ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on March 25, 2008
ICES Journal of Marine Science: Journal du Conseil 2008 65(4):551-559; doi:10.1093/icesjms/fsn037
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The trade of live crustaceans in Portugal: space for technological improvements
1 Unity of Upgrading of Fishery and Aquaculture Products (U-VPPA), National Institute of Biological Resources (INRB-IPIMAR), Avenida de Brasília, 1449-006 Lisbon, Portugal
2 Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Largo Prof. Abel Salazar 2, 4099-003 Porto, Portugal and Centre of Marine and Environmental Research of the University of Porto (CIIMAR-UP), R. Bragas, 289, 4050-123 Porto, Portugal
Correspondence to A. Marques: tel: +351 21 3027025; fax: +351 21 3015948; e-mail: marques_am{at}yahoo.com
Barrento, S., Marques, A., Pedro, S., Vaz-Pires, P., and Nunes, M. L. 2008. The trade of live crustaceans in Portugal: space for technological improvements. – ICES Journal of Marine Science, 65: 551–559.In Portuguese coastal areas, crabs and lobsters maintained alive until prepared for the table are commercially and economically very important. The trade in live crustaceans, mostly imported animals, is an interlinked and complex chain, from fishing, collection, holding facilities, and transportation, to the end-consumer, the various facilities playing a key role. Along the chain, animals can be affected by several stressors, inducing high mortality with consequent economic loss, and contributing to unsustainable exploitation of the resource. A survey was developed to characterize storage, transportation, and handling issues affecting various crustaceans at Portuguese holding facilities. In all, 22 facilities were identified and categorized by activity and water supply system. Despite the wide variation in their infrastructure, there were no major differences in mortality rate of crustaceans between importers, wholesalers, and exclusively retailers. At all facilities, Necora puber, Cancer pagurus, and Carcinus maenas had higher rates of mortality and shorter duration of captivity than Maja spp., Homarus sp., Panulirus regius, or Palinurus sp. Overall, the main problems identified were technical issues related to careless handling, high animal density, and the varying physiological needs of each species.
Keywords: crabs, handling, holding facilities, lobsters, transportation
Received 7 November 2007; accepted 13 February 2008; advance access publication 25 March 2008.
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Introduction |
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Portugal is the eighth biggest seafood consumer worldwide, with an average per capita consumption of 57.1 kg annually, well above the average world per capita consumption of 16.4 kg (data from 2003; FAO, 2007). Of the sought-after seafood products, crustaceans are central to Portuguese consumption and an important nutritional source for human consumption, providing all the essential amino acids, trace elements, and polyunsaturated fatty acids (precursors of biologically active molecules and crucial in preventing human cardiovascular and inflammatory disease; Skonberg and Perkins, 2002; Rosa and Nunes, 2003). In the past decade, the consumption of crustaceans in Portugal has increased by 59%, by 400 g per capita in 2005 along (DGPA, 2006; EUROSTAT, 2007). Consumption of seafood varies seasonally, increasing during summer and at the New Year. In Portuguese coastal areas, there is an ancient tradition of keeping certain crustacean species alive in holding facilities until needed for preparation, as a guarantee of freshness. The national trade of live crustaceans is commercially and economically very important, totalling almost 3000 t and
11 million (data from 2005; EUROSTAT, 2007). Crustaceans normally traded alive in Portugal are the edible crab (Cancer pagurus; 2325 t), Norway lobster (Nephrops norvegicus; 356 t), homarids (Homarus gammarus and Homarus americanus; 105 t), other crabs (spider crab, Maja spp.; green crab, Carcinus maenas; velvet crab, Necora puber; total 121 t), and spiny lobsters (mostly Palinurus elephas, Palinurus mauritanicus, and Panulirus regius; 70 t; data from 2005; EUROSTAT, 2007). The Portuguese crustacean fleet catches mainly N. norvegicus (318 t), C. maenas (219 t), Maja spp. (67 t), N. puber (43 t), P. elephas (12 t), P. mauritanicus (11 t), C. pagurus (9 t), and H. gammarus (4 t; data from 2006; EUROSTAT, 2007), but because of the shortage of national product, most live crustaceans are imported, to satisfy consumer demand. In fact, imports of live crustaceans accounted for 88% of national trade (EUROSTAT, 2007; INE, 2007). Most live animals are imported from other EU countries, especially France, the UK, and Spain (C. pagurus, H. gammarus, N. puber, Maja spp., C. maenas, and P. elephas), and small quantities also from the USA and Canada (H. americanus; 13 t), and from African countries (spiny lobsters; 49 t; DGPA, 2006; Holmyard and Franz, 2006; EUROSTAT, 2007).
The trade in imported and national live crustaceans is an interlinked, long, and complex chain from catch, through transportation, holding facilities, to consumption. Throughout this long chain, crustaceans are subjected to several stressors, such as periods of exposure to air, hypoxia, handling, interaction with other individuals, seawater physicochemical variation (e.g. temperature, ammonia, pH, salinity, nitrite, nitrate), and periods of starvation (Winkler, 1987; Whiteley and Taylor, 1992; Jussila et al., 1997; Paterson and Patrick, 1997; Taylor and Waldron, 1997; Taylor et al., 1997; Bergmann et al., 2001; Danford and Uglow, 2001a, b; Fotedar et al., 2001, 2006; Mercier et al., 2006; Ridgway et al., 2006; Woll, 2006). The effects of stress on live crustaceans tend to be cumulative, being reflected in increased rates of mortality at holding facilities (up to 66%; Burton, 2001), and up to 9.5% economic loss to those involved in the trade (data from 2003; FISHSTAT, 2007). Consequently, considerable quantities of crustaceans are wasted annually, representing important losses of valuable food and likely contributing to unsustainable exploitation of the resource.
The trade in live crustaceans is clearly highly dependent on importation, centralized in the holding facilities, and carries a considerable risk to what is obviously a valuable and profitable food source for the Portuguese, among others. Therefore, it is crucial that handling conditions at the most critical steps of the trade chain be evaluated. In this context, we carried out a thorough survey to characterize Portuguese holding facilities and handling conditions for each species, with the aim of developing strategies to decrease crustacean mortality.
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Material and methods |
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Surveys
In all, 31 holding facilities for live crustaceans were identified in Portugal, using information collected from (i) the Portuguese General Directorate of Fisheries and Aquaculture (DGPA), the government entity responsible for licensing the facilities; (ii) the Portuguese Association of Traders of Fishery Products (ACOPE); and (iii) the Portuguese national telephone directory. According to the DGPA, only 11 of these companies were officially licensed in 2006 as holding facilities for live crustaceans. We developed a survey to be sent to managers of these holding facilities, though participation was voluntary, and 22 facilities (including some that were officially licensed) across the country agreed to participate in it, representing 80% of the Portugal's total volume of trade (EUROSTAT, 2007). Holding facilities were categorized by activity type: (i) six importer–exporters (out of seven Portuguese companies identified as such; the main importer of spiny lobsters in Portugal declined to participate); (ii) nine wholesalers (which are also licensed as retailers); and (iii) seven that were exclusively retailers. Holding facilities were also categorized by their type of water supply system: open, semi-open, and closed.
All surveys were carried out at the holding facilities themselves, and the interviewer was able to observe the prevailing conditions. The three topics addressed in the surveys were: national trade chain, holding facility infrastructure, and species trading/storage conditions (Table 1). All species traded alive in Portugal were considered in the interviews: C. pagurus, Maja spp., N. puber, C. maenas, H. gammarus, H. americanus, P. elephas, P. mauritanicus, and P. regius. Nephrops norvegicus, although captured off Portugal, is rarely traded alive in national markets, because it is almost exclusively exported to Spain, so it was not considered in our study. For the remaining crustaceans, density, mortality rate, and captivity duration at a holding facility were presented as annual means.
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Statistical analysis
Differences among species, the nature of the holding facilities, and water supply systems were investigated with analysis of variance (ANOVA) and Tukey's multiple comparison. When necessary, data were transformed to satisfy normal distribution and homoscedasticity requirements, followed by non-parametric ANOVA (Kruskal–Wallis test), if transformed data could not meet these assumptions. All statistical analyses were tested at a 0.05 level of probability with the software STATISTICATM 6.1.
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Results |
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National trade chain
Most of the crustaceans imported come from foreign fishing vessels that offload their catches directly to be transported immediately to holding facilities in Portugal (Figure 1). On arrival, part of the catch is immediately conveyed to national traders, and the balance is stored in tanks. The major national traders are wholesalers/retailers and, to a lesser extent, restaurants, supermarkets, local seafood markets, and end-consumers. Small quantities of some species are exported either by the importation companies or through other holding facilities. The catch of Portuguese fishing vessels is usually sold at official auctions direct to wholesalers and retailers (Figure 1), although a small portion is unofficially sold directly to restaurants or to end-consumers.
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Infrastructure
Most of the holding facilities are <10 km from the sea and close to large cities such as Lisbon (Figure 2). In terms of their water supply system, closed systems are used by 45%, open systems by 32%, and semi-open systems by 23% (Table 2). Importers mostly use semi-open systems, wholesalers mainly semi-open or open systems, and retailers mainly closed systems (Table 2). The seawater used in these systems is mainly natural (95%) and obtained either by pumping it directly from the nearby open sea (75% of that pumped directly), estuary (17%), or lagoon (8%) in open and semi-open systems, or is transported by tank from the nearby open sea (56% of the water transported by tank), estuary (33%), or lagoon (11%) in closed systems. The seawater in open systems is renewed constantly, in semi-open systems it is renewed during the high tide, and in closed systems renewal takes place on average every 60 d (but ranging from weekly to twice per year). The capacity and the number of tanks used for open and semi-open systems are usually more than in closed systems (Table 2). All closed systems and 80% of the semi-open systems have chillers to cool seawater (to 10–13°C), but none of the open-system facilities we saw possessed chillers. Consequently, the water temperature in open and semi-open systems is more variable, dropping regularly to 10°C in winter and rising to 20°C in summer.
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To maintain water quality in the tanks, closed and semi-open systems usually have coal, sponges, or protein-skimmers, whereas open systems use sand (Table 2). In closed systems, more water-quality parameters are analysed regularly (salinity, temperature, ammonia, nitrites, pH, and nitrates) than in semi-open or open systems (generally just temperature and salinity; Table 2).
Feeding is common in semi-open and open systems, but rare in closed systems (Table 2). The practice of feeding is restricted in Portugal to Maja spp., homarids, and spiny lobsters, which are fed exclusively with bivalves such as mussels and clams.
Transportation and handling
Crustaceans imported from the EU are usually transported by tanks carried in refrigerated trucks (or in tankers), whereas imports from elsewhere are mainly by air.
Of the Portuguese importers, five have their own trucks, and one hires specialized transport companies. The loads of tankers and trucks mostly come from Scottish fishing ports or directly from Scottish fishing vessels, but sometimes also from French holding facilities. Usually, each truck has ten tanks filled with seawater at the animal's landing port or holding facility. Seawater is aerated, but not renewed or filtered during transportation (transport duration from Scotland to Portugal is 72 h, and from France to Portugal, 24 h). Each tank contains just one species at a maximum animal density of 1 kg l–1 (though densities are less for H. gammarus and P. elephas).
The transport by air of live crustaceans, mostly H. americanus, P. mauritanicus, and P. regius, is generally in cardboard boxes (in refrigerated and moist conditions), with separation between individual animals. Small refrigerated trucks are generally used to transport the animals between the airport and the holding facilities. Locally caught crustaceans are usually transported to holding facilities in wooden boxes or plastic buckets by small refrigerated trucks.
On arrival at a holding facility, part of the load (local and imported) is immediately distributed to wholesalers and retailers throughout the country by refrigerated truck, and the balance is stored in tanks at the holding facility. Depending on the species, three different procedures are used for offloading: (i) C. pagurus and Maja spp. are discharged into plastic boxes (30 kg capacity), weighed and thrown into tanks; (ii) homarids and spiny lobsters are unloaded individually, weighed, and placed carefully in the tanks; and (iii) N. puber (which are usually transported in 9 kg plastic or wooden boxes) are unloaded, dead animals discarded, and live animals transferred to tanks. In all facilities, dead animals are removed 3–5 h after arrival and twice per day thereafter.
Storage
Cancer pagurus, Maja spp., and H. gammarus are stored by all the holding facilities we surveyed, but N. puber, P. elephas, H. americanus, P. regius, P. mauritanicus, and C. maenas by 91%, 64%, 59%, 45%, 36%, and 14% of the facilities, respectively. Storage conditions varied between holding facilities (e.g. in the numbers of C. pagurus stored in closed and open systems; Tables 3 and 4).
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Differences in load size and subsequent mortality were found for the nine crustacean species, depending on the water supply system and the type of activity at the holding facilities (Tables 3 and 4). Rates of mortality were significantly higher for N. puber, C. pagurus, and C. maenas, and lower for P. elephas, Maja spp., H. gammarus, and H. americanus. In all water supply systems and activity types, significantly more C. pagurus were discharged per transportation than the other species. Storage was at significantly greater density in closed systems holding C. pagurus, H. americanus, and N. puber, in semi-open systems holding C. pagurus and P. mauritanicus, in open systems with C. pagurus and P. regius, at the facilities of importers of C. pagurus and H. americanus, and at the facilities of wholesalers of C. pagurus and P. elephas. The duration of captivity was usually longer for spiny lobsters, homarids, and Maja spp., and shorter for N. puber, C. maenas, and C. pagurus. Significant differences in the duration of captivity between facilities were found for P. elephas and H. gammarus held in closed systems, for P. elephas, Maja spp., and P. mauritanicus held in semi-open systems, for P. elephas, H. gammarus, and Maja spp. held in open systems, for Maja spp. at importers’ facilities, for H. gammarus and Maja spp. at wholesalers, and for P. elephas and both species of homarids at retailers.
Differences in the storage conditions of each species were also analysed in terms of type of water supply system and activity (Table 5). The analyses revealed no statistically significant differences in mortality rates, though retailers usually had higher rates of mortality of C. pagurus, Maja spp., C. maenas, H. americanus, and P. mauritanicus (Tables 3–5). Generally, semi-open systems and importers carried more animals per load of all species, though the differences were only significant for C. pagurus, Maja spp., and H. gammarus. Similarly, semi-open systems and importers usually maintained crustaceans at higher density, but differences were only significant for C. pagurus and H. gammarus. The densities naturally varied with the quantities carried by each truck or tanker, always being higher on the day of receipt at the facility, then decreasing as the product was sold, before the next load was received. In terms of duration of storage, open systems and retailers generally kept the crustaceans for longer in the tanks, and semi-open systems for shorter periods, though only significantly shorter for H. americanus and P. elephas.
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The length of time between loads varied among species, season (higher in summer and at the new year) and facility. Generally, the interval between loads was weekly (C. pagurus, N. puber, and C. maenas), two-weekly for homarids, and monthly for Maja spp. Palinurus mauritanicus and P. regius are typically traded whenever quantities of P. elephas are insufficient to satisfy market demand (mainly in summer). The periods between loads are usually more irregular and longer at wholesalers and retailers.
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Discussion |
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Infrastructure
Several studies have documented the trade chain of live crustaceans in the UK (Beard and MacGregor, 1991; Burton, 2001), France (Chartois et al., 1994), Australia (Bremner et al., 1997; Spanoghe and Bourne, 1997), India (Vijayakumaran and Radhakrishnan, 1997), the USA (Estrella, 2002), and Portugal (Araújo, 2006). However, to date, the type of holding facility has only been documented once, for France (Chartois et al., 1994). To the best of our knowledge, this work is the first attempt to quantify the conditions employed at the holding facilities to maintain crustaceans alive while awaiting sale.
The Portuguese trade of live crustaceans has some unique characteristics, in which the holding facilities play a central role. The facilities themselves are located mainly near landing ports and water supplies, to reduce costs related to transportation of natural seawater. Of the holding facilities we surveyed, importers and wholesalers generally had larger infrastructure than exclusive retailers in terms of storing the large numbers of live animals sought by the national market, particularly C. pagurus, H. gammarus, and P. mauritanicus. Importers and wholesalers generally employ cost-effective open or semi-open systems, with the purpose of reducing the costs related to treating large volumes of seawater. Such systems typically employ basic or no filtration systems, and control fewer water-quality parameters than closed systems (Salisbury, 2002). In contrast, retailers use mainly closed systems, because of the smaller facilities and volumes of seawater required. The management of closed systems is complex and laborious, requiring regular surveillance and maintenance of the physico-chemical parameters associated with water quality that are critical for crustaceans (temperature, salinity, oxygen, pH, ammonia, nitrite, and nitrate; Taylor et al., 1997). The larger volumes of seawater required for open and semi-open systems make the control of seawater temperature with chillers very expensive and difficult. However, owing to the importance of maintaining optimal conditions for crustaceans, 50% of importers, 57% of wholesalers, and 78% of retailers have such a device available.
Differences in seawater temperature along the trade chain pose an additional problem to the entrepreneurs. In particular, species from temperate regions are captured at low temperature (<10°C). Importers transport these animals at low temperature (average 10–15°C) to maintain low metabolic rates (e.g. of oxygen consumption and excretion) and to preclude stress and mortality (Chartois et al., 1994; Spanoghe and Bourne, 1997; Taylor et al., 1997). However, especially in summer, tank temperatures in open and semi-open systems without chillers increase above the optimal level (up to 20°C), thus contributing to higher rates of mortality. Salinity can also be problematic during winter because of precipitation, especially in open systems located close to estuaries or lagoons, because some crustacean species have a low tolerance to salinity variation (Chartois et al., 1994; Taylor et al., 1997).
Storage
Despite the great differences we saw in the infrastructure of the holding facilities, no major differences were found in the rates of mortality of all crustaceans between importers, wholesalers, and retailers. Generally, N. puber, C. pagurus, and C. maenas had greater rates of mortality and shorter duration of storage at the holding facilities than Maja spp., homarids, and spiny lobsters. The mortality of crustaceans is a direct consequence of cumulative stress along the trade chain, depending of course on the initial condition of the animal (soft shell, pale, empty, sick, and weak animals have little chance of survival to the table), the animal's physiological demands, the handling conditions, and technical issues related to storage (Chartois et al., 1994; Gomez-Jimenez et al., 2001). Data obtained during our survey indicate that each species faces different handling conditions during capture, transportation, and storage (e.g. the duration of transport, the unloading conditions, animal density, the extent of exposure to air, temperature variations, water quality, time in captivity), which can influence the levels of stress and hence the rates of mortality. Each species’ load quantity and economic value seems to influence the handling conditions. Crustaceans of low value per kilogramme in Portugal (e.g. C. pagurus, 5–12; C. maenas 5–7; N. puber, 14; Maja spp., 16) are generally handled less carefully than high-value per kilogramme species such as P. elephas (59–91), H. gammarus (40–47), H. americanus (20–28), P. mauritanicus (61), and P. regius (48). Note that these values are for 2007, obtained from a local Portuguese retailer.
Soon after capture of C. pagurus, the tendons in the dactyls of the chelae are cut to avoid injury/damage by the claws attributable to stress along the trade chain. This procedure causes needless wounds to animals that diminish their chances of survival, owing to the potential entrance of pathogens (e.g. Aerococcus viridans, Vibrio sp.) and loss of haemolymph (essential for gas transport and nutrition reserves; Ellender et al., 1992; Chartois et al., 1994). In terms of transportation, several tonnes of C. pagurus are loaded into lorry tanks, at high densities. Consequently, the crabs at the bottom are compressed by others above them and by handlers, and seawater accumulates significant quantities of excreted product (Chartois et al., 1994). On arrival at an importer's holding facility, the C. pagurus must be unloaded as fast as possible, meaning that careless discharge procedures are common (animals thrown into tanks, exposed to air, sunlight, and high temperature, and limbs lost). Finally, at the holding facilities, C. pagurus are maintained at high density (maximum density 300 kg m–3, even though the recommended stocking density for C. pagurus is 120 kg m–3; Chartois et al., 1994).
Despite the lesser quantities of N. puber and C. maenas traded, mortalities of those species can reach 50% during the first day of captivity. Despite the tendons in the dactyls of both species’ chelae not being cut after capture, the animals have very low tolerance to captivity, likely because of their fast rate of metabolism and aggression, and their limited capacity for acclimatization to temperature variation (Ingle, 1997; Cuculescu et al., 1998; Hopkin et al., 2006). The conditions during transport of those two species might also influence the rates of mortality, because individual animals are compressed and legs lost, and the death of one animal can promote the mortality of others (Hearn, 2002).
Generally, the rate of mortality of Maja spp. at holding facilities was low. Perhaps this was due to the different handling conditions of Maja spp. after capture (the tendons in the dactyls of the chelae are not cut), and to its rather greater physiological tolerance to variation in seawater temperature (8–19°C; Le Foll, 1993).
A different handling procedure is used for high-value species such as H. gammarus and H. americanus, to preclude cannibalism and physical damage following capture: the chelae are immobilized with elastic bandages. Palinurus elephas and both species of homarid had the lowest rates of mortality we found, likely because of the ultra-careful handling procedures (e.g. low density, animals loaded individually), and their high physiological tolerance to variations in seawater temperature in nature (H. gammarus, 7–19°C; H. americanus, –1–24°C; P. elephas, 9–20°C; Chartois et al., 1994). However, despite the careful handling of P. mauritanicus and P. regius, the rate of mortality of those species at the holding facilities was higher than that of P. elephas. This could be related to the species having different physiological demands. The optimal temperature range for P. regius (14–29°C; mortality is heavy <12°C; Chartois et al., 1994) can differ from the temperatures found at national holding facilities without chillers (10°C in winter).
During our survey, several traders stressed the seasonal nature of mortality trends, mainly of C. pagurus, C. maenas, N. puber, and P. regius. However, it was not possible for us to quantify the true seasonal variation in rates of mortality. Mortality of crabs was certainly highest during summer, likely because of the strong temperature variations along the trade chain, and lowest during winter. Seasonal mortality patterns for P. regius are the opposite of those for crabs, because this lobster requires higher temperatures to survive (>12°C).
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Conclusions |
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Overall, the main problems faced by Portuguese holding facilities are technical, related to the complex and time-consuming trade chain, storage conditions, handling procedures, animal densities, and the different economic value and physiological demand by species. Of course, possible solutions can be proposed to lessen the rate of mortality of live crustaceans during the trade chain. Following capture, all animals should be examined carefully (discarding individuals with soft shell, pale-exoskeleton, diseases, and notoriously weak), bandages should be used to immobilize the chelae, instead of cutting the tendon (plastic strips are currently used to immobilize claws in Australasian crab fisheries), air exposure and sunlight can be avoided, and on-board tanks with constant air flow can be used. Further, as the seawater temperature in some harbours is higher and the water more polluted than where the animals were originally caught, water flow to the tanks on board catching vessels should be stopped before entering port, though aeration should be maintained. Also at this stage, an anaesthetic agent could be used to decrease metabolism and stress. The same anaesthetic concentration could be used in the water of the trucks and tankers used for international and national transportation. Anaesthetics such as Aqui-S® are widely used in transporting ornamental aquatic animals, and for the culture of finfish and wild crustaceans. Cost-effective filtration systems and chillers could be installed on the trucks and tankers to maintain water quality at optimum levels, so allowing transportation in lesser volumes of seawater. Additionally, animal loading and unloading procedures need to be improved, to preclude mechanical and physico-chemical stress to the animals, air or sunshine exposure, and temperature variations. In holding facilities, water quality parameters should be regularly monitored and maintained at optimum levels for each species, by implementing efficient and cost-effective filtration systems and chillers. The maintenance of temperature throughout the trade chain is fundamental to precluding mortalities. Finally, rigorous codes of conduct and cautious handling conditions need to be implemented along the trade chain (similar to those described by FAO/WHO, 1979; Beard and MacGregor, 1991; APEC, 1999; Bennison, 2000; Woll, 2006).
To conclude, numerous improvements are required for the trade chain, to enhance animal welfare, to maintain high nutritional quality and safety of the animals, and to lessen the rates of mortality, economic losses, and ultimately the waste of an important, but finite, resource. To promote innovation and technological development, synergies between small and medium-size enterprises, scientific research institutes and industry are crucial tools in ensuring the ongoing viability of these important European products and the sector.
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Acknowledgements |
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The first two authors acknowledge a PhD scholarship and a Post-Doc grant, respectively, from the Portuguese Foundation for Science and Technology (FCT; Refs SFRH/BD/24 234/2005 and SFRH/BPD/33090/2007). The European Commission supported the study through the Collective Research Project "CrustaSea: Development of best practice, grading and transportation technology in the crustacean fishery sector" (Ref. COLL-CT-2006-030421). Finally, we thank the managers of the crustacean holding facilities who agreed to participate in the survey and to show us their sites and contents, and the two reviewers who made valuable comments on the draft text.
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