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Management of fish escapes from Mediterranean Sea cage aquaculture through artisanal fisheries
Ocean & Coastal Management 122 (2016) 57e63
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Management of fish escapes from Mediterranean Sea cage aquaculture through artisanal fisheries D. Izquierdo-Gomez*, P. Sanchez-Jerez Marine Science and Applied Biology Department, University of Alicante, 03690 Alicante, Spain
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 June 2015 Received in revised form 7 January 2016 Accepted 10 January 2016 Available online 28 January 2016
Fish escaping from net pens have always been considered a major source of socioeconomic and ecological issues entitling high economic loses for farmers. Local artisanal fisheries have proved the ability to mitigate escape events by recapturing escapees, but its effectiveness has always been questioned. However, the knowledge regarding the interaction of large scale escape events and local fisheries remains scant. The recapture dynamics of a massive escape of nearly 100 tones taking place in Western Mediterranean was analysed. The artisanal fishery showed efficient in recapturing escaped fish as 64.7% of the escaped biomass was recovered. The spatial distribution of escaped gilthead seabream along the shore was studied as well as the efficiency of the fishing fleet distinguishing between fishing gears. The recapture of escaped fish showed well correlated with the distance to the escape point. Moreover, a high recapture success (64.7%) was registered being fish traps (53.8%) more efficient in recovering escapees than nets (10.9%). Concluding, management implications and data-based measures to be implemented on further regulations of escape events are discussed. © 2016 Elsevier Ltd. All rights reserved.
Keywords: Small-scale fisheries Fish farm Gilthead Net pens Coastal zone management
1. Introduction Fish escaping from marine fish farms have always been considered a major source of socioeconomic and ecological issues (Hegberet et al., 1993; Fleming et al., 2000; Soto et al., 2001; Naylor et al., 2005; Johnson and Johnson, 2006; Jensen et al., 2010). Between 2009 and 2012, Jackson et al. (2015) claimed more than 8 million fish escaping from European farms with 77.6% corresponding to gilthead seabream (Sparus aurata) reared in the Mediterranean Sea. The derived economic loss resulted V47.5 million per annum, on average; V42.8 million due to escapes of sea bass and sea bream in the Mediterranean Sea and V4.7 million for salmon in Northern Europe (Jackson et al., 2015). Such problem was described decades ago from Atlantic salmon and cod escaping from sea cages of northern European countries (Gausen and Moen, 1991; Web et al., 1991; Milner and Evans, 2003; Butler et al., 2005; Fiske et al., 2006; Walker et al., 2006). Norway, as the main Atlantic salmon producer shed light on the causes driving salmon and cod escape events based on its national record of escapes, available since 2001 (Jensen et al., 2006, 2010; Moe et al., 2007; Hansen et al.,
* Corresponding author. E-mail address: [email protected] (D. Izquierdo-Gomez). http://dx.doi.org/10.1016/j.ocecoaman.2016.01.003 0964-5691/© 2016 Elsevier Ltd. All rights reserved.
2008). The main causes driving escapes resulted in different structure failures, operational errors and biological causes (netbiting), all combined with a high stress situations for materials during storms (Jensen et al., 2010; Jackson et al., 2015). Consequently, the implementation of a new technical standard (NS9415) for the materials of open sea fish farms was linked with a remarkable decrease of escape events in the following years (Jensen et al., 2010). In addition, new management measures were included in the national regulation of aquaculture (Norwegian Ministry of Fisheries and Coastal Affairs (2008)) as: mandatory reporting of all escape incidents, establishment of the Norwegian Escapes Commission, introduction of enforceable technical regulations for the design, dimensioning, installation and operation of sea cage farms, investment in research and development projects and training of fish farm operators to prevent escapes (Jensen et al., 2010). Nowadays, the escape events in all main fish producing countries in northern Europe (e.g. Norway, United Kingdom), America (e.g. Canada, United States and Chile) together with Australia are regulated by a specific framework, which, in general, is entailed in the aquaculture regulation of the country (all links at IzquierdoGomez et al., 2015). However, although since early eighties (FAO Fishstat, 2014) there is a growing Mediterranean market of reared gilthead seabream (S. aurata), European seabass (Dicentrarchus
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labrax) and more recently meagre (Argyrosomus regius), none of the main fish-producing coastal countries (i.e. Croatia, France, Greece, Italy, Spain, Turkey) yet provides specific regulation of fish escapes. Thus, a pan-Mediterranean scenario where fish escaping from sea cages influence the coastal ecosystem via gene introgression on populations of wild conspecifics (Segvi c-Bubi c et al., 2011a, 2014) and compete for food and habitat with other species (ArechavalaLopez et al., 2012; Valero-Rodrígez et al., 2015; Toledo-Guedes et al., 2014b) occurs. Furthermore, negative interactions with other forms of aquaculture (Segvi c-Bubic et al., 2011b; Glamuzina et al., 2014) have been described, together with influences either on the behaviour of high valued targeted species of predators (Arechavala-Lopez et al., 2013a, 2014a; 2015a) or on fisheries landings of the reared species (Dimitrou et al., 2007; ArechavalaLopez et al., 2015b). Local artisanal fisheries have proved very effective in mitigating escape events, but the knowledge regarding the interaction of large scale escape events with fisheries is still scarce. There is only one study (Toledo-Guedes et al., 2014a) providing data about fisheries catches after a massive escape of sea bass and sea bream in Canary Islands. Other studies based on experimental escapes involving several hundreds of externally tagged individuals and tenths of acoustically tagged fish (Arechavala et al., 2011, 2012, 2014b) provide valuable information, however, the results may not mirror the real scenario occurring after the escape of tens of thousands of fish. In this study, the recapture dynamics of a massive escape of nearly 100 tones taking place in Western Mediterranean was analysed. In addition, this study was conducted according to the principles of the new framework proposal for maritime spatial planning and integrated coastal management (ICZM; COM, 2013), which indicates that both the prevention and the mitigation of fish escapes from aquaculture should be taken into account by Mediterranean countries when developing integrated coastal zone management plans. The aim of this research is to provide valuable information to design knowledge-based mitigation measures of fish escapes within the Mediterranean Sea, with the specific goal of reducing the derived ecological and socio-economic issues. Thus, the spatial distribution of escaped gilthead seabream along the shore was studied based on the sea bream catches of local fisheries over time. In second term, the recapture efficiency of the whole fleet distinguishing between fishing gears was as well inspected. As a conclusion, a set of valuable guidelines to design contingency and control plans of fish escapes were outlined. 2. Materials and methods 2.1. Study area Aguilas (37 24.7060 N; 1 34.9700 W) is a town located in the southeast of Spain where fishing activities have been traditionally carried out. The commercial fleet is composed by trammelnetters (20), purse-seiners (3), long liners (2) and trawlers (10). The fishing effort of trammel-netters is distributed from cabo Cope (37 25.6530 N; 1 29.2510 W) to few km south of the marina of Aguilas, being generally circumscribed to depths from 10 to 60 m over an area of about 40 km2. Along the coast, sandy/rocky beaches with sandy bottoms patched with hard substrata and seagrass beds (Posidonia oceanica) are found from 1 m to 30 m depth. The studied fish farm is located at 500 m from the coast line (37 24.8180 N; 1 32.1220 W) at 40e60 m depth, where, about 200 tons of fish (D.labrax, S. aurata and A. regius) are reared per annum in 26e28 cages (25 m diam.) from about 20 years ago. Recreational and underwater fishing activities are widely carried out in the area, as well as scuba diving, being Calabardina (37 25.6080 N; 1 30.1550 W) one of the most concurred areas in the Levantine coast of Spain.
2.2. Description of the fishing gears and m etiers of the artisanal fishery Trammel-nets, with slight differences in mesh sizes, targeting Scorpaena spp., Sepia officinalis, and Mullus spp., are the most common fishing gear used by the artisanal fishing fleet in Aguilas, being its usage coupled with the biology and the abundances of each targeted species along the whole year. Octopus pots are used as well in different periods from May to September. The fishing gear “moruna” (hereafter referred as fish trap) responds to an arrow-head fixed trap (Slack-Smith, R. J. 2001) smaller than the “almadraba” (Thunnus thynnus trap), used since the Roman , 1980). The usage of fish traps is legally regulated and, Era (Sara depending on the targeted species (Loligo vulgaris, Seriola dummerilli or Sarda sarda), it is constructed differently, being its usage coupled with the biology and migration of the targeted species. Each fish trap is crafted and it must be authorized by the legal authority before it can be used. The potential locations to place the fish traps are traditionally set from decades, being assigned by draw to any fishermen deciding to use fish traps in a given season. In this research, the fish trap targeting Sarda sarda, deployed from September 15th to the last of November was studied. Nets are the only gear used by the fishing fleet as the permit to use fish traps expires the last of November. 2.3. Escape description and fisheries catches The capture of gilthead sea bream in the study area is common but not abundant compared to adjacent areas, being caught a mean biomass (±SE) of 59 ± 13.9 kg month1 along 2003 and 2004 without taking into to account the months where captures were influenced by the escape event. The escape event took place the last of October 2003 after a storm and SW winds of 13.3 knots together with waves of 3.2 m high, which damaged one sea cage. A total biomass of 93,600 kg of commercial sized gilthead sea bream escaped, being clearly noticeable the increase of its captures in the landings of artisanal fishermen (Fig. 1). 2.4. Statistical analyses In terms of the spatial distribution of the escaped fish, a nonlinear regression model was fitted using landings data derived from the fish trap fishery as independent variable and distance to the farm as control variable using SPSS statistical software package v15.0 (SPSS Inc, Chicago, IL, USA; www.ibm.com/SPPS_statistics). To unveil the recapture efficiency of the local fishing fleet, the daily landed biomass of escaped gilthead sea bream was inspected in terms of accumulated frequency of landed biomass after the escape. Differences in the mean CPUE (capture per unit of effort) of both gears (fish traps and nets) expressed in landed kilogrammes of escaped gilthead seabream $ day1 $ boat1 were analysed by means of one way PERMANOVA design using PRIMER V6.1.13 computer program (Clarke and Gorley, 2006) with the PERMANOVA þ V1.0.3 add-on package (Anderson et al., 2008). To detect further dispersion of the escapees, the catch data of the nearest landing ports was also inspected. All data was obtained from the fish market of Aguilas and the regional fisheries authorities of Murcia. 3. Results The escape event occurred between the last of October and the 1st of November of 2003 when maximum waves height of 6 m were registered in the evening. All fish traps were set along 11 km of coast following the shoreline (Fig. 2). The captured biomass of fish
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Fig. 1. A) Bar plot depicting the daily landed biomass (Y left axis) of gilthead sea bream (Sparus aurata) by artisanal fishermen in Aguilas (Murcia, SE Spain). Dots correspond to number of fishing boats per day (grey) and the total number of boats censused per year (black). B) Detailed daily landings of recaptured fish. Notice left Y axis is shared with A figure. The asterisk (*) indicates the day of the escape: 31-Oct-2003.
traps showed inversely correlated to the distance to the escape site (F ¼ 14.23; p-value ¼ 0.009), according to the best fitting exponential regression model (Fig. 3). The closest fish trap (C; Fig. 2) was located at ca.1441 m, however, it did not capture the larger biomass of escaped seabream which corresponded to the fish trap D (2nd in distance; 1552 m) located 100 m further south which caught a total biomass of 14,126 kg of gilthead sea bream. The influence of escaped fish was noticed along 7 months (NovembereMay, 2003), being the highest gilthead sea bream biomasses landed along November and December 2003. The mean landed biomass (±SE) in the first two weeks of study was 4281 ± 2064 kg and 2132 ± 501 kg respectively, showing thereafter a decreasing trend ranging from 639.74 ± 222.48 kg to 0.83 ± 0.48 kg in December and May respectively. The incidence of escaped fish was not noticeable in the closest landing ports located ca. 35 km both to the north and to the south to the escape event (landings data not shown). Neither purse-seiners nor trawling fleets landed higher biomasses of gilthead sea bream compared to previous years (data not shown). A total biomass of 60,577 kg was landed in 84 fishing days, representing 64.7% of the escaped fish biomass. A total of 53.8% of the recaptured biomass was caught by means of fish traps while
Fig. 2. Map of the study area showing the location of “morunas” (arrow-head shape fish traps) with a given letter (A, B, C, D, E, F, G and H), together with the yielded biomass of escaped fish per trap (Y axis). The fish farm, located between fish traps B and C, is aligned at 0 m in the X axis, which corresponds to the escape point. Recaptured biomass form traps H to A correspond to bars from left to right in the X axis, respectively.
10.9% was so by nets. The amount of fish recaptured within the 7th (19%) and 8th (21%) day after the escape accounted for 40% of the total recaptured biomass (Fig. 4). Half of the total escaped biomass was recaptured within the first three weeks and the last remarkable recapture event was registered two months after the escape, with a total of 95.6% of the total escaped biomass recaptured at that time (Fig. 4). In November, the bulk of the recaptured biomass (90.5%; 44,828 kg) was landed by means of fish traps (Figs. 4 and 5) and only the first fishing day (3rd of November), nets were responsible of higher landings than fish traps (Fig. 5). Through November and December, differences in the mean cpue values (±SE) of fish traps and nets were found (pseudoF7.6; 0.01; Fig. 6) showing higher for fish traps (262 ± 14.5 kg day1 boat1) than for nets (86 ± 1.1 kg day1 boat1; t3.7; 0.0002), whereas in December, no differences were found (t0.9; 0.45), resulting the mean cpue value 93 ± 2.98 kg day1 boat1 (±SE; Fig. 6).
4. Discussion This is the first study showing an effective recapture of escaped fish after a massive escape event within the Mediterranean boundaries. The recapture success responded to the distance to
Fig. 3. Dispersion plot showing landed biomass values of gilthead sea bream (Sparus aurata; Y axis) versus distance to farm (X axis). The dashed line corresponds to the best fitting exponential model obtained.
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Fig. 4. Bar plot depicting the recapture frequencies of gilthead sea bream (Sparus aurata) biomass (Y axis), by means of fish traps (light grey) and nets (dark grey) through time (X axis). The asterisk (*) indicates the end of the fishing permit to use fish traps.
farm, taking place along up to 11 km of the coast. The incidence of escapees in the artisanal fishermen catches spanned throughout seven months, being higher through the first two months after the escape event. The first two weeks following the escape showed important for the recapture of escapees, especially the first days, when nearly half of the landed biomass was captured. A total of 64.7% of the escaped fish was recaptured by local fisheries, being fish traps (53.8%) more effective than nets (10.9%). 4.1. Interaction between escaped fish and local fisheries
Fig. 5. Bar plot depicting the accumulated frequency (%) of the gilthead sea bream (Sparus aurata) biomass recaptured (Y axis) as a function of the number of days after the escape (X axis) by netters (dark grey) and trappers (light grey). The dotted line represents the total accumulated proportion of recaptured biomass.
Fig. 6. Whiskers box plot showing differences in the mean capture per unit of effort (cpue) of netters (A) and fish trap fishermen (B) in November, compared to the same tier to nets in December (B*), once the netters (A) and fish trappers which changed me permit to use traps expired by the last of November. Different colours indicate significant differences among groups.
The distance to the escape point showed correlated to the recapture success of escaped individuals, since larger biomasses of escapees were recaptured in fish traps next to the escape point than far away. Similarly, Toledo-Guedes et al. (2009) described decreasing abundances of escaped European sea bass as moving away from the farms. The dispersion of the escaped fish spanned 11 km along the coast, based on the landings of the fish trap nets pez et al. (2012) did not detect (fix gear). Similarly, Arechavala-Lo the recapture of tagged fish further than 10e15 km from the escape point, whereas, Toledo-Guedes et al. (2014a) described escapees being landed 50 km off the escape. Since gilthead sea bream is a demersal species, the narrower continental shelf present in Canary Islands could have made individuals disperse further distances along the shore. In the present case, the lack of abnormal captures of gilthead seabream landed in the nearest fish markets indicates that dispersion of escapees did not span more than 30 km off the escape point. The incidence of escaped fish was noticeable throughout the next seven months after the escape. Similarly, Toledo-Guedes et al. (2014a) detected the incidence of escaped sea bass in fisheries landings over a period of more than 12 months after a massive escape in Canary Islands. Along the recapture period, the pattern of escapees landings described by Toledo-Guedes et al. (2014a) showed constant, while in our case a dramatic biomass was landed in the first weeks after the escape. The latter could be due to the high success of fish traps, which might have recaptured the main bulk of the escaped fish faster than if only nets would have been used. The recapture efficiency of the fishing fleet resulted in 64.7%, the largest reported for a large-scale escape event so far. Other studies stress the low recapture success once the fish have escaped (SerraLinares et al., 2013; Noble et al., 2013) and only Chittenden et al. (2011) reported high recapture rates using coastal fish bags during the first month after the simulated escape. However, less than 40 acoustically tagged individuals were released in this study. In
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this study, nets responded faster to the recapture of escapees than fish traps since the latter are anchored to the shoreline whereas nets can be deployed in higher depths closer to fish farms. Interestingly, the presence of escapees swimming alive inside the fish traps may exert an attraction effect over their counterparts, driving to a higher recapture success and it should be further studied. Moreover, fish traps might bring advantages to farmers compared to other fishing gears e.g. live fish can be harvested from fish traps to minimize the economic loss by reallocating the fish in the sea cages. 4.2. Guidelines for the design of a contingency plan for fish escapes In the main fish-producing countries as Norway, Canada, United States, Australia, Scotland or more recently Chile, sea cage aquaculture together with potential escape events are specifically regulated under a legal framework (all links in Izquierdo-Gomez et al., 2014), either preventing or mitigating the negative effects of escapees. All actions taking place from the declaration of the escape until its control, are included in a contingency plan for fish escapes, which is compulsory to obtain a new aquaculture licence. Therefore, similar contingency plans should be developed within an adaptive management framework in all Mediterranean fin-fish producers. In case a fish escape occurs, a rapid response informing the authorities about an escape event is needed to initiate as quickly as possible the recapture actions to minimize the dispersion of the escapees (fishing actions defined further in the text). Since the studied escape event occurred on Friday evening (31st Oct 2003), the escapees dispersed over the weekend before fishermen set their fish traps and nets (professional fishermen cannot fish during weekend days). Thus, the escape detection system should be active during non-working days or bank holidays, as well as wellcoordinated with authorities for a quick response. In order to trigger the escape alarm, it must be defined what an escape event is and it should be quantifiable in terms of fish number and/or escaped biomass. In case the farmer does not inform the authorities, an independent escape alarm system triggered when abnormal catches of a given cultured species occur is suggested (field surveys and/or monitoring further described in the text). Eventually, if the authorities are not informed by farmers, legal actions (to be developed) should be carried out against fish farming enterprises. Once the escaped event is declared and no longer than a week after, the farmer should issue a first report to the authority describing the causes of the escape, species and quantity of escaped fish/biomass. All damages occurring at the fish farm facility must be repaired as quickly as possible and a photographic document of the damaged structures must be included in the first report. The medical condition of the fish must be included in the report as well, since medicated fish may contain active substances and thus, public health issues may arise from the uncontrolled consumption of escaped fish (Sapkota et al., 2008). Based on the aforementioned behaviour of escaped fish, which seek refuge in shallow areas near the shoreline, farmers must come to an agreement with the authorities to pre-set the recapture actions to be carried out before an escape event occurs. The fishing gear, distance to the fish farm and the areas to distribute the fishing effort, as well as the economic terms, should be mandatorily agreed to mitigate the effects of potential escape events as cost-effectively as possible. Due to the strong ability to recapture escaped fish shown by artisanal fishermen, this professional guild should be taken into account for the planning of the recapture actions. The first days after the escape event are critical, thus the fishing actions must be carried out around the farm and thereafter along the
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nearest shallow areas from the escape point throughout a month. The authority should hold the right to extend the duration of the fishing activities according its success and the abnormal presence of escapees in the area. As a consequence of the high recapture success of fish traps, its usage is strongly advised if not the construction of a customized version optimized for specific areas next to the fish farms. However, the usage of fish traps is only allowed along certain periods of the year and in certain parts of the Mediterranean Sea. Therefore, special permits should be issued to set fish traps when a massive escape takes place. In the same way, the usage of nets have constraints regarding the distance to the shore (200 m) and given the behaviour of escaped fish seeking refuge in shallow waters and closed inlets, a special permit should be issued to allow the usage of nets in swimming zones (e.g. beaches, creeks). Beach-seines were prohibited a few decades ago but its usage should be considered as they are adapted to fish in the preferred areas for escapees. During the recapture actions, by-catch composed by non-targeted species could be released since fish traps and beach-seines might not kill the fish. During the recapture actions, parameters as the captured species, fish sizes and the recapture success should be always surveyed by the authorities not to jeopardize the stock of other species or the wild conspecific population. The usage of identification tools resulting from PREVENT ESCAPE project (http://preventescape.eu) are advised to discern between wild and escaped fish, especially the presence of ontogenic scales (Arechavala-Lopez et al., 2013b). The authorities should inform the users of the coastal zone (e.g. swimmers, tourism or recreational fishermen) to prevent social conflicts arising from the unusual presence of professional fishing carrying out legal recapture activities in shallow areas. In case the authorities are not present, passive fishing gears should be clearly labelled indicating its legal status, purpose and contact information of the authorities. In addition, it must be noticeable to prevent accidents derived from entanglement of coastal users. Surveys to monitor the presence of escapees should be carried out through the whole year. Areas of ecological importance, if existing, should be included in the survey (i.e. Natura2000 zones and marine protected areas). In case of escapees of locally absent species as meagre (A. regius), the visual identification would be simple, whereas in case of gilthead sea bream or European sea bass, either individuals of similar sizes to those which escaped or abnormal schools of fish would trigger the alarm. In case that high abundances of escapees are still detected once the recapture actions are completed, the contingency plan must be activated again. If the abundances are low or escapees invade protected areas, eradication measures as underwater fishing should be activated due to its high specificity. Once the presence of escapees is no longer detected, authorities will continue with the normal monitoring program of escapees. In parallel, the fish farm should be inspected by the authority to validate the actions conducted to repair the reported damages after the escape. Long term monitoring data of the escapees or the incidence of escape events, could be used to validate further strategies to prevent fish escapes as it occurred with the new standard of materials implemented in Norway in 2004 (NS9415; LOV-2005-06-17-79-x12); It was concluded that, the introduction of a new standard of materials led to a dramatic reduction in the number of major escape incidents in Norway (Jensen et al., 2010). An effective management of sea cage aquaculture will only be possible if the escape events are declared to authorities. Once the fishing actions to recapture escaped fish conclude, the farmer must report in detail to the authority with the causes of the escape, structural damages and economic losses, together with the description of the recapture actions (e.g. fishing gear, spatiotemporal distribution of the fishing effort, main affected areas,
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recapture success, hot-spots of recapture, medical condition of the fish, etc …). The latter will be issued in a standardized report sheet (to be created when designing the regulation of escape events). In case the presence of escapees is still high when the fishing permit issued for recapture purposes expires, the farmer should request the authorities to extend the permit to carry on with the recapture actions. Eventually, the information contained in the final report provided by farmers and the data obtained from the monitoring program of escapees will be used to improve the former contingency plan to better address the fishing effort of the recapture actions towards the areas where escapees prefer to disperse. In last term, the escape event and its features (e.g. magnitude, species, fish sizes, medical condition, causes and date) should be registered in a data base for a detailed control of the escape events which will be available for future research. Summarizing, this is the first time that the recapture process after a large-scale escape event of gilthead sea bream has been analysed in detail through fisheries landings. The obtained results showed valuable to design mitigation measures to be implemented in future aquaculture regulations of coastal Mediterranean countries, which are inexistent so far. It is suggested that either the procedure to inform authorities or the recapture actions to be carried out after a fish escape event, are mandatorily issued together with the environmental impact assessment for its approval, in order to obtain the licence for fish farming activities. Despite the existing regulations for escape events of Atlantic salmon (S. salar) provide valuable information, further specific studies focussing on the recapture of species reared in the Mediterranean Sea (i.e. gilthead sea bream, European sea bass and meagre) are critical. Only through data-based management measures, the sustainable development of the aquaculture industry along the Mediterranean coast will be achieved. Acknowledgements Special thanks to the administration staff of the landing port of Aguilas for providing us with the landings data sets. This research was part of ESCAFEP project, cofounded by the European Fisheries Fund (EFF) and the Biodiversity Foundation, in collaboration with the Spanish Ministry of Agriculture, Food and Environment. References Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. Permanovaþ for PRIMER. Primer-E, Plymouth, UK. Arechavala Lopez, P., Uglem, I., Fernandez-Jover, D., Bayle-Sempere, J.T., SanchezJerez, P., 2011. Immediate post-escape behaviour of farmed seabass (Dicentrarchus labrax L.) in the Mediterranean Sea. J. Appl. Ichthyol. 27, 1375e1378. http://dx.doi.org/10.1111/j.1439-0426.2011.01786.x. Arechavala-Lopez, P., Uglem, I., Fernandez-Jover, D., Bayle-Sempere, J.T., SanchezJerez, P., 2012. Post-escape dispersion of farmed seabream (Sparus aurata L.) and recaptures by local fisheries in the western Mediterranean Sea. Fish. Res. 121, 126e135. http://dx.doi.org/10.1016/j.fishres.2012.02.003. Arechavala-Lopez, P., Izquierdo-Gomez, D., Sanchez-Jerez, P., 2013a. First report of a swordfish (Xiphias gladius Linnaeus, 1758) beneath open-sea farming cages in the western Mediterranean Sea. Mediterr. Mar. Sci. 15, 72e73. http://dx.doi.org/ 10.12681/mms.503. Arechavala Lopez, P., Fernandez-Jover, D., Black, K.D., Ladoukakis, E., BayleSempere, J.T., Sanchez-Jerez, P., Dempster, T., 2013b. Differentiating the wild or farmed origin of Mediterranean fish: a review of tools for sea bream and sea bass. Rev. Aquac. 5, 137e157. http://dx.doi.org/10.1111/fme.12129. pez, P., Izquierdo Go mez, D., Uglem, I., Sa nchez Jerez, P., 2014a. AgArechavala Lo gregations of bluefish Pomatomus saltatrix (L.) at Mediterranean coastal fish farms: seasonal presence, daily patterns and influence of farming activity. Environ. Biol. Fishes. http://dx.doi.org/10.1007/s10641-014-0280-5. Arechavala Lopez, P., Izquierdo-Gomez, D., Sanchez-Jerez, P., Bayle-Sempere, J.T., 2014b. Simulating escapes of farmed sea bass from Mediterranean open seacages: low recaptures by local fishermen. J. Appl. Ichthyol. 30, 185e188. http:// dx.doi.org/10.1111/jai.12357. € Arechavala-Lopez, P., Borg, J.A., Segvi c-Bubi c, T., Tomassetti, P., Ozgül, A., SanchezJerez, P., 2015a. Aggregations of wild Atlantic Bluefin Tuna (Thunnus thynnus L.)
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Sci. 63, 1182e1189. http:// dx.doi.org/10.1016/j.icesjms.2006.04.006. € € I.B., Jonsson, B., Balstad, T., Lamberg, A., 2000. Fleming, I.A., Hindar, K., MjOlner Od, Lifetime success and interactions of farm salmon invading a native population. Proc. R. Soc. Lond. Ser. B Biol. Sci. 267, 1517e1523. http://dx.doi.org/10.1098/ rspb.2000.1173. Food and Agriculture Organization of the United Nations. FIGIS. FishStat (Database). (Latest update: 31 Jan 2014) URI: http://data.fao.org/ref/babf3346-ff2d-4e6c9a40-ef6a50fcd422.html?version¼1.0. Gausen, D., Moen, V., 1991. Large-scale escapes of farmed Atlantic salmon (Salmo salar) into Norwegian rivers threaten natural populations. Can. J. Fish. Aquatic Sci. 48, 426e428. http://dx.doi.org/10.1139/f91-055. Glamuzina, B., Pesi c, A., Joksimovi c, A., Glamuzina, L., Mati c-Skoko, S., Conides, A., Klaoudatos, D., Zacharaki, P., 2014. Observations on the increase of wild gilthead seabream, Sparus aurata abundance, in the eastern Adriatic Sea: problems and opportunities. Int. Aquatic Res. 6, 127e134. http://dx.doi.org/10.1007/s40071014-0073-7. Hansen, L.A., Dale, T., Uglem, I., Aas, K., Damsgård, B., Bjørn, P.A., 2008. Escape related behaviour of Atlantic cod (Gadus morhua L.) in a simulated farm situation. Aquac. Res. 40, 26e34. http://dx.doi.org/10.1111/j.13652109.2008.02057.x. Heggberget, T.G., Johnsen, B.O., Hindar, K., Jonsson, B., Hansen, L.P., Hvidsten, N.A., Jensen, A.J., 1993. Interactions between wild and cultured Atlantic salmon: a review of the Norwegian experience. Fish. Res. 18, 123e146. http://dx.doi.org/ 10.1016/0165-7836(93)90044-8. Izquierdo-Gomez, D., Fernandez-Jover, D., Sanchez-Jerez, P., Toledo-Guedes, K., rez, C., 2014. Guia de buenas practicas Arechavala-Lopez, P., Forcada, A., Valle-Pe para la gestion de escapes en la acuicultura marina, vol. II. Mitigacion. (ISBN: 978-84-606-5522-0). ~ a, G., Borg, J.A., Jackson, D., Drumm, A., McEvoy, S., Jensen, Ø., Mendiola, D., Gabin Papageorgiou, N., Karakassis, Y., Black, K.D., 2015. A pan-European valuation of the extent, causes and cost of escape events from sea cage fish farming. Aquaculture 436, 21e26. http://dx.doi.org/10.1016/j.aquaculture.2014.10.040. Jensen, Ø., 2006. Assessment of Technical Requirements for Floating Fish Farmsdbased on Escape Incidents January 2006. Rep no SFH80 A066056. ISBN 8214-03953-8. SINTEF, Trondheim (in Norwegian). Jensen, Ø., Dempster, T., Thorstad, E.B., Uglem, I., Fredheim, A., 2010. Escapes of fishes from Norwegian sea-cage aquaculture: causes, consequences and prevention. Aquac. Environ. Interact. 1, 71e83. http://dx.doi.org/10.3354/aei00008. Jonsson, B., Jonsson, N., 2006. Cultured Atlantic salmon in nature: a review of their ecology and interaction with wild fish. ICES J. Mar. Sci. J. du Conseil 63, 1162e1181. http://dx.doi.org/10.1016/j.icesjms.2006.03.004. Milner, N.J., Evans, R., 2003. The incidence of escaped Irish farmed salmon in English and Welsh rivers. Fish. Manag. Ecol. 10, 403e406. http://dx.doi.org/ 10.1111/j.1365-2400.2003.00348.x. Moe, H., Dempster, T., Sunde, L.M., Winther, U., Fredheim, A., 2007. Technological solutions and operational measures to prevent escapes of Atlantic cod (Gadus morhua) from sea-cages. Aquac. Res. 38, 91e99. http://dx.doi.org/10.1111/ j.1365-2109.2006.01638.x. Naylor, R., Hindar, K., Fleming, I.A., Goldburg, R., Williams, S., Volpe, J., Whoriksey, F., Eagle, J., Keslo, D., Mangel, M., 2005. Fugitive salmon: assessing the risks of escaped fish from net-pen aquaculture. Bioscience 55, 427e437. http:// ́ ́ dx.doi.org/10.1641/0006-3568(2005)055[0427:FSATRO]2.0.CO;2. ́ R.D., Uglem, I., Papadakis, V.M., Papadakis, V.M., Papadakis, ́ Noble, C., Hedger, I.E., Glaropoulos, A., Kentouri, M., Smith, C.J., Zimmermann, E., Fleming, I.A., Høy, E., Damsgård, B., 2013. General conclusions and recommendations for preventing and mitigating escape-related fish behaviour. In: PREVENT ESCAPE Project
D. Izquierdo-Gomez, P. Sanchez-Jerez / Ocean & Coastal Management 122 (2016) 57e63 Compendium. Chapter 3.5. Commission of the European Communities, 7th Research Framework Program. ISBN: 978-82-14-05565-8. www.preventescape. eu. Norwegian Ministry of Fisheries and Coastal Affairs, 2008. Aquaculture Operations Regulations with Remarks. Norwegian Ministry of Fisheries and Coastal Affairs, Bergen. Available at: http://www.lovdata.no/cgi-wift/ldles?doc¼/sf/sf/sf20080617-0822.html (in Norwegian). Sapkota, A., Sapkota, A.R., Kucharski, M., Burke, J., McKenzie, S., Walker, P., Lawrence, R., 2008. Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ. Int. 34, 1215e1226. http:// dx.doi.org/10.1016/j.envint.2008.04.009. , R., 1980. La pe ^che du thon au thonaire en Me diterrane e. ICCAT Col. Vol. Sci. Sara Pap. 11, 351e366. Serra-Llinares, R., Nilsen, R., Uglem, I., Arechavala-Lopez, P., Bjørn, P.A., Noble, C., 2013. Post-escape dispersal of juvenile Atlantic cod (Gadus morhua) from Norwegian fish farms and their potential for recapture. Aquac. Environ. Interact. 3, 107e116. http://dx.doi.org/10.3354/aei00051. Ljubkovi Segvi c-Bubi c, T., Lepen, I., Trumbi c, Z., c, J., Sutlovi c, D., Mati c-Skoko, S., Grubisi c, L., Glamuzina, B., Mladineo, I., 2011a. Population genetic structure of reared and wild gilthead sea bream (Sparus aurata) in the Adriatic sea inferred with microsatellite loci. Aquaculture 318, 309e315. http://dx.doi.org/10.1016/ j.aquaculture.2011.06.007. Segvi c-Bubi c, T., Grubisi c, L., Karaman, N., Ti cina, V., Jelavi c, K.M., Katavi c, I., 2011b. Damages on mussel farms potentially caused by fish predationdself-service on the ropes? Aquaculture 319, 497e504. http://dx.doi.org/10.1016/ j.aquaculture.2011.07.031. Segvi c-Bubi c, T., Talijan ci c, I., Grubisi c, L., Izquierdo-Gomez, D., Katavi c, I., 2014. Morphological and molecular differentiation of wild and farmed gilthead sea bream Sparus aurata: implications for management. Aquac. Environ. Interact. 6, 43e54. http://dx.doi.org/10.3354/aei00111.
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Soto, D., Jara, F., Moreno, C., 2001. Escaped salmon in the inner seas, southern Chile: facing ecological and social conflicts. Ecol. Appl. 11, 1750e1762. http:// dx.doi.org/10.1890/1051-0761(2001)011[1750:ESITIS]2.0.CO;2. Slack-Smith, R.J., 2001. Fishing with traps and pots (No. 26). Food & Agric. Org. ISBN: 92-5-104307-8. nchez-Jerez, P., Gonza lez-Lorenzo, G., Herna ndez, A.B., 2009. Toledo-Guedes, K., Sa Detecting the degree of establishment of a non-indigenous species in coastal ecosystems: sea bass Dicentrarchus labrax escapes from sea cages in Canary islands (Northeastern Central Atlantic). Hydrobiologia 623, 203e212. http:// dx.doi.org/10.1007/s10750-008-9658-8. Toledo Guedes, K., Sanchez-Jerez, P., Brito, A., 2014a. Influence of a massive aquaculture escape event on artisanal fisheries. Fish. Manag. Ecol. 21, 113e121. http://dx.doi.org/10.1111/fme.12059. Toledo-Guedes, K., Sanchez-Jerez, P., Benjumea, M.E., Brito, A., 2014b. Farming-up coastal fish assemblages through a massive aquaculture escape event. Mar. Environ. Res. 98, 86e95. http://dx.doi.org/10.1016/j.marenvres.2014.03.009. Valero Rodríguez, J.M., Toledo-Guedes, K., Arechavala-Lopez, P., IzquierdoGomez, D., Sanchez-Jerez, P., 2015. The use of trophic resources by Argyrosomus regius (Asso, 1801) escaped from Mediterranean offshore fish farms. J. Appl. Ichthyol. 31, 10e15. http://dx.doi.org/10.1111/jai.12649. Walker, A.M., Beveridge, M.C.M., Crozier, W., O'Maoileidigh, N., Milner, N., 2006. Monitoring the incidence of escaped farmed Atlantic salmon, Salmo salar L., in rivers and fisheries of the United Kingdom and Ireland: current progress and recommendations for future programmes. Ices J. Mar. Sci. 63, 1201e1210. http:// dx.doi.org/10.1016/j.icesjms.2006.04.018. Webb, J.H., Hay, D.W., Cunningham, P.D., Youngson, A.F., 1991. The spawning behaviour of escaped farmed and wild adult Atlantic salmon (Salmo salar L.) in a northern Scottish river. Aquaculture 98, 97e110. http://dx.doi.org/10.1016/ 0044-8486(91)90375-H.
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Management of fish escapes from Mediterranean Sea cage aquaculture through artisanal fisheries D. Izquierdo-Gomez*, P. Sanchez-Jerez Marine Science and Applied Biology Department, University of Alicante, 03690 Alicante, Spain
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 June 2015 Received in revised form 7 January 2016 Accepted 10 January 2016 Available online 28 January 2016
Fish escaping from net pens have always been considered a major source of socioeconomic and ecological issues entitling high economic loses for farmers. Local artisanal fisheries have proved the ability to mitigate escape events by recapturing escapees, but its effectiveness has always been questioned. However, the knowledge regarding the interaction of large scale escape events and local fisheries remains scant. The recapture dynamics of a massive escape of nearly 100 tones taking place in Western Mediterranean was analysed. The artisanal fishery showed efficient in recapturing escaped fish as 64.7% of the escaped biomass was recovered. The spatial distribution of escaped gilthead seabream along the shore was studied as well as the efficiency of the fishing fleet distinguishing between fishing gears. The recapture of escaped fish showed well correlated with the distance to the escape point. Moreover, a high recapture success (64.7%) was registered being fish traps (53.8%) more efficient in recovering escapees than nets (10.9%). Concluding, management implications and data-based measures to be implemented on further regulations of escape events are discussed. © 2016 Elsevier Ltd. All rights reserved.
Keywords: Small-scale fisheries Fish farm Gilthead Net pens Coastal zone management
1. Introduction Fish escaping from marine fish farms have always been considered a major source of socioeconomic and ecological issues (Hegberet et al., 1993; Fleming et al., 2000; Soto et al., 2001; Naylor et al., 2005; Johnson and Johnson, 2006; Jensen et al., 2010). Between 2009 and 2012, Jackson et al. (2015) claimed more than 8 million fish escaping from European farms with 77.6% corresponding to gilthead seabream (Sparus aurata) reared in the Mediterranean Sea. The derived economic loss resulted V47.5 million per annum, on average; V42.8 million due to escapes of sea bass and sea bream in the Mediterranean Sea and V4.7 million for salmon in Northern Europe (Jackson et al., 2015). Such problem was described decades ago from Atlantic salmon and cod escaping from sea cages of northern European countries (Gausen and Moen, 1991; Web et al., 1991; Milner and Evans, 2003; Butler et al., 2005; Fiske et al., 2006; Walker et al., 2006). Norway, as the main Atlantic salmon producer shed light on the causes driving salmon and cod escape events based on its national record of escapes, available since 2001 (Jensen et al., 2006, 2010; Moe et al., 2007; Hansen et al.,
* Corresponding author. E-mail address: [email protected] (D. Izquierdo-Gomez). http://dx.doi.org/10.1016/j.ocecoaman.2016.01.003 0964-5691/© 2016 Elsevier Ltd. All rights reserved.
2008). The main causes driving escapes resulted in different structure failures, operational errors and biological causes (netbiting), all combined with a high stress situations for materials during storms (Jensen et al., 2010; Jackson et al., 2015). Consequently, the implementation of a new technical standard (NS9415) for the materials of open sea fish farms was linked with a remarkable decrease of escape events in the following years (Jensen et al., 2010). In addition, new management measures were included in the national regulation of aquaculture (Norwegian Ministry of Fisheries and Coastal Affairs (2008)) as: mandatory reporting of all escape incidents, establishment of the Norwegian Escapes Commission, introduction of enforceable technical regulations for the design, dimensioning, installation and operation of sea cage farms, investment in research and development projects and training of fish farm operators to prevent escapes (Jensen et al., 2010). Nowadays, the escape events in all main fish producing countries in northern Europe (e.g. Norway, United Kingdom), America (e.g. Canada, United States and Chile) together with Australia are regulated by a specific framework, which, in general, is entailed in the aquaculture regulation of the country (all links at IzquierdoGomez et al., 2015). However, although since early eighties (FAO Fishstat, 2014) there is a growing Mediterranean market of reared gilthead seabream (S. aurata), European seabass (Dicentrarchus
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labrax) and more recently meagre (Argyrosomus regius), none of the main fish-producing coastal countries (i.e. Croatia, France, Greece, Italy, Spain, Turkey) yet provides specific regulation of fish escapes. Thus, a pan-Mediterranean scenario where fish escaping from sea cages influence the coastal ecosystem via gene introgression on populations of wild conspecifics (Segvi c-Bubi c et al., 2011a, 2014) and compete for food and habitat with other species (ArechavalaLopez et al., 2012; Valero-Rodrígez et al., 2015; Toledo-Guedes et al., 2014b) occurs. Furthermore, negative interactions with other forms of aquaculture (Segvi c-Bubic et al., 2011b; Glamuzina et al., 2014) have been described, together with influences either on the behaviour of high valued targeted species of predators (Arechavala-Lopez et al., 2013a, 2014a; 2015a) or on fisheries landings of the reared species (Dimitrou et al., 2007; ArechavalaLopez et al., 2015b). Local artisanal fisheries have proved very effective in mitigating escape events, but the knowledge regarding the interaction of large scale escape events with fisheries is still scarce. There is only one study (Toledo-Guedes et al., 2014a) providing data about fisheries catches after a massive escape of sea bass and sea bream in Canary Islands. Other studies based on experimental escapes involving several hundreds of externally tagged individuals and tenths of acoustically tagged fish (Arechavala et al., 2011, 2012, 2014b) provide valuable information, however, the results may not mirror the real scenario occurring after the escape of tens of thousands of fish. In this study, the recapture dynamics of a massive escape of nearly 100 tones taking place in Western Mediterranean was analysed. In addition, this study was conducted according to the principles of the new framework proposal for maritime spatial planning and integrated coastal management (ICZM; COM, 2013), which indicates that both the prevention and the mitigation of fish escapes from aquaculture should be taken into account by Mediterranean countries when developing integrated coastal zone management plans. The aim of this research is to provide valuable information to design knowledge-based mitigation measures of fish escapes within the Mediterranean Sea, with the specific goal of reducing the derived ecological and socio-economic issues. Thus, the spatial distribution of escaped gilthead seabream along the shore was studied based on the sea bream catches of local fisheries over time. In second term, the recapture efficiency of the whole fleet distinguishing between fishing gears was as well inspected. As a conclusion, a set of valuable guidelines to design contingency and control plans of fish escapes were outlined. 2. Materials and methods 2.1. Study area Aguilas (37 24.7060 N; 1 34.9700 W) is a town located in the southeast of Spain where fishing activities have been traditionally carried out. The commercial fleet is composed by trammelnetters (20), purse-seiners (3), long liners (2) and trawlers (10). The fishing effort of trammel-netters is distributed from cabo Cope (37 25.6530 N; 1 29.2510 W) to few km south of the marina of Aguilas, being generally circumscribed to depths from 10 to 60 m over an area of about 40 km2. Along the coast, sandy/rocky beaches with sandy bottoms patched with hard substrata and seagrass beds (Posidonia oceanica) are found from 1 m to 30 m depth. The studied fish farm is located at 500 m from the coast line (37 24.8180 N; 1 32.1220 W) at 40e60 m depth, where, about 200 tons of fish (D.labrax, S. aurata and A. regius) are reared per annum in 26e28 cages (25 m diam.) from about 20 years ago. Recreational and underwater fishing activities are widely carried out in the area, as well as scuba diving, being Calabardina (37 25.6080 N; 1 30.1550 W) one of the most concurred areas in the Levantine coast of Spain.
2.2. Description of the fishing gears and m etiers of the artisanal fishery Trammel-nets, with slight differences in mesh sizes, targeting Scorpaena spp., Sepia officinalis, and Mullus spp., are the most common fishing gear used by the artisanal fishing fleet in Aguilas, being its usage coupled with the biology and the abundances of each targeted species along the whole year. Octopus pots are used as well in different periods from May to September. The fishing gear “moruna” (hereafter referred as fish trap) responds to an arrow-head fixed trap (Slack-Smith, R. J. 2001) smaller than the “almadraba” (Thunnus thynnus trap), used since the Roman , 1980). The usage of fish traps is legally regulated and, Era (Sara depending on the targeted species (Loligo vulgaris, Seriola dummerilli or Sarda sarda), it is constructed differently, being its usage coupled with the biology and migration of the targeted species. Each fish trap is crafted and it must be authorized by the legal authority before it can be used. The potential locations to place the fish traps are traditionally set from decades, being assigned by draw to any fishermen deciding to use fish traps in a given season. In this research, the fish trap targeting Sarda sarda, deployed from September 15th to the last of November was studied. Nets are the only gear used by the fishing fleet as the permit to use fish traps expires the last of November. 2.3. Escape description and fisheries catches The capture of gilthead sea bream in the study area is common but not abundant compared to adjacent areas, being caught a mean biomass (±SE) of 59 ± 13.9 kg month1 along 2003 and 2004 without taking into to account the months where captures were influenced by the escape event. The escape event took place the last of October 2003 after a storm and SW winds of 13.3 knots together with waves of 3.2 m high, which damaged one sea cage. A total biomass of 93,600 kg of commercial sized gilthead sea bream escaped, being clearly noticeable the increase of its captures in the landings of artisanal fishermen (Fig. 1). 2.4. Statistical analyses In terms of the spatial distribution of the escaped fish, a nonlinear regression model was fitted using landings data derived from the fish trap fishery as independent variable and distance to the farm as control variable using SPSS statistical software package v15.0 (SPSS Inc, Chicago, IL, USA; www.ibm.com/SPPS_statistics). To unveil the recapture efficiency of the local fishing fleet, the daily landed biomass of escaped gilthead sea bream was inspected in terms of accumulated frequency of landed biomass after the escape. Differences in the mean CPUE (capture per unit of effort) of both gears (fish traps and nets) expressed in landed kilogrammes of escaped gilthead seabream $ day1 $ boat1 were analysed by means of one way PERMANOVA design using PRIMER V6.1.13 computer program (Clarke and Gorley, 2006) with the PERMANOVA þ V1.0.3 add-on package (Anderson et al., 2008). To detect further dispersion of the escapees, the catch data of the nearest landing ports was also inspected. All data was obtained from the fish market of Aguilas and the regional fisheries authorities of Murcia. 3. Results The escape event occurred between the last of October and the 1st of November of 2003 when maximum waves height of 6 m were registered in the evening. All fish traps were set along 11 km of coast following the shoreline (Fig. 2). The captured biomass of fish
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Fig. 1. A) Bar plot depicting the daily landed biomass (Y left axis) of gilthead sea bream (Sparus aurata) by artisanal fishermen in Aguilas (Murcia, SE Spain). Dots correspond to number of fishing boats per day (grey) and the total number of boats censused per year (black). B) Detailed daily landings of recaptured fish. Notice left Y axis is shared with A figure. The asterisk (*) indicates the day of the escape: 31-Oct-2003.
traps showed inversely correlated to the distance to the escape site (F ¼ 14.23; p-value ¼ 0.009), according to the best fitting exponential regression model (Fig. 3). The closest fish trap (C; Fig. 2) was located at ca.1441 m, however, it did not capture the larger biomass of escaped seabream which corresponded to the fish trap D (2nd in distance; 1552 m) located 100 m further south which caught a total biomass of 14,126 kg of gilthead sea bream. The influence of escaped fish was noticed along 7 months (NovembereMay, 2003), being the highest gilthead sea bream biomasses landed along November and December 2003. The mean landed biomass (±SE) in the first two weeks of study was 4281 ± 2064 kg and 2132 ± 501 kg respectively, showing thereafter a decreasing trend ranging from 639.74 ± 222.48 kg to 0.83 ± 0.48 kg in December and May respectively. The incidence of escaped fish was not noticeable in the closest landing ports located ca. 35 km both to the north and to the south to the escape event (landings data not shown). Neither purse-seiners nor trawling fleets landed higher biomasses of gilthead sea bream compared to previous years (data not shown). A total biomass of 60,577 kg was landed in 84 fishing days, representing 64.7% of the escaped fish biomass. A total of 53.8% of the recaptured biomass was caught by means of fish traps while
Fig. 2. Map of the study area showing the location of “morunas” (arrow-head shape fish traps) with a given letter (A, B, C, D, E, F, G and H), together with the yielded biomass of escaped fish per trap (Y axis). The fish farm, located between fish traps B and C, is aligned at 0 m in the X axis, which corresponds to the escape point. Recaptured biomass form traps H to A correspond to bars from left to right in the X axis, respectively.
10.9% was so by nets. The amount of fish recaptured within the 7th (19%) and 8th (21%) day after the escape accounted for 40% of the total recaptured biomass (Fig. 4). Half of the total escaped biomass was recaptured within the first three weeks and the last remarkable recapture event was registered two months after the escape, with a total of 95.6% of the total escaped biomass recaptured at that time (Fig. 4). In November, the bulk of the recaptured biomass (90.5%; 44,828 kg) was landed by means of fish traps (Figs. 4 and 5) and only the first fishing day (3rd of November), nets were responsible of higher landings than fish traps (Fig. 5). Through November and December, differences in the mean cpue values (±SE) of fish traps and nets were found (pseudoF7.6; 0.01; Fig. 6) showing higher for fish traps (262 ± 14.5 kg day1 boat1) than for nets (86 ± 1.1 kg day1 boat1; t3.7; 0.0002), whereas in December, no differences were found (t0.9; 0.45), resulting the mean cpue value 93 ± 2.98 kg day1 boat1 (±SE; Fig. 6).
4. Discussion This is the first study showing an effective recapture of escaped fish after a massive escape event within the Mediterranean boundaries. The recapture success responded to the distance to
Fig. 3. Dispersion plot showing landed biomass values of gilthead sea bream (Sparus aurata; Y axis) versus distance to farm (X axis). The dashed line corresponds to the best fitting exponential model obtained.
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Fig. 4. Bar plot depicting the recapture frequencies of gilthead sea bream (Sparus aurata) biomass (Y axis), by means of fish traps (light grey) and nets (dark grey) through time (X axis). The asterisk (*) indicates the end of the fishing permit to use fish traps.
farm, taking place along up to 11 km of the coast. The incidence of escapees in the artisanal fishermen catches spanned throughout seven months, being higher through the first two months after the escape event. The first two weeks following the escape showed important for the recapture of escapees, especially the first days, when nearly half of the landed biomass was captured. A total of 64.7% of the escaped fish was recaptured by local fisheries, being fish traps (53.8%) more effective than nets (10.9%). 4.1. Interaction between escaped fish and local fisheries
Fig. 5. Bar plot depicting the accumulated frequency (%) of the gilthead sea bream (Sparus aurata) biomass recaptured (Y axis) as a function of the number of days after the escape (X axis) by netters (dark grey) and trappers (light grey). The dotted line represents the total accumulated proportion of recaptured biomass.
Fig. 6. Whiskers box plot showing differences in the mean capture per unit of effort (cpue) of netters (A) and fish trap fishermen (B) in November, compared to the same tier to nets in December (B*), once the netters (A) and fish trappers which changed me permit to use traps expired by the last of November. Different colours indicate significant differences among groups.
The distance to the escape point showed correlated to the recapture success of escaped individuals, since larger biomasses of escapees were recaptured in fish traps next to the escape point than far away. Similarly, Toledo-Guedes et al. (2009) described decreasing abundances of escaped European sea bass as moving away from the farms. The dispersion of the escaped fish spanned 11 km along the coast, based on the landings of the fish trap nets pez et al. (2012) did not detect (fix gear). Similarly, Arechavala-Lo the recapture of tagged fish further than 10e15 km from the escape point, whereas, Toledo-Guedes et al. (2014a) described escapees being landed 50 km off the escape. Since gilthead sea bream is a demersal species, the narrower continental shelf present in Canary Islands could have made individuals disperse further distances along the shore. In the present case, the lack of abnormal captures of gilthead seabream landed in the nearest fish markets indicates that dispersion of escapees did not span more than 30 km off the escape point. The incidence of escaped fish was noticeable throughout the next seven months after the escape. Similarly, Toledo-Guedes et al. (2014a) detected the incidence of escaped sea bass in fisheries landings over a period of more than 12 months after a massive escape in Canary Islands. Along the recapture period, the pattern of escapees landings described by Toledo-Guedes et al. (2014a) showed constant, while in our case a dramatic biomass was landed in the first weeks after the escape. The latter could be due to the high success of fish traps, which might have recaptured the main bulk of the escaped fish faster than if only nets would have been used. The recapture efficiency of the fishing fleet resulted in 64.7%, the largest reported for a large-scale escape event so far. Other studies stress the low recapture success once the fish have escaped (SerraLinares et al., 2013; Noble et al., 2013) and only Chittenden et al. (2011) reported high recapture rates using coastal fish bags during the first month after the simulated escape. However, less than 40 acoustically tagged individuals were released in this study. In
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this study, nets responded faster to the recapture of escapees than fish traps since the latter are anchored to the shoreline whereas nets can be deployed in higher depths closer to fish farms. Interestingly, the presence of escapees swimming alive inside the fish traps may exert an attraction effect over their counterparts, driving to a higher recapture success and it should be further studied. Moreover, fish traps might bring advantages to farmers compared to other fishing gears e.g. live fish can be harvested from fish traps to minimize the economic loss by reallocating the fish in the sea cages. 4.2. Guidelines for the design of a contingency plan for fish escapes In the main fish-producing countries as Norway, Canada, United States, Australia, Scotland or more recently Chile, sea cage aquaculture together with potential escape events are specifically regulated under a legal framework (all links in Izquierdo-Gomez et al., 2014), either preventing or mitigating the negative effects of escapees. All actions taking place from the declaration of the escape until its control, are included in a contingency plan for fish escapes, which is compulsory to obtain a new aquaculture licence. Therefore, similar contingency plans should be developed within an adaptive management framework in all Mediterranean fin-fish producers. In case a fish escape occurs, a rapid response informing the authorities about an escape event is needed to initiate as quickly as possible the recapture actions to minimize the dispersion of the escapees (fishing actions defined further in the text). Since the studied escape event occurred on Friday evening (31st Oct 2003), the escapees dispersed over the weekend before fishermen set their fish traps and nets (professional fishermen cannot fish during weekend days). Thus, the escape detection system should be active during non-working days or bank holidays, as well as wellcoordinated with authorities for a quick response. In order to trigger the escape alarm, it must be defined what an escape event is and it should be quantifiable in terms of fish number and/or escaped biomass. In case the farmer does not inform the authorities, an independent escape alarm system triggered when abnormal catches of a given cultured species occur is suggested (field surveys and/or monitoring further described in the text). Eventually, if the authorities are not informed by farmers, legal actions (to be developed) should be carried out against fish farming enterprises. Once the escaped event is declared and no longer than a week after, the farmer should issue a first report to the authority describing the causes of the escape, species and quantity of escaped fish/biomass. All damages occurring at the fish farm facility must be repaired as quickly as possible and a photographic document of the damaged structures must be included in the first report. The medical condition of the fish must be included in the report as well, since medicated fish may contain active substances and thus, public health issues may arise from the uncontrolled consumption of escaped fish (Sapkota et al., 2008). Based on the aforementioned behaviour of escaped fish, which seek refuge in shallow areas near the shoreline, farmers must come to an agreement with the authorities to pre-set the recapture actions to be carried out before an escape event occurs. The fishing gear, distance to the fish farm and the areas to distribute the fishing effort, as well as the economic terms, should be mandatorily agreed to mitigate the effects of potential escape events as cost-effectively as possible. Due to the strong ability to recapture escaped fish shown by artisanal fishermen, this professional guild should be taken into account for the planning of the recapture actions. The first days after the escape event are critical, thus the fishing actions must be carried out around the farm and thereafter along the
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nearest shallow areas from the escape point throughout a month. The authority should hold the right to extend the duration of the fishing activities according its success and the abnormal presence of escapees in the area. As a consequence of the high recapture success of fish traps, its usage is strongly advised if not the construction of a customized version optimized for specific areas next to the fish farms. However, the usage of fish traps is only allowed along certain periods of the year and in certain parts of the Mediterranean Sea. Therefore, special permits should be issued to set fish traps when a massive escape takes place. In the same way, the usage of nets have constraints regarding the distance to the shore (200 m) and given the behaviour of escaped fish seeking refuge in shallow waters and closed inlets, a special permit should be issued to allow the usage of nets in swimming zones (e.g. beaches, creeks). Beach-seines were prohibited a few decades ago but its usage should be considered as they are adapted to fish in the preferred areas for escapees. During the recapture actions, by-catch composed by non-targeted species could be released since fish traps and beach-seines might not kill the fish. During the recapture actions, parameters as the captured species, fish sizes and the recapture success should be always surveyed by the authorities not to jeopardize the stock of other species or the wild conspecific population. The usage of identification tools resulting from PREVENT ESCAPE project (http://preventescape.eu) are advised to discern between wild and escaped fish, especially the presence of ontogenic scales (Arechavala-Lopez et al., 2013b). The authorities should inform the users of the coastal zone (e.g. swimmers, tourism or recreational fishermen) to prevent social conflicts arising from the unusual presence of professional fishing carrying out legal recapture activities in shallow areas. In case the authorities are not present, passive fishing gears should be clearly labelled indicating its legal status, purpose and contact information of the authorities. In addition, it must be noticeable to prevent accidents derived from entanglement of coastal users. Surveys to monitor the presence of escapees should be carried out through the whole year. Areas of ecological importance, if existing, should be included in the survey (i.e. Natura2000 zones and marine protected areas). In case of escapees of locally absent species as meagre (A. regius), the visual identification would be simple, whereas in case of gilthead sea bream or European sea bass, either individuals of similar sizes to those which escaped or abnormal schools of fish would trigger the alarm. In case that high abundances of escapees are still detected once the recapture actions are completed, the contingency plan must be activated again. If the abundances are low or escapees invade protected areas, eradication measures as underwater fishing should be activated due to its high specificity. Once the presence of escapees is no longer detected, authorities will continue with the normal monitoring program of escapees. In parallel, the fish farm should be inspected by the authority to validate the actions conducted to repair the reported damages after the escape. Long term monitoring data of the escapees or the incidence of escape events, could be used to validate further strategies to prevent fish escapes as it occurred with the new standard of materials implemented in Norway in 2004 (NS9415; LOV-2005-06-17-79-x12); It was concluded that, the introduction of a new standard of materials led to a dramatic reduction in the number of major escape incidents in Norway (Jensen et al., 2010). An effective management of sea cage aquaculture will only be possible if the escape events are declared to authorities. Once the fishing actions to recapture escaped fish conclude, the farmer must report in detail to the authority with the causes of the escape, structural damages and economic losses, together with the description of the recapture actions (e.g. fishing gear, spatiotemporal distribution of the fishing effort, main affected areas,
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recapture success, hot-spots of recapture, medical condition of the fish, etc …). The latter will be issued in a standardized report sheet (to be created when designing the regulation of escape events). In case the presence of escapees is still high when the fishing permit issued for recapture purposes expires, the farmer should request the authorities to extend the permit to carry on with the recapture actions. Eventually, the information contained in the final report provided by farmers and the data obtained from the monitoring program of escapees will be used to improve the former contingency plan to better address the fishing effort of the recapture actions towards the areas where escapees prefer to disperse. In last term, the escape event and its features (e.g. magnitude, species, fish sizes, medical condition, causes and date) should be registered in a data base for a detailed control of the escape events which will be available for future research. Summarizing, this is the first time that the recapture process after a large-scale escape event of gilthead sea bream has been analysed in detail through fisheries landings. The obtained results showed valuable to design mitigation measures to be implemented in future aquaculture regulations of coastal Mediterranean countries, which are inexistent so far. It is suggested that either the procedure to inform authorities or the recapture actions to be carried out after a fish escape event, are mandatorily issued together with the environmental impact assessment for its approval, in order to obtain the licence for fish farming activities. Despite the existing regulations for escape events of Atlantic salmon (S. salar) provide valuable information, further specific studies focussing on the recapture of species reared in the Mediterranean Sea (i.e. gilthead sea bream, European sea bass and meagre) are critical. Only through data-based management measures, the sustainable development of the aquaculture industry along the Mediterranean coast will be achieved. Acknowledgements Special thanks to the administration staff of the landing port of Aguilas for providing us with the landings data sets. This research was part of ESCAFEP project, cofounded by the European Fisheries Fund (EFF) and the Biodiversity Foundation, in collaboration with the Spanish Ministry of Agriculture, Food and Environment. References Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. Permanovaþ for PRIMER. Primer-E, Plymouth, UK. Arechavala Lopez, P., Uglem, I., Fernandez-Jover, D., Bayle-Sempere, J.T., SanchezJerez, P., 2011. Immediate post-escape behaviour of farmed seabass (Dicentrarchus labrax L.) in the Mediterranean Sea. J. Appl. Ichthyol. 27, 1375e1378. http://dx.doi.org/10.1111/j.1439-0426.2011.01786.x. Arechavala-Lopez, P., Uglem, I., Fernandez-Jover, D., Bayle-Sempere, J.T., SanchezJerez, P., 2012. Post-escape dispersion of farmed seabream (Sparus aurata L.) and recaptures by local fisheries in the western Mediterranean Sea. Fish. Res. 121, 126e135. http://dx.doi.org/10.1016/j.fishres.2012.02.003. Arechavala-Lopez, P., Izquierdo-Gomez, D., Sanchez-Jerez, P., 2013a. First report of a swordfish (Xiphias gladius Linnaeus, 1758) beneath open-sea farming cages in the western Mediterranean Sea. Mediterr. Mar. Sci. 15, 72e73. http://dx.doi.org/ 10.12681/mms.503. Arechavala Lopez, P., Fernandez-Jover, D., Black, K.D., Ladoukakis, E., BayleSempere, J.T., Sanchez-Jerez, P., Dempster, T., 2013b. Differentiating the wild or farmed origin of Mediterranean fish: a review of tools for sea bream and sea bass. Rev. Aquac. 5, 137e157. http://dx.doi.org/10.1111/fme.12129. pez, P., Izquierdo Go mez, D., Uglem, I., Sa nchez Jerez, P., 2014a. AgArechavala Lo gregations of bluefish Pomatomus saltatrix (L.) at Mediterranean coastal fish farms: seasonal presence, daily patterns and influence of farming activity. Environ. Biol. Fishes. http://dx.doi.org/10.1007/s10641-014-0280-5. Arechavala Lopez, P., Izquierdo-Gomez, D., Sanchez-Jerez, P., Bayle-Sempere, J.T., 2014b. Simulating escapes of farmed sea bass from Mediterranean open seacages: low recaptures by local fishermen. J. Appl. Ichthyol. 30, 185e188. http:// dx.doi.org/10.1111/jai.12357. € Arechavala-Lopez, P., Borg, J.A., Segvi c-Bubi c, T., Tomassetti, P., Ozgül, A., SanchezJerez, P., 2015a. Aggregations of wild Atlantic Bluefin Tuna (Thunnus thynnus L.)
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