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Assessing the causes and developing measures to prevent the escape of fish from sea-cage aquaculture

Final Report Summary - PREVENT ESCAPE (Assessing the causes and developing measures to prevent the escape of fish from sea-cage aquaculture)

Executive summary:

The escape of fish from sea-cage aquaculture is perceived as a threat to natural biodiversity in Europe's marine waters. Escaped fish may cause undesirable genetic effects in native populations through interbreeding, and ecological effects through predation, competition and the transfer of diseases to wild fish. Technical and operational failures of fish farming technology cause escapes. Cages break down in storms, wear and tear of the netting causes holes, and operational accidents lead to spills of fish. The PREVENT ESCAPE project conducted and integrated biological and technological research on a pan-European scale to improve recommendations and guidelines for aquaculture technologies and operational strategies that reduce escape events.

Through research focused on sea-cages and their immediate surrounds, we determined that escapes events are widespread throughout European sea-cage aquaculture. From 2007-2009, we documented 255 escape events across 6 countries and encompassing Atlantic salmon, Atlantic cod, rainbow trout, sea bream, sea bass and meagre production. 9.2 million fish escaped from these 255 events, which mostly occurred due to structural failures during storms and the appearance of holes in nets. Sea bream accounted for the highest number of escapes (74%) followed by Atlantic salmon (11.8%). On a pan-European scale, we estimate that and that this directly cost the industry €47.5 per year. Costs to the reputation of the industry were not able to be assessed, but were likely substantial. In addition to juvenile and adult fish escaping, both sea bream and Atlantic cod mature and spawn in sea-cages. They produce viable eggs which flow out from fish farms and enter wild populations.

A detailed analysis of escapes in Europe’s largest industry, Atlantic salmon production in Norway, revealed that after the Norwegian technical standard (NS 9415) for the design, dimensioning and operation of for sea-cage farms was implemented in 2006, the total number of escaped Atlantic salmon declined from greater than 600 000 (2001 to 2006) to less than 300 000 fish yr–1 (2007 to 2011), despite the total number of salmon held in sea-cages increasing by greater than 50% during this period. Based on the success of this measure, to PREVENT ESCAPEs of juvenile and adult fish as sea-cage aquaculture industries develop, we recommend that policy-makers introduce a technical standard for sea-cage aquaculture equipment coupled with an independent mechanism to enforce the standard.

Both sea bream and Atlantic cod swim close to net walls and bite the netting, both of which may add to the risk of escape through holes. Cage management strategies may be effective in reducing cage risk, such as keeping fish well-fed, using environmental enrichment and maintaining clean nets.

Fast, accurate and cost-effective tools for identifying escapees are central for assessments of the extent and consequences of fish escapes. The project tested a range of techniques to distinguish escaped fish within wild populations. Ultimately, the selection of suitable indicators depends on the final stakeholder. Farmers and consumers could use external appearance and morphometry for rapid assessment, however, trace elements in scales and fatty acid profiles are more useful for fisheries and environmental management applications.

Project Context and Objectives:

Escapes of fishes from European sea-cage aquaculture: consequences and measures to better PREVENT ESCAPEs

The rise of modern aquaculture of fish and its environmental impacts

In 1971, famous marine explorer and ecologist Jacques Cousteau proclaimed that 'We must plant the sea and herd its animals using the sea as farmers instead of hunters. That is what civilization is all about - farming replacing hunting'. Cousteau's prediction has been borne out dramatically. Aquaculture is approaching wild fisheries as the major source of fish protein for humans (FAO 2011) through rapid domestication of marine species (Duarte et al. 2008). European aquaculture production has mirrored the global trend, rising from 1 million tons yr-1 in 1990 to greater than 2 million tons y-1 in 2008, principally though producing fish in coastal waters in large net pens (hereafter sea-cages). This enormous expansion of aquaculture has multiplied its interactions with the environment in ways Cousteau could never have predicted. Chief among these are the interactions that occur when farmed fish escape from fish farms and enter wild populations.

Sea-cage aquaculture and escaped farmed fish

Escapes of fish from sea-cage aquaculture have typically been thought of as referring to juvenile and adult fish. Such escapes have been reported for almost all species presently cultured around the world, including Atlantic salmon, Atlantic cod, rainbow trout, Arctic charr, halibut, sea bream, sea bass, meagre and kingfish (e.g. Soto et al. 2001, Naylor et al. 2005, Gillanders & Joyce 2005, Moe et al. 2007, Toledo Guedes et al. 2009). Recently, a second form of escape has come into focus, involving the escape of viable, fertilized eggs spawned by farmed individuals from sea-cage facilities, or so called 'escape through spawning' (Jorstad et al. 2008). This phenomenon has forced a redefinition of the term 'escapes from aquaculture' to include the escapement of fertilized eggs into the wider marine environment.

Escapees can have detrimental genetic and ecological effects on populations of wild conspecifics, and the present level of escapees is regarded as a problem for the future sustainability of sea-cage aquaculture (Naylor et al. 2005). For example, over 350 million Atlantic salmon are held in sea-cages in Norway at any given time (Jensen et al. 2010), which outnumbers the approximately 500000 to 1 million salmon that return to Norwegian rivers from the ocean each year to spawn. In 2010, 291 000 farmed salmon were reported to escape from Norwegian farms, whereas the pre-fishery abundance of wild spawners was estimated at 480 000 salmon (Anon. 2011). A single fish farm cage may hold hundreds of thousands of cultured fish with over a million fish per site within multiple cages now common. Due to the large numerical imbalances of caged compared to wild populations, escapement raises important concerns about ecological and genetic impacts. Evidence of environmental effects on wild populations is largely limited to Atlantic salmon, as these interactions have been intensively studied, with more limited information for the other species farmed across Europe.

Environmental consequences of escaped Atlantic salmon

In a comprehensive review of the effects of escaped Atlantic salmon on wild populations, Thorstad et al. (2008) concluded that while outcomes of escapee-wild fish interactions vary with environmental and genetic factors, they are frequently negative for wild salmon. As fish farm areas are typically located close to wild fish habitats, and escaped fish may disperse over large geographic areas (e.g. Furevik et al. 1990, Whoriskey et al. 2006, Hansen 2006, Hansen and Youngson 2010), escaped salmon may mix with their wild con-specifics and enter rivers tens to hundreds of kilometres from the escape site during the spawning period. The average proportion of escaped salmon in Norwegian rivers monitored close to the spawning period varied between 11 and 35% during 1989-2010 (13% in 2010), with the highest proportions during the late 1980s and early 1990s (Anon. 2011). Consequently, the potential exists for escapees to interact negatively with wild populations, through competition, transfer of diseases and pathogens, and interbreeding. Hindar and Diserud (2007) recommended that intrusion rates of escaped farmed salmon in rivers during spawning should not exceed 5% to avoid substantial and definite genetic changes of wild populations.

Transfer of diseases and pathogens

Escape incidents may heighten the potential for the transfer of diseases and parasites, which are considered to be amplified in aquaculture settings (e.g. Heuch and Mo 2001, Bjørn and Finstad 2002, Skilbrei and Wennevik 2006, Krkosek et al. 2007). Escapees from salmon aquaculture in Norway have been identified as reservoirs of sea lice Lepeophtheirus salmonis in coastal waters (Heuch and Mo 2001). Newly-migrated post-smolts are particularly vulnerable for sea lice infestations, and salmon lice may represent a significant threat for some wild Atlantic salmon populations (Revie et al. 2009, Finstad et al. 2011, Gargan et al. 2012). In addition, 60000 salmon infected with infectious salmon anaemia (ISA) and 115 000 salmon infected with pancreas disease (PD) escaped from farms in southern Norway in 2007, yet whether these precipitated infections in wild populations is unknown. The ability for escaped fish to transfer disease to wild fish depends on the extent of mixing between the two groups, which in turns varies with the life stage, timing and location of the escape (summarized by Thorstad et al. 2008). However, while escaped and wild fish mix, little direct evidence for disease transfer from escapees to wild salmon population has been documented, other than for the possible case of furunculosus, a fungal disease accidently introduced to Norway from Scotland in the 1990s with the transfer of stock and then believed to have been spread from farmed to wild populations by escapees (summarized in Naylor et al. 2005).


Successful spawning of escaped farmed salmon in rivers both within and outside their native range has been widely documented (see review by Weir and Grant 2006). The ability of escaped salmon to interbreed with wild salmon depends on their ability to ascend rivers, access spawning grounds and spawn successfully with wild partners. While the spawning success of farmed female salmon may be just 20-40% that of wild salmon and even lower for males (1-24%; Fleming et al. 1996, 2000), high proportions of escaped fish in many rivers can lead to a high proportion of farm×wild hybrids. Escaped female salmon may also interfere with wild salmon breeding through destroying the spawning redds of wild fish if they spawn later (Lura and Saegrov 1991, 1993).

Wild Atlantic salmon are structured into populations and meta-populations with little gene flow between them, and evidence for local adaptation in wild Atlantic salmon is compelling (reviewed by Garcia de Leaniz et al. 2007). Farmed salmon differ genetically from wild populations due to founder effects, domestication selection, selection for economic traits and genetic drift (reviewed by Ferguson et al. 2007). Hybridisation of farmed with wild salmon and later backcrossing of hybrids may change the level of genetic variability and the frequency and type of alleles present. Hence, hybridisation of farmed with wild salmon has the potential to genetically alter native populations, reduce local adaptation and negatively affect population viability and character (Ferguson et al. 2007). Several studies have shown that escaped farmed salmon breeding in the wild have changed the genetic composition of wild populations (e.g. Clifford et al. 1998, Skaala et al. 2006).

Competition for food

Escaped salmon consume much the same diet as wild salmon in oceanic waters (Jacobsen and Hansen 2001, Hislop and Webb 1992) and could potentially compete for food with wild stocks. Substantial competitive interactions in the ocean, however, appear unlikely to occur as ocean mortality of salmon appears to be density-independent (Jonsson and Jonsson 2004), although limited information exists to assess if this is also the case for coastal waters (Jonsson and Jonsson 2006).

Environmental consequences of escaped Atlantic cod

At present, little direct evidence exists for negative interactions of escaped and wild Atlantic cod juveniles or adults, despite predictions that negative consequences will result (Bekkevold et al. 2006). Cod farming is a relatively new industry, thus if negative consequences exist they may not have had sufficient time to manifest and/or be detected. Telemetry studies of simulated cod escapes have indicated that escapees, regardless of whether they originated from stocks of coastal or oceanic origin, mix with wild populations in fjord environments and can move to spawning grounds in the spawning season (Uglem et al. 2008, 2010). Behavioral studies have further indicated that escaped farmed cod are likely to hybridise with wild cod (Meager et al. 2009). However, farmed cod may have limited reproductive success in sperm competition with wild cod, which lowers the risk of genetic introgression from escapees (Skjæraasen et al. 2009).

Possible impacts of 'escape through spawning' of Atlantic cod

In the culture of Atlantic cod, some fish mature during the first year of culture, while a majority of farmed cod are believed to mature during the second year. This means that almost the entire culture stock in any particular farm has the potential to spawn in sea-cages before they are slaughtered. Spawning of Atlantic cod within a small experimental sea-cage containing 1000 farmed cod and dispersal of their spawned eggs in a fjord system has been demonstrated (Jorstad et al. 2008). In the proximity of this experimental sea-cage, 20-25% of the cod larvae in plankton samples were determined by genetic analyses to have originated from the 1000 farmed cod (Jorstad et al. 2008). Furthermore, preliminary results indicate that 4-6 % of juvenile cod (35-40 cm total length) caught in the area around the farm in following years were offspring of the farmed cod (van der Meeren and Jorstad 2009). This illustrates that if spawning occurs within commercial cod farms where numbers of farmed individuals are far greater, the contribution of 'escaped' larvae to cod recruitment within fjord systems may be substantial.

Environmental consequences of escaped sea bream and sea bass

For sea bream and sea bass, knowledge regarding how escapes might affect ecosystems is limited. Intentional releases of cultured sea bream for stock enhancement have been reported from the southern Atlantic coast of Spain, and in the Bay of Cadiz (Sanchez-Lamadrid 2002, 2004). Released fish moved less than 10 km from the release point. Good growth rates and condition indices indicate that the released fish adapted to life in the wild and suggest that populations of wild fish could also be altered by released fish. For example, there is correlative evidence of a substantial increase in wild populations of sea bream after fish farming began in the Messolonghi lagoon, Greece (Dimitriou et al. 2007). Dempster et al. (2002) found very few sea bream near sea-cages in which sea bream were being reared, which suggests either low levels of escape or that escapees move rapidly away from the farms to other habitats. Based on the ecology of sea bream and the location of most fish farms in areas close to wild sea bream habitats, it is probable that escapees would mix with their wild con-specifics. Consequently, the potential exists for escapees to interact negatively with wild populations, through interbreeding, competition and transfer of diseases and pathogens.

Possible impacts of 'escape through spawning' of sea bream

In the Mediterranean region, information about spawning by fish kept in sea-cages is sparse. In Greece, the largest EU producer of sea bream, both the number of fish farms and their production capacity increased over the past decade, accompanied by a substantial decrease in the price of sea bream. This industrial development led to structural and functional changes in the rearing process. The time individual fish were farmed increased from just 12 to 18 months before 1995 (Petridis and Rogdakis 1996) to durations of up to 40 months after 1999 (Dimitriou et al. 2007). Gilthead sea bream is a protandrous hermaphrodite species and the increased farming duration has resulted in the production of fish of a size compatible with that necessary for fish to reach the stage of sex inversion and female sexual maturation, normally observed at the age of 2-3 years in the wild. The changes in rearing processes have resulted in the presence of large gilthead sea bream individuals (larger than 500g) in cages during the normal reproductive period of their wild counterparts (November-March: Bauchot and Hureau 1986). There is evidence that sex inversion and the production of both male and female gametes occur within cages under the present industrial rearing pattern (Dimitriou et al. 2007). A doubling of the population of wild sea bream within the Messolonghi lagoon in Greece, based on standardised commercial fishing trap catch returns, correlates with the advent of farming sea-bream to large sizes in the region. Spawning within sea-cages is suspected to have led to greater recruitment to wild sea bream stocks (Dimitriou et al. 2007). Ecological and economic consequences of this population shift have ensued as while more wild sea-bream are now available to the fishery, they are of much smaller mean size resulting in an overall lower economic return to local fishers.

The need to better prevent the escape of fish from sea-cage fish farms

Improved physical containment at marine fish farming sites, through research and development of fish-farming technology, is a central recommendation of many international workshops and forums on the environmental impacts of escapees (Hansen & Windsor 2006). For example, the FP-6 EU Coordinating Action on the 'Genetic Impact of Aquaculture Activities on Native Populations; GENIMPACT' has concluded that efforts should be made to PREVENT ESCAPEs, as 'instead of trying to protect wild populations from escapees, the best logical solution would be to try to PREVENT ESCAPEs. This will rely on technical improvements from the industry …' (Triantafyllidis et al. 2007). A global report from the Salmon Aquaculture Dialogue on the incidence and impacts of escaped farmed Atlantic salmon in nature (Thorstad et al. 2008) concluded similarly: 'The most important management issue at present is the need to reduce the numbers of escaped farmed salmon in nature. ' Further, it is a stated goal of both the Norwegian authorities and the Norwegian Fish Farmers Association to reduce escapes of fish to a level where they do not threaten wild populations (Norwegian Fisheries Directorate 2009).

Prevention and Mitigation

The PREVENT ESCAPE project was specifically aimed at assessing the extent and causes of escapes and generating new knowledge through research to help mitigate the effects of escapees on wild populations on a pan-European scale. Solving technical and operational problems related to escapes is dependent on a combination of research into several technological disciplines and biological knowledge related to the behavior of fish in sea-cages.

Through five research work packages (WPs) focused on sea-cages and their immediate surroundings, we assessed the detailed technical and operational causes of escape incidents, assess the extent of escapes of reproductive gametes, juveniles and large fish from sea-cages, determined the inherent biological mechanisms that pre-dispose certain species of fish towards behaviors within sea-cages that make escapes more likely, and documented the dispersal of escapees to better understand how they may be recaptured. Finally, through research on aquaculture structures, materials, designs and operational methods, we have developed new knowledge to PREVENT ESCAPEs and use technologies to recapture fish after they have escaped. Both of these results will assist efforts to mitigate the effects of escapes.

Project Results:

WP Map Escape

The overall goal of the MAP Escape WP was to assess how and why escapes occur and to determine the full economic cost of escape events to farmers. There were four specific objectives set out:

-To document the extent, size and knowledge of the causes of escapes
-Make detailed assessments of the technical/operational causes of escapes
-Establish the cost of escape events
-Compile a final report for publication and dissemination

A specific methodology was developed and applied across all of the countries involved in the MAP Escape WP in order to ensure comparability of results. The methodology was made up of the following components and actions:

- Consultations with industry and relevant agencies through a confidential questionnaire and follow up interviews to gather information on methodologies and technologies currently used in on growing finfish in the marine environment.

- Gathering of available existing information on the extent, size and knowledge of the causes of escapes from national reports and other published data.

- Conducting detailed assessments of the explicit technical or operational causes of escapes at sea-cage fish farms throughout Europe by direct assessment of known escape events at industrial fish farms. By way of site visits and interviews.

- The total economic cost of escape events was estimated through a cost evaluation using both available data and through direct gathering of data by way of interview.

The methodology and technology presently used in on-growing at sea, the incidence of escapes and their underlying reasons were documented. There were a total of 255 escape incidents identified through questionnaires which were completed across 6 countries (Ireland, UK, Norway, Spain, Greece, and Malta), and other data supplied by the Norwegian Fisheries Directorate and the Scottish Aquaculture Research Forum. Some of the events were as a result of a combination of causes. The majority of escape incidents related to net damage due to predator attacks and abrasion. Storm damage or weather was also a common cause. However, it was not clear from the responses obtained whether the storm losses were due to net, mooring or floater damage.

WP Pre-Escape

To prevent and successfully mitigate against fish escapes from open cage aquaculture production systems, one must have a broad overview of the potential interactions that fish can have with the netting materials. Numerous species of farmed fish can exhibit escape related behavior and damage the cage wall by biting the net. These include three key European farmed fish species: Atlantic cod, European seabass and gilthead seabream. The PREVENT ESCAPE project has identified key risk factors that increase escape related behavior in each of these species and has also drawn up a series of mitigation strategies to minimise the expression of these behaviours in aquaculture.

There are several behavioral repertoires that fish can exhibit when interacting with the cage wall and these include i) general net inspection behavior, ii) overt net biting that weaken the net and potentially lead to hole formation, and iii) the exploratory or risk taking behavior exhibited when fish pass though holes in the net.

With regard to Atlantic cod, several of the involved behavioral mechanisms differ between genetic strains, and some individual fish are repeatedly more prone to escape through small holes in the net wall, probably due to differences in so-called boldness or willingness to explore new environments. Factors that promoted escape related behaviors included both physical net traits and the motivation to feed. For example, most of the inspecting and biting behavior on the net were focused on loose threads, e.g. after a net repair, and especially if the repair was done with a contrasting colour thread. Other factors that can increase escape related behaviors include prolonged periods of starvation (ca. 1 week) and also short periods of feed restriction. However, escape behaviors can be reduced by environment enrichment within the cages and also by keeping the net clean.

With regard to gilthead seabream and European seabass, PREVENT ESCAPE identified a number of factors that can contribute to fish escaping from sea cage facilities. Small-scale experiments were performed in experimental tanks (closed recirculation system tanks) and also in experimental sea cages under completely controlled conditions at the University of Crete. These studies investigated behavioral interactions with the net in relation to:
i) stocking density,
ii) feed availability,
iii) biofouling and
iv) light conditions.

Results suggest elevated stocking densities, biofouling and restricted feeding conditions increased escape related behaviors and net biting in gilthead seabream. Increased stocking densities and higher light intensities increased escape related behavior in European seabass.

WP Post-Escape

Fast, accurate and cost-effective tools for identifying escapees are central for assessments of the extent and consequences of fish escapes. Moreover, knowledge of short- and long- term post-escape dispersal of fish is directly applicable for assessing the prospects for recapturing escapees and it is fundamental for predicting possible negative environmental effects. In addition, knowledge of the movement patterns of fish after escape may provide information that will assist in the selection of farms sites that might minimize negative effects of escapees. The POST Escape WP aims to fill essential knowledge gaps for identification of escapees and to provide fundamental data for assessment escapes and mitigation of escapes of sea bass, sea bream and meagre.

Growth pattern in scales (scale-circuli patterns), using computed-based image analysis was useful for distinguish cod, seabass and seabream. Farmed cod appear to grow faster than wild fish, as indicated by an increasingly larger cumulative circuli breadth and relatively larger scale radius for farmed compared to wild cod. Seabream showed regenerated nuclei and malformed scales in farmed fish. In seabass, number of annuli was clearly observed in wild fish scales but it was not possible to measure them in farmed individuals due to the absolute lack of such annual deposition in farmed fish scales, which is really helpful to identify large-sized farmed individuals. For seabass, the otoliths area, perimeter and shape descriptors showed clear differences between wild and farmed values, mostly for higher fish sizes. Seabream otoliths were quite similar, but statistically significant differences were found also through shape descriptors between wild and farmed individuals. Changes in body morphology, described by relatively easily measured parameters and compared using a multivariate approach, was also useful for distinguish between wild and farmed cod, seabream, and seabass with a percentage of discrimination higher than 90 %. Fulton's Condition Index (K) revealed significant differences between wild and farmed individuals of seabass and seabream, with the farmed fish exhibiting the highest values. Additionally, farmed seabream fins resulted more eroded and splitted than wild seabream fins, due to seabream swimming behaviour and farming conditions within open-sea cages, but fins may recover from farming abrasion along the time once they are in the wild.

For trace element analysis using an ICP-MS, 10 to 20 scales from the left hand side of the fish (cod, seabass, seabream and meagre), 2-3 rows above the lateral line, were removed using one disposable plastic knife per fish and kept them on paper bags. Otoliths trace element signature were also analysed for seabass and seabream. Scale chemistry proved very good at discriminating between farmed and wild (and escaped in the case of meagre in the canaries) populations of cod and meagre but typically discriminated between sea bass and sea bream wild (and escaped populations in the canaries) and farmed populations less well - with some exceptions. The performance of the method for both sea bass and sea bream was least good in Greece where there was overlap between wild and farmed populations in a multivariate analysis.

Regarding otolith trace element signatures, differences between farmed and wild fish were also found but no so strong as scales. Seabream otolith microchemistry revealed significant differences between farmed and wild fish using multivariate analysis, and also when performing univariate analysis on Sr:Ca, Mn:Ca, Ba:Ca and Fe:Ca ratios. Nevertheless multivariate analysis of seabass otoliths did not show differences between groups and the only significant differences between groups analyzing seabass otoliths appeared in Mn:Ca and Ba:Ca ratios.

Fatty acid composition was analysed from different tissues as a potential for being used as a physiological indicator. For cod, seabass, seabream and meagre, multivariate analysis revealed that a high % of the fish could be correctly classified with respect to origin. In addition, other significant differences were found for univariant analysis, such as decreased levels of the ratio n3/n6 and DHA in farmed adult sea bass muscle; increased levels of n9 FAs in farmed juvenile sea bass; decreased levels of n3/n6 in farmed adult sea bream muscle; increased levels of DHA in juvenile sea bream and increased levels of EPA in farmed adult sea bass liver. Therefore, special attention should be taken into account to the low levels of arachidonic and high of linoleic acids which may be characteristic of cultured sea bass and sea bream. For meagre, it was revealed significant differences between farmed and escaped meagre muscle and liver FA profile. Deviations in the FA data coming from escaped fish are caused by recent escaped fish, which presented similar profile that cultivated fish, however results do not change if we do not take into account near farm samples.

The genetic structure of farmed and wild populations of seabream and seabass from Spain and Greece were analysed using 16 polymorphic microsatellite loci for each species. There was significant departure from Hardy-Weinberg equilibrium for all populations for both species. Gene diversity was significantly lower for farmed populations. Farmed populations also had lower number of privet alleles. These observations could be the result of a bottleneck that the farmed populations have experienced. Inbreeding coefficient was significantly higher than zero for all populations apart from the Greek farmed populations for both species. FST values indicated that all populations for both species were genetically differentiated from each other. Greek farmed populations for both seabream and seabass were most differentiated from the rest of the populations. Bayesian clustering confirmed that each farmed population was distinct from its proximal wild population. This distinction was more pronounced for Greek samples. Using this analysis, each individual can be allocated to a specific population with a certain probability. This probability is as higher as the difference between populations is increased. Using this analysis an individual captured in the wild can be identified as 'wild' or 'farmed' (i.e. escapee). The analysis showed that group allocation using the genetic profile could very accurate for Greek populations of both species. For Spanish sample the method is reliable but not as accurate as for Greek samples.

Cost-benefit analysis indicates that the scale features, followed by morphometry were the most efficient variables taken into account accuracy and cost. Regarding to temporal usefulness of indicator, genetic and scale feature can be use for long term monitoring, but other indicator as external appearance, fin erosion and fatty acid can change over time. The selection of indicator will depend on the final stakeholder. Farmers and consumer should understand in a better way external appearance and morphometry, but for fisheries and environmental management features and trace element of scale, as well as fatty acid profile should be more useful. In the case of the need of identify a single individual, genetic methods and features and trace element of scales could be recommended, but if it is required to identify the original farm genetic method could be the technique to be use.

Regarding to the short dispersal pattern of escapes, estimated by internal acoustic tagging, cod results indicate that 70 % of the fish left the immediate farm area during the first 3 days post-escape, and after one week only 20 % of the escapees remained in the area. For long dispersal pattern, recaptures of adult tagged cod varied between localities with higher recapture rate for fished released from the farm located in the inner part of the fjord. For the adult fish tagged and released at the farm located close to the coast only one fish were recaptured close to the release farm three months after release. The adult fish from the release at the farm located in the inner part of a fjord were recaptures throughout the entire fjord, up to 70 km away from the farm. The difference in recapture rates for adult fish between these two locations may be a result of that the fish released closest to the coast rapidly dispersed to areas with a lower intensity of both commercial and recreational fishery. In general, the recapture rates of both adult and juvenile cod in local fisheries and organized recapture efforts were low. However, the high predation rates for the smallest release group that was documented for a relatively low number of predators only indicate that the number of escapees below 25 cm of total length that were able to evade from the farm area was negligible at the present location and period. For salmon, the results indicate that the short-term potential for interaction between wild and escaped salmon juveniles was low under the actual conditions with an early and cold autumn, since the escapees not moved up into fresh water. In addition, the relatively high immediate mortality of nearly smoltified parr indicate that the mortality of younger parr could be high following escape from smolt farms, as long as they are inhibited from migrating into fresh water in the immediate vicinity of the farm.

Farmed seabream, after escape, are able to survive for long periods (a least up to 2 months) once they are in the wild, swimming to nearby facilities, coastal areas or far away from farming areas. For instance, tagged seabream showed both a high dispersion within the first 5 days after release and a high mortality rate (greater than 60%) where the fish appeared to be predated at the release farm. However, some individuals remained not only at the release farm but also at the nearby farm facilities for long periods, surviving up to 4 weeks at farms with a clear diurnal swimming depth behavior related to farm activity. Local fisheries contributed recapturing tagged individuals that disperse from farm facilities, being professional trammel-netters the major contributors. Results for escaped seabass showed that a proportion of escapees may move relatively quickly and repeatedly among several ?sh farms, however, a number of them dispersed away from farming areas. However, escaped seabass showed less farm-affinity than escaped seabream. Therefore, a high dispersion from farm areas was detected for seabass, but also that mortality is likely to be high, and some of them swam to coastal areas where they are able to survive at least up to 3 months. The results thus might indicate that long-term ecological impacts of such seabream can be more important on wild congeners compared with seabass, since seabream use natural habitats. However, both of them presented high mortalities, but also they are able to survive for long periods feeding on natural preys. Furthermore, local fisheries could help to mitigate the potential negative effects of escapees through their recaptures.

In the case of the experimental release of adult meagre, those fishes don't aggregate on the cages, all went to the sea bottom and remained there until the 4th day. Those fishes showed a similar behavior than the ones used in the large scale simulated release, staying in small crevices and ledges during first days and then they disappears from the areas.

WP Egg Escape

During the last decade, culture of species that may reproduce within sea-cages has become more common. Examples of such species within European aquaculture are the Atlantic cod and the gilthead sea bream. The potential for negative ecological effects to occur as a result of spawning in sea cages may be significant.

The main objective of WP5: 'EGG Escape' was to assess the extent and ecological importance of escape through spawning in sea-cages and suggest possible mitigation actions. The work consisted of both an extensive field program and a modeling component. In the field program, farmed fish were randomly collected at selected cod (Gadus morhua), sea bream (Sparus aurata) and meagre (Argyrosomus regius) farms in Norway, Greece and Spain, respectively. The three species were selected to include:
(a) a major industrial species (sea bream) with increasing potential to spawn within cages;
(b) a species (cod) initially predicted to make a transition from an emerging to a major industrial species within a few years, which is known to spawn within cages; and
(c) a new emerging species (meagre) that was suspected to spawn within cages.

The specific objectives of WP5 were:
(1) to evaluate extent, frequency and timing of spawning within sea-cage fish farms at an industry-wide scale;
(2) to assess the quantity and quality of released eggs;
(3) to assess the survival and distribution of escaped eggs, and
(4) to evaluate the need for implementation of mitigative strategies for reducing or preventing escape of eggs

In the gilthead sea bream, the findings of WP5 demonstrate that fish cultivated in sea cages, at sizes beyond sex reversal, can reach maturation and ovulation and release eggs during the normal spawning period of the species. However, egg production is very low, decreases considerably with sex ratio (i.e. with higher mean fish size in the cage) and varies considerably from day to day. The survival of fertilized eggs is likely to be very low. The probability of producing more eggs or that larvae might recruit to the wild populations is increased when the sex ratio in the cages is balanced (close to 1:1) and when the farms are located in areas where the gilthead sea bream is able to close its life cycle, e.g. in the vicinity of lagoons.

The investigations on meagre, in both the Canary islands and the Mediterranean Sea revealed that this species does not reach sexual maturity prior to current commercial sizes in Spain. Furthermore, no spontaneous spawning has been recorded for meagre brood stocks held in the Canary Islands, whatever the size of the fish.

The major findings for cod are that farming has the potential of producing large amounts of eggs and larvae through spawning in cages. The amount of eggs spawned during the second year is 4 to 5 times higher than during the first year in sea cages. The quality of the escaped eggs is likely to be sufficiently good for larvae to develop until first feeding. Furthermore, eggs and larvae from farms may, at least during parts of the spawning season, experience conditions comparable to wild larvae. Finally, the survival of escaped cod eggs up to the adult stage is likely to vary considerably and is difficult to predict.


Much of the state-of-the-art of knowledge for ensuring that fish farms do not fail structurally and that operations do not cause escapes is contained in technical standards. Such standards are well developed in some European countries, but non-existent in others. Even though Norway has a comprehensive technical standard, escapes still occur at a level which is regarded by many to be detrimental to wild stocks, indicating that the knowledge which forms the basis of technical standards is in constant need of improvement. Work is ongoing to develop an ISO standard that can apply to all sea-cage fish farm installations.

The main objective of WP6 PREVENT ESCAPE was to extend the knowledge on culture operations and technology to improve technical and operational guidelines to prevent fish escape and to increase the recapture success of escaped fish on the basis of integrated biological and technological research. The work consisted of full scale tests, physical and numerical modeling of farms and structures, material and component testing as well as developing recommendations and guidelines for the design an operation of marine fish farms.

The specific objectives of WP6 were:
(1) integrate biological and technological research to facilitate knowledge-based development of robust containment technology,
(2) generate fundamental knowledge on the properties of component aquaculture technologies to help improve design and production of sea-cage equipment components,
(3) develop guidelines for the design and use of sea-cage technologies and equipment to minimise the risk of escapes,
(4) test recapture technologies to improve recapture rates of escapees based on knowledge of the post escape behaviour of fish, and
(5) disseminate the results to fish farmers, aquaculture technology manufacturers and suppliers, standards organisations, government agencies and the wider scientific community.

Net cages used to farm cod, salmon, sea bass and sea bream were inspected for holes throughout a production cycle. A higher number of holes were found in nets used to farm sea bream and cod compared to nets used to farm salmon and sea bass, due to the cod and sea bream biting the net. Measurements performed during laboratory tests confirmed that even small to medium sized cod were able to pull the net with a force sufficient to tear a single nylon filament in the net. To avoid the farmed fish creating holes in the net, the strength of a single filament should be higher than the strength of the fish. Numerous tests have been performed on new virgin material as well as on net materials used to farm cod, salmon, sea bass and sea bream. Different mesh types and different materials have been tested using different procedures to determine the strength, flexibility, resistance to abrasion, weakening due to washing and other operations on the net. The net strength declines with use, but it was not possible to directly relate the remaining strength of the material to the age or number of productions cycles for the net. Some of the tests performed (high pressure cleaning, cyclic tests, creep tests) had a minor if any effect on the strength of the material whereas others (e.g. washing in tumble washers and abrasion) had larger impact on the net strength.

Potential Impact:

Dissemination activities conducted in PREVENT ESCAPE have included dissemination to:
1) the general public through the project’s web page;
2) directly to the fish farming industry and governmental regulatory authorities through a series of targeted workshops held during the project period and participation in other industry-related workshops on the topic of escapes;
3) to the aquaculture technology supply industry through direct contact between researchers and industry participants; and
4) the broader scientific community through presentations at conferences and a dedicated session to escapes at the European Aquaculture Conference in 2011.

1)Dissemination to the general public through the project's web page and the PREVENT ESCAPE Compendium of final results

The PREVENT ESCAPE website has existed from the very beginning of the project on April 1, 2009. In June 2010, the website content and presentation was overhauled and the website was re-launched in June 2010 at a new web address: The new website has been built by (a specialist firm for web design with a marine theme) with material provided by the coordinator and the WP leaders. The website was updated in August 2010, again in September 30, 2010 and finally in 2012 with the publication of the PREVENT ESCAPE results Compendium. The Compendium has 30 chapters (as outlined below) spanning the topics covered by PREVENT ESCAPE which are each downloadable as individual pdf files. The Compendium chapters are written for a broad, non-technical audience.


Executive Summary


1 Escapes of fishes from European sea-cage aquaculture: causes, consequences and the need to better PREVENT ESCAPEs

2 A pan-European evaluation of the extent, causes and cost of escape events from sea-cage fish farming

3.1 Does the farming environment and the inherent behaviors of fish predispose some species to higher rates of escape?

3.2 Factors affecting escape-related behaviors in Atlantic cod (Gadus morhua)

3.3 Escape behavior - sea bass

3.4 Escape behavior - sea bream

3.5 General conclusions and recommendations


4.1 The importance of identifying escapes and their post-escape behaviors for environmental and fisheries management.

4.2 Methods to identify Atlantic escaped cod
4.3 Methods to identify escaped sea bass and sea bream (responsible: Arechavala).

4.4 Methods to identify escaped meagre

4.5 Post-escape behaviors of cod

4.6 Post-escape behaviors of sea bream and sea bass

4.7 Post-escape behaviors of meagre

4.8 General conclusions and recommendations


5.1 General introduction to escape through spawning

5.2 Egg escape - Sea bream

5.3 Egg Escape - Cod

5.4 Egg Escape - Meagre

5.5 General Conclusions and recommendations


6.1 General Introduction on techniques and technologies to PREVENT ESCAPE

6.2 Damage to the net cage
6.3 Measurement of biting strength of cod, and filming of sea bream biting the net cage

6.4 Environmental conditions in Ireland, Norway and Spain

6.5 Net materials

6.6 Sea load exposure

6.7 Recapture of sea bass and sea bream

6.8 Recapture of Atlantic cod

6.9 Prevention of egg escapes

6.10 Recommendations/guidelines for standards and legislation to PREVENT ESCAPE

2)Dissemination to the fish farming industry and governmental regulatory authorities through a series of targeted workshops

Towards the end of the project, dedicated stakeholder workshops were held to disseminate the results of the project directly to fish farmers, aquaculture technology producers and suppliers. Well attended workshops were held in Ireland (March 2011; 50 participants) and Spain (October 2010; 40 participants). A less well attended workshop was held in Greece in October 2011 alongside the European Aquaculture Society conference. Throughout the project period, WP6 leader Dr Osten Jensen from SINTEF Fisheries and Aquaculture gave 10 separate presentations within Preventing Escape 1-day workshops organised by the Norwegian Seafood Federation (FHL) to a combined audience of over 1000 participants from the fish farming industry and Norway’s regulatory bodies.

3)Dissemination to the aquaculture technology supply industry through direct contact between researchers and industry participants

Much of the work in WPs 2 and 6 has involved direct contact with the aquaculture technology supply industry project as we have collected netting materials and ropes for properties and strength testing and discussed design principles with suppliers. As the work in these WPs has been completed, we have directly provided written feedback and data from the project’s test results. This form of direct dissemination has high and rapid impact in terms of industrial implementation of results.

4)Dissemination to the broader scientific community through presentations at conferences and a dedicated session to escapes at the European Aquaculture Conference in 2011.

As part of the European Aquaculture Society Conference held in Rhodes, Greece, in October 2011, the PREVENT ESCAPE Project organised and coordinated a 1.5 day conference session titled 'Environmental effects and methods to trace, mitigate and PREVENT ESCAPEs'. The session was chaired by Dr. Tim Dempster (PREVENT ESCAPE Scientific Coordinator, SINTEF Fisheries and Aquaculture, Norway) and Prof. Ian Fleming (PREVENT ESCAPE participant, Memorial University of Newfoundland, Canada).

The session comprised 30 talks and several posters which integrated research results from the PREVENT ESCAPE project with other research underway throughout Europe and the Americas on the environmental effects of fish that escape from aquaculture and techniques and technologies to trace and mitigate escapes. The session was roughly organised along five major themes that reflect the organisation of the PREVENT ESCAPE project:
1) Extent of escape events and developing methods to accurately trace escapees;
2) Pre-escape behaviors of fish and determining whether cage management strategies may PREVENT ESCAPEs;
3) Post-escape behaviours of fish and recapture efforts;
4) Extent and importance of 'escape through spawning'; and
5) Technological developments to PREVENT ESCAPE incidents.

Prof. Ian Fleming introduced the session with a plenary to discuss the historical perspectives behind the escapes issue. Escapes have likely always occurred, yet it is only recently, since the industry expanded rapidly during the 1970s and 1980s, that escapes of have been seen as anything other than an economic concern. Since the 1980s, concern has turned to the environmental consequences of escapes as large numbers of farmed fish began appearing in wild populations. Since that time, perspectives on the causes and consequences of escapes have changed, as have management policies. These changes reflected the industry's growth in scale and inclusion of new species, advancements in our understanding of escapes through research, and concern over declining fish stocks. Dave Jackson presented a summary of estimates of the extent and causes of escapes across European fish aquaculture made within the PREVENT ESCAPE project. Escapes are extensive and frequent across European aquaculture, with escapes more frequent for sea bream and sea bass than for salmon. Approximately 75% of fish that escaped were due to either structure failure or operational error, often coincident with storms.

Eight presentations addressed the general topic of developing methods (scale morphology and microchemistry, fatty acids, stable isotopes and genetics) to accurately trace farmed fish (salmon, cod, sea bream and sea bass) in wild populations, which allowed for a robust analysis of which techniques work best for different purposes based on their relative costs and benefits. Several presentations from Europe, South America and the Mediterranean addressed the extent to which escapees were entering wild populations for salmonids, sea bream and sea bass. Among these was a presentation from Killian Toledo which indicated that while sea bass were now present in Canary waters as an introduced species due to escapes from aquaculture, they may not yet have established breeding, self-sustaining populations and become invasive. Several papers presented results on the post-escape behavior of sea-bass and sea bream; the conclusions of these studies converged to suggest that for re-capture success, fishing efforts must be rapidly deployed on the scale of days post-escape.

Stelios Somarakis summarised the results of work within the PREVENT ESCAPE project on the extent and importance of maturation of sea bream in sea-cages and escape through spawning. This work demonstrated that a significant proportion of sea bream mature if they are cultured beyond 800 g and are able to spawn within sea-cages. However, fecundity was low relative to wild sea bream. Later in the session, Ed Trippel presented promising results which indicated that triploidy may be a viable solution to the ongoing problems of maturation in sea-cages and escape through spawning. Trippel's results show that the growth performance of Atlantic cod triploids was good relative to diploids, that triploidy suppressed maturation rates of cod, and that larvae produced by triploid fish were non-viable.

In summary, the session demonstrated that a number of options to reduce and mitigate escapes are presently available and viable; the challenge is to ensure uptake of these by the various industries across Europe and worldwide. A general consensus from the session was that the greatest single measure to rapidly reduce the number of escape events could be obtained through the implementation of technical standards and processes to ensure the independent accreditation of component technologies to meet these standards. Strong correlative evidence over the past decade in Norway with the implementation of the NS 9415 technical standard for the design, dimensioning and operation of fish farms has demonstrated a dramatic reduction in escape incidents and the number of fish that have been reported to escape. Major European aquaculture producing countries should consider development and implementation of a similar standard.

Socio-economic impact and the wider societal implications of the project

The research in PREVENT ESCAPE will lead to impacts related to: 1) biodiversity conservation and increased sustainability of aquaculture; 2) policy and regulatory mechanisms at both European and national levels; 3) increased profitability in the industrial/commercial sector; and 4) science and technology. These impacts are detailed below:

Biodiversity conservation and increased sustainability of aquaculture

The primary focus of research under Area 2.1.2 'Assessment and mitigation of the impact of aquaculture on wild populations' in theme 2 Food, Agriculture and Fisheries and Biotechnology (KBBE-2008-1-2-03), is to increase sustainability and competitiveness, while decreasing environmental impacts of aquaculture through the development of new technologies and improved approaches to husbandry. Prevention of fish escapes from aquaculture is a prerequisite to reach this goal. If farmed fish are prevented from escaping, the majority of the possible ecological effects will be avoided. Fewer escapees will implicitly reduce genetic impacts on wild stocks through interbreeding, transfer of pathogens from escapees to wild populations and levels of ecological impacts due to predation by escapees and competition with wild con-specifics.

Research undertaken in the PREVENT ESCAPE project has provided a number of key outputs that all contribute to minimizing the escape of fish and their subsequent dispersal into wild populations. These include:

- Identifying the key technical and operational causes of escapes from sea-cages and suggesting preventative measures

- Improving the robustness of sea-cage equipment by providing better knowledge for the production of components and the design of entire installations

- Developing information relevant to siting recommendations of fish farms based on the dispersal of eggs spawned by fish in sea-cages

- Making recommendations to national and international standards organisations regarding the development and improvement of standards

- Increasing awareness of the need for technical and operational standards for sea-cage fish farming throughout Europe

- Developing information for assessing the likelihood of escape for marine species under industrial sea-cage culture

Policy and regulatory impacts at both European and national levels

The European Union's Aquaculture Strategy (2002) explicitly states that efforts should be made to 'develop instruments to tackle the impact of escapees'. More specifically, the strategy states that efforts to '…develop guidelines to minimise salmon escapees is particularly worthy of support. The Commission will examine whether such guidelines should be implemented by way of compulsory rules and may extend them to other fish species and strains'. PREVENT ESCAPE has contributed to prevention of escapes through improving our knowledge in central areas of the technology and husbandry practices used to culture fish in sea-cages. This knowledge will be directly used to improve containment technologies, improve sea-cage farming operations, improve fish husbandry practices, and improve technical standards, guidelines and regulations, with the common objective of minimising the number of cultured fish that escape and enter wild populations. Preventing escapes is the obvious first line of defence in this context. Research within the project indicates that recapture efforts are a poor secondary option with likely limited chance of success.

The project has distributed the information generated on improved containment measures and methodologies to PREVENT ESCAPEs to regulatory bodies in Norway, Scotland, Ireland and throughout the Mediterranean countries. At present, Norway remains the only European country to have a compulsory standard for sea-cage fish farming technology and operations. The PREVENT ESCAPE project has highlighted the lack of technical standards elsewhere. A key result of the project has been to demonstrate just how effective technical standards are in reducing escapes. This has led to PREVENT ESCAPE's core recommendation that the most cost effective measure which will yield the greatest benefit in terms of reducing escapes is to introduce technical standards for the design, dimensioning and operation of sea-cage fish farms in other European nations. Since the PREVENT ESCAPE project commenced and after publication of the seminal research paper which demonstrated this (Jensen et al. 2012), Scotland has moved towards developing and implementing its own technical standard. SINTEF Fisheries and Aquaculture, the lead institute in PREVENT ESCAPE, has been engaged to assist in establishing the Scottish technical standard. Thus, the knowledge generated within PREVENT ESCAPE will be directly translated into the Scottish national standard.

In addition to the technical standards, PREVENT ESCAPE will provide knowledge for implementation and development of significant environmental and maritime EU policies. Specifically, PREVENT ESCAPE will address a range of EU policy related issues as follows:

- PREVENT ESCAPE will provide scientific information to support policies related to sustainable management of Europe’s natural resources and sustainable fisheries and aquaculture production. Escape of farm organisms is currently regarded by many as the most serious environmental threat of aquaculture and prevention or reduction of the amount of escaped organisms will be the first and foremost line of defence to avoid detrimental ecosystems effects. The avoidance of such effects is essential for conservation of biodiversity, sustainable use of wild resources and viable culture of aquatic organisms.

- PREVENT ESCAPE will contribute to achievement of the central objectives of the common fisheries policies. By providing knowledge that will contribute to reduction of fish escapes from marine aquaculture, PREVENT ESCAPE will implicitly also contribute to a viable coexistence of the fisheries and aquaculture industries. An integrated management of these two industries depends on resolution of conflicts related to environmental effects imposed by industrial activities. This will, among other issues, depend on knowledge and guidelines for avoiding critical environmental impacts.

- The application of the ecosystem approach to the management of natural resources is a key pillar in EU policies related to sustainable management and use of natural resources and ecosystem services. This involves that use of ecosystem services and ecosystem conservation should be promoted in an equitable manner. PREVENT ESCAPE will generate knowledge that will allow more effective use of ecosystem services as it will contribute to reducing the numbers of fish that escape, as well as providing knowledge that will reduce the risk of detrimental ecosystem impacts which implicitly will promote the conservation of natural resources.

Commercial/Industrial impact

Escape of farmed fish is not only an environmental problem; it also represents a direct economic loss for the industry, through loss of farmed fish, damaged equipment, clean-up operations and higher insurance costs. The project has estimated that the direct cost of escapes across Europe is in the order of EUROS 50 million yr-1. By providing knowledge that may PREVENT ESCAPEs as far as possible, PREVENT ESCAPE will thus contribute to increase the economic profitability of fish farming and the public’s perception of the industry.

Indirectly, escape events greatly damage the aquaculture industry's reputation as an environmentally sustainable enterprise, as escapees are perceived by consumers to cause environmental problems. Escape incidents are almost invariably followed by negative reports in the press. These perceptions may manifest in a number of ways, including feeding conflict and inhibiting expansion and development of sea-cage aquaculture in coastal waters. A significant reduction in the number of farmed fish that escape to levels that are not environmentally damaging would boost the confidence of consumers.

Finally, there is considerable momentum for the development of an offshore aquaculture industry in various locations in Europe. Results produced in PREVENT ESCAPE, both through improved operational techniques and development of more robust containment technologies, will inspire greater confidence for operators to venture to more offshore sites.

Science and technology impact

The attention directed to escapes, and implicitly also the knowledge and efforts devoted to manage and solve this problem, varies among fish farming countries in Europe. For instance, the significance of fish escapes as a factor affecting the ecosystems varies from country to country. In some countries, fish escape is perceived by some as positive as it is thought to strengthen wild populations of fish, a perception that over time may prove incorrect. In other countries, fish escapes are proven to affect important wild fish resources in a negative manner, which has significant socio-economic impacts and tarnishes the reputation of the farming industry. The varying perception of escapes as a problem and the differing level of knowledge among countries, called for collaborative research and development across borders. PREVENT ESCAPE has done exactly this, through active collaboration from the south to the north of Europe and through focusing its research on the most important European culture species. The three Norwegian institutes involved, SFH, NOFIMA and NINA, which had a pre-existing track record in escape-related research, have transferred knowledge to all other partners within the group, boost future regional research efforts in the topic of escapes.

Exploitation of PREVENT ESCAPEs results

Certain key results from the PREVENT ESCAPE project have already been exploited to reduce the main form of escape in Norway from 2008-2010. It is likely that this form of escape has also been a significant cause of escape elsewhere in Europe. Work conducted in WP2 identified the main causes of escapes in salmon aquaculture in Norway from 2008-2010. This form of escape was related to the sea-cage netting deforming with waves and currents and the netting then rubbing on the chains which connected the floating sea-cage collar to the bottom weighting ring. The chafed net would subsequently tear and a hole would form from which the fish could escape.

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