees could sustain landings regardless of the state of wild stocks (Arechavala-Lopez et al. 2013a, Warren-Myers et al. 2015). Aside from the multi-specific nature and wide variety of gears used in Mediterranean fisheries, stock assessments and fisheries management occur at both regional and national levels, adding to the complexity of dealing with escapees (Smith & Garcia 2014). For the first time, we show that escapees can influence landings at a pan-Mediterranean scale, highlighting the urgent need to identify wild and escaped stocks and adjust catch records accordingly (Hansen et al. 1999).
Most restocking programs use wild broodstock to produce fish that will be released (Araki et al. 2007); thus, escape events may be defined as ‘unplanned restocking actions’ because they represent an unintentional and non-controlled release of cultured fish coming from selectively bred broodstock. How suitable farmed fish are for maintaining and improving wild populations remains unclear (Araki & Schmid 2010). Some studies point out that using farmed fish with low genetic diversity to restock small wild populations can cause introgression and loss of local adaptations, which could end in local extinctions due to genetic drift and bottlenecks (Youngson et al. 2001, Baskett et al. 2013). Both seabream and seabass are well established in the Mediterranean; in the case of seabass, its population is divided into three main genetic groups: the North-Eastern Atlantic, the Western Mediterranean and the Eastern Mediterranean (Haffray et al. 2007). However, Mediterranean haplotypes have been detected as far as the Thames estuary and Norway (Coscia & Mariani 2011), which is explained by the common use of Mediterranean hatchery strains in the Atlantic. Genetic admixture is evident between wild and farmed seabass in Cyprus, where at some locations, escapees represent up to 70% of individuals captured in the wild (Brown et al. 2015). For seabream, some genetic differentiation exists between Atlantic and Mediterranean populations (Sola et al. 2007), and genetic admixture between farmed escapees and wild populations occurs at the regional level (Šegvić-Bubić et al. 2014). Continuous escape-mediated replenishment of wild populations could affect the genetic landscape and dilute local adaptations in both species, which may compromise the sustainability of wild stocks in the long term (Youngson et al. 2001). However, for seabass, the oldest domesticated stocks have been bred in captivity for only eight generations without input from wild stocks (Chavanne et al. 2016), and most seabream broodstocks are genetically similar to wild ones (Maroso et al. 2021), which may limit the extent of genetic effects of farmed fish over wild populations. Finally, unlike proper restocking, parasites and diseases are not monitored during escape events, posing a transmission risk to wild populations (Toledo-Guedes et al. 2012, Arechavala-Lopez et al. 2013b).
Consumers have concerns that aquaculture escapees are not labelled correctly (Luque & Donlan 2019). Mislabelled escapees are sold as wild fish in local markets because discriminating tools are not applied (Arechavala-Lopez et al. 2013a). Food security could be compromised due to the antibiotic concentration that recent escapees, previously subjected to treatment, could carry (Juan-García et al. 2007). Conversely, commercial and recreational fisheries can benefit from escape events, which can be seen as positive events in the short term. Escapees provide extra income for commercial fishers, enhancing the fishing experience and boosting recreational fishers' capture (Lorenzen et al. 2012). Together with natural mortality, both professional and recreational fisheries can play an important role in removing escapees from the wild (Toledo‐Guedes et al. 2014). Although the overall impact may be low (Dempster et al. 2018), the inclusion of recapture actions in future contingency plans could boost the effectiveness of fisheries in preventing the entrance of farmed fish labelled as wild in the markets.
While technical standards in farm designs have been implemented in Norway and Scotland (Jensen et al. 2010); there is a clear need to implement these standards to prevent escapes in Mediterranean countries, to avoid impacts on the functioning and structure of marine ecosystems and promote the industry's sustainable development. Mitigation measures, including monitoring plans aiming to identify escaped fish both in the wild and within fisheries landings, are needed to address the fishing actions contained in a contingency plan removing escapees from the wild or to label escaped fish entering the food chain correctly. These measures would, in turn, improve the reliability of wild stock assessments for the correct resource management and food safety.