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4.5. POST-ESCAPE

BEHAVIOURS OF FARMED SEABREAM

AND SEABASS Cite this article as: Arechavala-Lopez P, Sanchez-Jerez P, Fernandez-Jover D, Bayle-Sempere JT, Uglem I, Dempster T (2013) Post-escape behaviours of farmed seabream and seabass. In: PREVENT ESCAPE Project Compendium. Chapter 4.5. Commission of the European Communities, 7th Research Framework Program. www.preventescape.eu ISBN: 978-82-14-05565-8

authors: Pablo Arechavala-Lopez1, Pablo Sanchez-Jerez1, Damiรกn Fernandez-Jover1, Just T. BayleSempere1, Ingebrigt Uglem2 & Tim Dempster3. University of Alicante, Spain; Norwegian Institute of Nature Research, Norway; 3 SINTEF, Norway. 1 2

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INTRODUCTION

OF THE PROBLEM/TASK

Escape of farmed fish from sea-cages is considered as one of the main environmental problems caused by aquaculture and it is perceived as a threat to natural biodiversity in marine waters (Dempster et al. 2007, Prevent Escape Compendium Chapter 1). Escaped fish may cause undesirable ecological effects in native populations through interbreeding, competition for food or habitats, as well as transfer of pathogens to wild fish or other farmed stocks (Fiske et al. 2005, Dempster et al. 2007, Thorstad et al., 2008). Escape events of gilthead seabream Sparus aurata and European seabass Dicentrarchus labrax have been sporadically recorded in the Mediterranean Sea (Dempster et al. 2002, Boyra et al. 2004, Vita et al. 2004, Tuya et al. 2005, 2006, Valle et al. 2007, Fernandez-Jover et al. 2008, Toledo-Guedes et al. 2009). Escapes occur mainly as a result of technical and operational failures in terms of cage breakdown due to extreme weather, holes caused by wear and tear of the netting and operational accidents (Prevent Escape Compendium Chapter 2). Farmed fish experience non-natural high densities within the cages, with an abundance of food and typically an absence of predators. This may affect the development of behaviour and possibly also entail artificial selection on traits that adapt the farmed fish to a life in captivity, and may also influence the fitness of escaped fish compared to their wild conspecifics (Huntingford et al. 2006, Salvanes and Braithwaite 2006). The post-escape behaviour of several other aquaculture fish species has been studied, for instance in Atlantic salmon Salmo salar (Thorstad et al. 2008, Skilbrei et al. 2009, 2010), and Atlantic cod Gadus morhua (Moe et al. 2007, Uglem et al. 2008, 2010, Hansen et al. 2009, Prevent Escape Compendium Chapter 4.4). These studies have suggested escapees are a potential risk to natural populations. However, few corresponding studies have been carried out for escaped fish from fish farms in the Mediterranean.

IMPORTANCE

OF SEABREAM AND SEABASS

Gilthead seabream have traditionally been cultured in the Mediterranean Sea and is a popular target species for fisheries which is regularly present in the fish markets. The world capture production of gilthead seabream is relatively constant across years, fluctuating from 5000 to 8000 t y-1 (total world capture was 7889 t in 2009). However, cultured seabream production has increased over the past 2 decades and now accounts for 95% of total seabream production (APROMAR 2011). The wild gilthead seabream is a subtropical fish that inhabits seagrass beds, sandy bottoms and the surf zone, commonly to depths of about 30 m, but adults may occur at 150 m depth. They occur naturally in the Mediterranean and the Black Sea (rare), and in the Eastern Atlantic, from the British Isles, Strait of Gibraltar to Cape Verde and around the Canary Islands. It is reported as a sedentary fish, though migrations are likely to occur on the Eastern Atlantic coast, from Spain to the British Isles. Seabream are present as either solitary individuals or in small aggregations. It is a euryaline species and moves in early spring towards protected coastal waters in search of abundant food and milder temperatures (trophic migration). In late autumn, they return to the open sea for breeding purposes, being very sensitive to low temperatures (lower lethal limit is 2째C). They are mainly carnivorous (shellfish, including mussels and oysters) and occasionally herbivorous (Froese and Pauly 2006).

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The European (or common) seabass is also a fish with high commercial interest for both aquaculture and fisheries. Captures fisheries production in the Mediterranean Sea and Atlantic Ocean remain relatively constant among years at 8000 – 12000 t y-1. Like seabream, aquaculture production now accounts for 90% of total seabass production (APROMAR 2011). The European seabass is a gonochoristic species demersal fish that inhabits coastal waters down to about 100 m depth, but is more common in shallow waters. They occur in coastal waters of the Atlantic Ocean from South of Norway (60°N) to the Western Sahara (30°N) and throughout the Mediterranean Sea and the Black Sea. They are found on various kinds of bottoms on marine coastal waters, estuaries, lagoons and occasionally rivers. Young fish form schools, but adults are less gregarious. Juveniles feed on invertebrates (shrimps and molluscs), but consume more fish in their diets as they grow. European seabass is a gonochoristic species. Spawning takes place in winter in the Mediterranean Sea (December to March) and in spring (up to June) in the Atlantic Ocean. Eggs and larvae disperse widely during the first 3 months of life and adults migrate over several hundreds of kilometres (Froese and Pauly 2006).

OBJECTIVE We simulated small and large-scale escape incidents with fish equipped with acoustic transmitters or tagged with external tags to: (i) assess the dispersion and survival of farmed seabream after an escape incident; (ii) test for connectivity among farms and local fishing areas through escaped seabream and seabass movements; (iii) study the habitat use and feeding habits of escapees; and (iv) evaluate to what extent escapees are recaptured by local fisheries.

POST-ESCAPE

BEHAVIOUR OF FARMED SEABREAM AND SEABASS

Simulated escapes of seabream and seabass were made from fish farms in a coastal bay in the southeast of Spain (UTM: 30S 0710736 4219249; Figure 4.5.1). In this bay, there are four floating-cage fish farms located 3 - 4 km offshore on soft muddy bottoms at depths ranging from 23 - 30 m. Distances among farms varied from 1 - 5 km. Farms F1, F3 and FR (the farm where the experimental releases were carried out) grow approximately 1200 t y-1 each, mainly of seabream but also seabass. Farm F2 was an inactive farm whose floating structures remain without fish and nets (Figure 4.5.1). Artisanal fisheries usually work at a local scale, i.e. near the coast and around farm facilities, only moving some kilometres away from their local harbours. Eleven artisanal vessels operate in the study area from the port of Guardamar del Segura, around 30 artisanal vessels from Santa Pola, 4 artisanal vessels from Tabarca and 9 vessels from Torrevieja (Figure 4.5.1). Most artisanal fishers were trammel-netters, with some long-line boats. Furthermore, a marine protected area with special fishing restrictions is located around Tabarca Island (Forcada et al. 2009).

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Figure 4.5.1 Farming area and acoustic receiver array (Vemco速, model: VR2W) where the seabream and seabass behavioural assessment was carried out. F: fish-farm facility; White pushpins: acoustic receivers sited at farms; Black pushpins: receivers surrounding the release farm (FR).

Survival and behaviour at farm facilities Tagging of seabream with ultrasonic tags allowed evaluation of their survival and movements after the simulated escape event. Escaped seabream survived up to 4 weeks at farm facilities and a high proportion of them remained at the release/escape farm for the first 5 days. The escaped seabream that remained next to farms for long periods tended to stay close to the surface during the night time, while they descended to greater depths in the morning (Figure 4.5.2). This may be a result of the natural diurnal variation in behaviour and vertical movements of escaped seabream, or may have been influenced by activity and feeding time (typically 06:00 to 14:00) at farms, since waste feed from farms becomes available at depths below 10 m for escapees and wild fish that reside outside the cages. Some escapees visited farms in the bay other than their release farm, indicating the existence of connectivity among farm facilities through their repeated movements among farms (Figure 4.5.3). Similar movement patterns were found for escaped seabass; several individuals moved quickly and repeatedly among several fish farms in the bay (Figure 4.5.3). Fast and repeated movements among fish farms might represent a vector for disease transmission (Uglem et al. 2009), since an infected escapee could spread pathogens to nearby cages.

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A high proportion of both escaped seabream and seabass dispersed away from farms within the first week and recorded mortality rates were high (50 - 60%). Toledo–Guedes et al. (2009) suggested that escapees show a high degree of site fidelity or, in contrast, low site fidelity but high mortality rates. High densities of piscivorous predators occur around farms in this specific area (Fernandez-Jover et al. 2008, Arechavala-Lopez et al. 2010), such as bluefish Pomatomus saltatrix, which are attracted to the farms due to an abundance of smaller prey fish. These predators occasionally enter cages and feed on the caged seabream and seabass (Sanchez-Jerez et al. 2008). Hence, it is likely the released seabream and seabass experienced high predation pressure during the first few days after escape. Further, it is likely that some of the tagged fish were caught by local fishermen and not reported. However, it cannot be ruled out that tagging in some way affected the behaviour and survival of the escapees.

Figure 4.5.2 Vertical distribution (bars) and daily detections (dots) of tagged seabream around fish farms during the period of a day. Bars show mean depth values with standard error lines. Plotted line shows mean number of daily detections. Dark area: night time; white area: day time; striped area: feeding time at farms.

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Figure 4.5.3 Movement sequences of escapees at farming area. Example of 2 tagged seabream individuals (A, B) and 2 tagged seabass individuals (C, D) within the receivers array visiting different farms (rectangles). Arrows represent a simulated direction of the tagged fish following the detections. F: acoustic receiver at farm; A-G: receivers surrounding release farm (FR).

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Dispersion, habitat use and feeding habits A high number of farmed seabream (>2100) and seabass (>1200) were externally tagged (Hallprint速, model: T-bar) and released at farm facilities, simulating escape events, to assess the dispersion of escapees. Altogether, a total of 159 tagged seabream (7%) and 15 tagged seabass (1%) that dispersed from farm facilities were recaptured by local fisheries. Professional trammel-netters (gill-nets) caught most escaped seabream (72%), while recreational fishermen (fishing rods) caught all of the recaptured escaped seabass (100%). For seabream, most of the tagged and recaptured individuals were caught over seagrass and sandy bottoms, where their wild conspecifics live, but some were also captured in Guardamar harbour. The recorded recapture rates should be regarded as minimum estimates due to possible tag loss (Sanchez-Lamadrid 2001) and capture under-reporting. It is remarkable that 75% of total recaptures were caught within the first week after escape (Figure 4.5.4). This indicates a high intensity of fishing on the released seabream, mainly during the first days after release, and presumably before the escapees had adapted to their new environment (Sanchez-Lamadrid et al. 2004). Moreover, the last 2 recaptures were reported 45 and 60 days after release in a nearby coastal fishing ground, and the two farthest recaptures were reported >20 km (the 3rd day) and >15 km (the 4th day) distance, both south and north, from the release farm. Moreover, a significant number of wild fish were caught together with escapees, even up to 20 km from the release farm. Analysis of the stomach content of recaptured seabream illustrated their ability to feed on the most common natural prey after a short period of time, as the feeding habits of escapees approached those of wild seabream one week after escape. Initially, escaped seabream fed on macrophytes and food pellets from farms. Later, they began to prey on echinoderms and crustaceans mostly associated with benthic habitats beneath farms. Finally, their diet shifted to more common natural prey from the fifth day after release, consisting mainly of molluscs and crustaceans. For seabass, individuals were recaptured gradually over 3 months at the same site (Figure 4.5.4), Guardamar harbour. Wild seabass are also commonly caught in this estuarine environment by local recreational fishermen. However, huge shoals of farmed individuals occur in local harbours after escape incidents at farms (Lopez pers. comm.). Stomach content analyses of recaptured seabass did not reveal as clear a pattern as for seabream. Empty stomachs, particulate organic matter, food pellets and natural preys (decapods, echinoderms and fish) were observed throughout the study period (from day 7 to 69). Further studies with a greater number of samples are necessary for a better understanding of feeding habits and habitat use of seabass escapees. Thus, the fact that feeding grounds and habitat use of both seabream and seabass escapees overlapped with their wild counterparts, since escapees occur together with their wild conspecific and are able to switch to natural prey within short time periods, reflects their potential for survival and interaction with wild fish populations.

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Figure 4.5.4 Percentage of recaptured tagged seabream and seabass from total recaptures throughout the study time.

DISCUSSION Escaped seabream and seabass can remain for long periods around farm facilities, making repeated movements among farms, which increases the risk of pathogen transmission to other farmed stocks. Moreover, they disperse from farm facilities to natural habitats and fishing grounds where they co-occur with wild conspecifics, and are able to utilize natural food resources within a short time frame. Therefore, the potential for interactions of escapees with wild populations is evident from our results. The initial mortality of farmed fish following small-scale escape incidents may be high, possibly as a result of predation, but vary according to season and the occurrence of predators around the farms. The recapture of seabream escapees from small-scale escape incidents that survive the first days may also be substantial, even without specific recapture fisheries. In addition, successfully recapturing escaped seabass appears more difficult than for seabream, due to their better swimming capability and dispersion. Our data do not allow long-term evaluation of the survival and ecological effects of escapees, but it is possible that the cumulative impact of escapees may be substantially reduced by the high rate of mortalities after escape. However, as known from other farmed species, even a modest survival rate after escape might entail negative ecological consequences for wild populations (Thorstad et al. 2008). A greater knowledge basis regarding the survival and movements of escapees following large-scale escape incidents is required to evaluate the potential for negative ecological impacts due to escaped farmed seabass. This will improve the management for recapture of escapees and thereby reduce the potential risk of intermingling and compete with natural populations.

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RECOMMENDATIONS s There is a high connectivity among farms through movements of escapees. This increases the potential risk of transfer of pathogens among farming sites. s Escapees are able to survive, disperse to nearby natural habitats, and feed on natural prey. These aspects increase the potential genetic and ecological risk of escapees to wild populations, since they could interbreed with wild conspecifics, prey upon wild food sources and thus compete for food and habitat, and share pathogens with wild stocks. s Predation of escapees immediately after escape incidents by wild fish closely associated to fish farms was likely significant. Thus, measures to maintain healthy populations of wild fish predators in the near vicinity of fish farms will assist in mitigating the ecological effects of escapees.

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LINKS

TO PUBLISHED DOCUMENTS

Arechavala-Lopez P, Uglem I, Fernandez-Jover D, Bayle-Sempere JT, Sanchez-Jerez P (2011) Immediate post-escape behaviour of farmed seabass (Dicentrarchus labrax) in the Mediterranean Sea. J Appl Ichthyol 27:1375-1378 Arechavala-Lopez P, Uglem I, Fernandez-Jover D, Bayle-Sempere JT, Sanchez-Jerez P (2012) Post-escape dispersion of farmed seabream (Sparus aurata L.) and recaptures by local fisheries in the Western Mediterranean Sea. Fisheries Research (in press). Sanchez-Jerez P, Fernandez-Jover D, Uglem I, Arechavala-Lopez P, Dempster T, Bayle-Sempere JT, Valle C, Izquierdo-Gomez D, Bjørn PA, Nilsen R (2011) Coastal fish farms as Fish Aggregation Devices (FADs). In: Artificial Reefs in Fisheries Management. Ed: Bortone S. et al., Taylor and Francis/CRC Press

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