Exploring the biological and socio-economic potential of new-emerging candidate fish species for the expansion of the European aquaculture industry – the DIVERSIFY project (EU FP7-GA603121)

by Constantinos C. Mylonas (Project Coordinator) and Nikos Papandroulakis (Greater amberjack species leader and Grow out work-package leader), Hellenic Center for Marine Research, Heraklion, Crete, Greece; Aldo Corriero (Reproduction & Genetics work-package leader), University of Bari, Italy; Daniel Montero (Nutrition and Fish Health work-package leader) and Carmen Maria Hernández-Cruz (Larval husbandry work-package leader); Fundación Canaria Parque Científico Tecnológico, Universidad de Las Palmas de Gran Canaria, Spain; Marija Banovic (Socioeconomics Task leader), University of Aarhus, Denmark; Gemma Tacken (Socioeconomics work-package leader), Wageningen University and Research, The Netherlands; Rocio Robles (Dissemination leader), CTAQUA, Spain (present affiliation Testing Blue S.L., Spain).

 

Introduction

Another one of the species included in the EU-funded DIVERSIFY project which ran between 2013 and 2018 was the greater amberjack (Figure 1). This is a valuable commercial species, but with a limited total worldwide catch of only 3,287 tonnes in 2009 (FAO, 2018). The greater amberjack flesh is much appreciated by consumers, especially for sushi and sashimi, and its market quotations are high, being around €8-16 per kg in Europe and reaching $20–30 per kg in Japan.

In the late 1980s, a greater amberjack farming activity was initiated in the Mediterranean basin, based on the capture and grow-out of juveniles from the wild (Lovatelli and Holthus, 2008; Ottolenghi et al., 2004). The rapid growth rate and worldwide market demand make the greater amberjack a very promising aquaculture species. Proper commercial aquaculture production, however, had not developed prior to the DIVERSIFY project. This was mainly due to its inconsistent and unpredictable reproduction in captivity, which prevented the development of hatchery production of juveniles.

Here we present a summary of the results obtained in DIVERSIFY, which enabled the commercial production of greater amberjack in the Mediterranean and East Atlantic regions.

 

Reproduction

In order to facilitate the broodstock management of greater amberjack in aquaculture, important life history traits of wild fish were first determined. Fish were shown to be 35-40 cm in length (fork length, FL) and 1 kg in weight (body weight, BW) at age 1; 60-70 cm FL and 3-5 kg BW at age 2; 80-90 cm FL and 7-10 kg BW at age 3.

Male greater amberjack are reproductively active at the age of 3 years and females reach the first sexual maturity at 3-4 years of age. The spawning season of the wild greater amberjack population from the western Mediterranean is extended from late May to early July. When greater amberjack reared in sea cages in the Mediterranean (Figure 2) were handled as other captive species, they exhibited poor gonadal development, low pituitary gonadotropin gene expression, low gonadotropin and sex steroid plasma concentrations, atresia of vitellogenic follicles, reduced proliferation and increased apoptosis of male germ cell (Pousis et al., 2018; Zupa et al., 2017a; Zupa et al., 2017b).

As a consequence of the spermatogenesis impairment, greater amberjack confined in captivity showed low sperm quality, in terms of sperm density, motility and velocity, as well as ATP content and membrane integrity (Zupa et al., 2017a). The observed reproductive impairments are likely related to the handling stress, the lack of optimal conditions required for reproductive maturation and/or to nutritional unbalances caused by the lack of specific broodstock diet for the species. In fact, gonads of captive-reared greater amberjack had different lipid and fatty acid contents compared to wild individuals. An overall improvement of rearing technology, particularly as it relates to husbandry operations (e.g. fish handling and transferring) together with a better formulation of dietary ingredients (Sarih et al., 2019) is suggested to overcome the observed dysfunctions and improve greater amberjack reproductive performance.

Greater amberjack reared in sea cages in the Mediterranean without any handling during the reproductive period, were treated successfully with the reproductive hormone gonadotropin releasing hormone agonist (GnRHa) implants and injections (Mylonas et al., 2018) (Figure 3). Treatments with GnRHa implants were more effective that injections in promoting the proper endocrine pathways leading to multiple cycles of oocyte maturation, ovulation and spawning and allowed producing more eggs with good fertilization, embryo survival, hatching and larval survival.

Greater amberjack caught from the wild in the eastern Atlantic (southwester coast of Gran Canaria, Spain) and reared for two years in indoor tanks under appropriate environmental and nutritional conditions (Sarih et al., 2019), were able to undergo normal gametogenesis, and spawned spontaneously large quantities of high-quality eggs (Sarih et al., 2018).

In the same stock, hatchery-produced F1 greater amberjack (15-30 kg body weight) reared in outdoor tanks in Tenerife (Spain) underwent normal gametogenesis and were induced successfully to undergo maturation, ovulation and spawning through the administration of GnRHa implants (Jerez et al., 2018). The repeated administration of GnRHa implants resulted in multiple spawns of high quality fertilized and viable eggs for an extended period lasting from May to September. Consistent egg production is now available for this species, and has enabled the further development of larval rearing methods within the project. Therefore, thanks to the experimental work carried out within DIVERSIFY, a set of tools to reproduce greater amberjack reared under different conditions in the Mediterranean Sea and in the eastern Atlantic is now available, and this represents a fundamental step towards the large-scale aquaculture production of this species.

 

Nutrition

To improve larval enrichment products for greater amberjack (Figure 4), the optimum levels and ratios of essential fatty acids and combined PUFA and carotenoids in greater amberjack enrichment products were determined (Roo et al., 2019). The highest growth was obtained when larvae (17-35 days after hatching, dah) were fed Artemia containing docosahexaenoic acid (DHA; 22:6n-3) in a range of 5-8% of Total Fatty Acids (TFA), with a maximum around 7% (1.5 g 100 g-1 DHA DM). The essential FA (EFA) requirements of the larvae are similar during the rotifer and Artemia feeding periods, as reported for larvae of other marine fish species.

Requirements of amberjack larvae for DHA (1.5 g.100 g-1DHA DM) were higher than those found in other marine fish species and similar to those for other fast-growing species. Increases in DHA levels tend to improve larval resistance to handling. Even the highest DHA levels in the enrichment emulsion (70% DHA of TFA) resulted in reduced incorporation of DHA into Artemia lipids (11% DHA of TFA).

Despite that eicosapentaenoic acid (EPA; 20:5n-3) levels in Artemia increased from 0.87 to 6.81 % TFA, EPA levels in greater amberjack larvae were only increased up to 5.2% of TFA, suggesting a saturation process that could be associated with the fulfillment of the EPA requirements. On the contrary, DHA levels in greater amberjack larvae showed a linear increase. Dietary DHA was linearly related to skull anomalies with dietary DHA levels over 2 g per 100 g-1 inducing a higher incidence of skeletal malformations, particularly those related with skull development.

It is well known that raising the ratio of Phospholipids (PL) to Total Lipids (TL) in larval feeds may enhance growth. Rotifers enriched with marine lecithin (E1) displayed a fast incorporation of polar lipids particularly rich in DHA. Although the role of carotenoids in the embryonic development is not very well established, there is evidence that the presence of carotenoids mitigates deleterious oxidative damage to the developing embryo.

Larvae fed diets with astaxanthin below 5.3 ppm were found to have marginal growth, whereas those fed levels above 5.3 ppm had a better performance and significantly higher lipid levels. Rotifers enriched with polar rich emulsion containing a marine natural lecithin LC60 combined with 10 ppm of Naturose (Cyanotech) also resulted in a significant advantage in larval growth, survival and welfare compared to rotifers enriched with other emulsions.

Thus, DIVERSIFY established the following recommendations for enrichment products for greater amberjack larvae culture: DHA in enrichment products for Artemia10-17% TFA, EPA 14-20% TFA, and DHA/EPA ratio 1-5. For rotifers (Brachionus sp.), DHA in enrichment products 14% TFA, EPA 6% TFA, and DHA/EPA ratio 2.3. Carotenoids levels in enrichment products must be around 10 ppm.

In broodstock diets, the requirements of essential fatty acids were determined to obtain improved spawning quality (Sarih et al., 2019). Broodstock fed a diet containing 1.57% EPA+DHA showed high fertilisation and egg viability, higher number of eggs per spawn and kg of female, with the highest percent of fertilization, egg viability, hatching rate and larval survival. Egg fatty acid composition was shown to be influenced by broodstock diets.

A diet containing 14-15 % EPA+DHA of total fatty acids (corresponding to 2.5-3 % in a dry diet) resulted in the best spawning performance in greater amberjack broodstock. Increasing dietary EPA+DHA contents did not improve spawning performance. Histidinecontents in broodstock diets ranging between 1 and 1.5% and inclusion of Taurine were shown to increase the reproductive performance of greater amberjack.

 

Larval husbandry

The objectives of DIVERSIFY for larval husbandry were to (a) study the effects of different feeding strategies on larval performance in intensive systems, and (b) develop feeding protocols and rearing methodologies in semi-intensive systems for the industrial production of the species. The results indicated that larval rearing in large tanks and low initial stocking of eggs-larvae improved the growth performance and survival of greater amberjack.

Egg stocking densities >25 eggs l-1affected negatively the results. For the different environmental parameters, the ranges considered as optimum can be summarized as follows: The recommended photo phase is 24L:00D from 1 to 20 dah and 18L:06D between 21 and 30 dah, with light intensities of 800, 1200, 1000 and 500 lux at 3, 6, 12, and 20 dah, respectively. A renewal of filtered seawater (5 μm) at an increasing rate ranging from 15-40% day-1 at 1 dah, 30-40% at 10 dah, 100-120% at 20 dah, and 200-240% at 30 dah ensures a good quality of the rearing environment.

Dissolved oxygen ranged between 4.9 and 8.2 mg l-1, but must be preferably > 6.0 mg l-1, salinity between 35 and 40 psu, pH between 7.8 and 8.5, and temperature between 23.5 and 25.0ºC. Furthermore, the feeding protocols used have to be coordinated with the rearing conditions and the larval development. The larva has to be able to see, ingest and digest the food, and therefore needs the coordinated development of vision and digestive system.

In general, the addition of live microalgae at 150-300 x 103 cell ml-1 from 1 dah, enriched rotifers two or more times a day, from 3 to 25 dah, at densities between 3 and 10 rot ml-1, Artemia nauplii at 12 dah and enriched 1-day-old Artemia EG at 14-18 dah, followed by commercial weaning diets (200-800 μm) from 18 dah can be a good sequence. Moreover, the live feed enrichment emulsions supplemented with PL, carotenoids, arachidonic acid (ARA; 20:4n-6) and immune modulators such as Echium oil and black cumin oil improved the larval rearing of greater amberjack, so enriching that results in these characteristics would give better results.

During larval rearing, and especially following 20 dah, high size variability occurred in all rearing systems tested to date. This high variability has been managed until now with early sorting of the reared groups to appropriate size classes. Applying standard methods and equipment available in all hatcheries, the sorting procedure resulted in significantly higher survival compared to unsorted groups (Figure 6).

 

Grow out husbandry

For the grow-out tasks of greater amberjack, development of methodologies emphasized cage technology (Figure 7). The feeding pattern of different age classes has been studied, while trials to define optimal stocking densities were implemented. Furthermore, there were trials aiming to study temperature effects on growth performance of greater amberjack.

Cage rearing is important for the commercial production of greater amberjack, but appears to be challenging. Several trials have been performed at an industrial scale and during all trials fish accepted commercial feed of appropriate composition, i.e. high protein (of fish origin) without problem. There was also no problem during the standard husbandry practices of net cleaning/changing and although the stocking density was not high, a value of ~ 5 kg m-3 is considered acceptable for a pelagic fish. Regarding the growth performance, during the first 4 months the growth was high (5 g d-1) while it decreased by 50% later on. Significant variations in growth were observed among individuals resulting in size variability of almost 100%, a problem that requires further investigation.

Environmental temperature was shown to affect significantly the performance of greater amberjack. Juveniles of 5 g held at 26ºC showed significantly higher body weight compared to fish held at 22ºC or 17ºC (Fernández-Montero et al., 2017). Morphological analysis showed that the increase of temperature led to an elongated fish body, especially of the head. For individuals of 350 g body weight, fish held at 21ºC showed significantly higher growth compared to fish held at 26ºC, while fish held at 16ºC showed the lowest final body weight.

The survival was higher at 16ºC, but there was no significant difference in the FCR for the whole experimental period of 3 months. Nutrient digestibility coefficients were high, indicating the good quality of the diets. Although temperature is one of many parameters affecting gut transit time, it did not affect energy fat, protein and dry matter digestibility in greater amberjack. Finally, fish of 500 g showed no significant differences for the temperature studied (20ºC and 23ºC) on feed intake and growth.

 

Fish health

Fish health is a key aspect to be optimized in cultured fish. Neobenedenia girellae is a monogenean parasite of the skin, and causes the main health problem for Atlantic populations of greater amberjack in aquaculture (Figure 8). This monogenean has been described in relation with water temperature increases in sea cages around the Canary Islands, Spain. New insights about the relation of this parasite with its host shows the mechanical damage that the fixation causes, resulting in thickening of the epidermis, vacuolization of epidermal cells, disruption of cellular layers, recruitment of goblet cells, and mononuclear cell lymphocytic type mobilization to the adhesion regions. Because of this, secondary infections appear and could result in 100% mortality.

New prevention strategies have been developed, such as the inclusion in the diet of mannan oligosaccharides (MOS and cMOS), which enhanced mucus production and increased the immune response, reducing the parasite load and growth (Fernández-Montero et al., 2019). A functional diet has been formulated to increase resistance of greater amberjack to the monogenean parasite Neobenedenia girellae and could be applicable for other monogenean parasites as well. This diet was based on a high protein inclusion (required for fast growing species) and the utilization of the mentioned additives with immunostimulant properties. This important milestone will provide a tool to reduce the incidence of this parasite in sea cages, reducing mortality of greater amberjack juveniles in farms.

Zeuxapa seriolae is another monogenean parasite of greater amberjack, considered the main health problem for greater amberjack culture in the Mediterranean region. This parasite gets attached to the gills (Figure 9), being hematophagous, producing important gill anaemia and inefficient oxygen exchange. Due to its rapid lifecycle and its increase with water temperature, it could cause the demise of the whole production.

Treatments with hydrogen peroxide at 75 ppm during 30 min have been reported to be efficient for killing the adults, always combined with repeated treatments after 15 and 30 days, and net changes to avoid reinfection from the released eggs. Other parasites have also been described, such as the blood fluke Paradeontacylix sp., which is a blood parasite that has been observed in cultured greater amberjack in the Mediterranean.

The proliferation inside the host circulatory system could produce obstruction of blood flow, resulting in ischemia and necrosis, and gill destruction when the eggs hatch. Penella sp.is one of the largest copepod parasites of fish, typically from swordfish (Xiphias gladius) and marine mammals. This parasite gets imbedded inside the skin of greater amberjack, nevertheless, it is not considered a problem for greater amberjack culture.

A Health Manual for greater amberjack describing different pathologies has been produced (https://www.diversifyfish.eu/amberjack-workshop.html) and is freely available in the project's website, and can be used immediately by the industry in order to improve their stock management.

 

Socioeconomics research

Market research in DIVERSIFY has identified two cross-cultural consumer segments of 'involved traditional', 'involved innovators' across the top fish markets in Europe (i.e. France, Germany, Italy, Spain, and the UK) comprising of consumers that could be more interested in adopting new DIVERSIFY fish species and greater amberjack in particular (Reinders et al., 2016). The market segmentation has further shown that the future aquaculture production lays in the hand of the consumers who are more dependent on and involved in ethical and sustainability issues.

The market segmentation further allowed opportunity to co-create new product concepts from DIVERSIFY fish species at the cross-border European level. The co-creation was undertaken with consumers from the same selected market segments mentioned above (Banović et al., 2016). The co-created product ideas were screened out and developed into product concepts and prototypes. From the selected concepts a few showed promising future if developed with greater amberjack.

One (i.e. fresh fish steak) was selected for the greater amberjack product prototype involving lower levels of processing (Figure 10). The physical prototype was selected based on the market potential, the consumer value perceptions, physicochemical characteristics of raw material, the technical properties of the products and the process, and the availability of similar products in the market. The undertaken research showed that product from greater amberjack was in all cases and across all investigated countries the best-perceived and -preferred product over all the other products developed from meagre, pikeperch, and grey mullet, always providing alignment with consumer expectations and consumption experience.

Furthermore, it has been found that the products with a lower degree of processing and those characterized by the distinctive fish sensory properties, as the product from grater amberjack, were those products that had higher consumer acceptance. Products with higher degree of processing were more accepted by the consumers who do not like fish because of its taste, odor, as well as the presence of bones. This shows that the presence of different processed product alternatives could be a good solution to be able to cover more consumer segments.

The developed product concept from greater amberjack was further tested for optimal labelling attribute combination on packaging and price range. The experiments were undertaken in the same selected countries and with the same product from greater amberjack developed into the previously tested prototype.

Based on this study it was concluded that country of origin and price are the attributes that drive the product acceptance, followed by quality certification (i.e. Aquaculture Stewardship Council - ASC label), while nutrition and health claims had a varying effect dependent on the country. The use of ASC label as the marketing signal to consumers that the product is coming from a controlled, certified and responsible aquaculture actually increases the likelihood of consumers adopting this product.

On the other hand, the use of nutrition and health claims actually assist European consumers to make more informed choices aligned with their preferences and stimulate health-related behaviour. However, nutrition and health claims are needed to be customized based on the target country. This research has also pointed to different segments of people how are nutrition conscious, ethnocentric, price conscious and eco-conscious, further suggesting possible targeted marketing campaigns that could be designed and used to further facilitate adoption of new fish species and greater amberjack in particular. Willingness to pay has also been estimated for the product from greater amberjack across investigated countries showing how the product should be priced.

The results from the virtual online market test also showed good acceptance of greater amberjack and its product in the same markets. This is related to two findings. First, the percentage of first-time buyers of greater amberjack product was above 10%. Even if one assumes that not every one of these first-time buyers might like the flavor of the new fish, it does inform that the new product has the serious potential on the market. Second, even those consumers that had not selected products from greater amberjack in the online market test, after receiving additional information decided to switch, with this number being above 11%. Finally, when the numbers of people that directly or indirectly purchased greater amberjack have been aggregated, a total acceptance rate of 1/4 was estimated with slight variations depending on the country (i.e.southern versus northern countries).

Based on the results obtained in DIVERSIFY, greater amberjack shows very promising market prospects, given its superior sensory characteristics, good consumer acceptance, and price margins. Nevertheless, its introduction would have a larger impact if done country by country instead of general pan-European level. The developing outlooks per country vary, as in some countries early adopters easily try new fish species, while in other countries consumers' need extra marketing efforts. In all investigated countries, introduction of the new products with a reference to already familiar products advances consumer acceptance.

Thus, the production of products from greater amberjack at an industrial scale is a feasible task (Figure 11) if raw materials of good quality are used, as sensory properties are decisive factor for consumers, especially in new fish species. Additionally, good production practices should be applied with proper traceability, as this further influence overall product acceptability. The above factors are necessary and adequate conditions for achieving high quality and economically satisfactory products.

A technical 'Production Manual' for greater amberjack, has been also produced by the project and is freely available in the project's website (https://www.diversifyfish.eu/amberjack-workshop.html), and can be used by the industry to begin investigating the potential of greater amberjack as an alternative marine species for European warm-water aquaculture.

 

 

References

Banović, M., Krystallis, A., Guerrero, L., Reinders, M.J., 2016. Consumers as co-creators of new product ideas: An application of projective and creative research techniques. Food Research International 87, 211-223.

FAO, 2018. The State of World Fisheries and Aquaculture 2018 - Meeting the sustainable development goals. Food and Agriculture Organization of the United Nations, Rome, 210 pp.

Fernández-Montero, A., Caballero, M.J., Torrecillas, S., Tuset, V.M., Lombarte, A., Ginés, R.R., Izquierdo, M., Robaina, L., Montero, D., 2017. Effect of temperature on growth performance of greater amberjack SERIOLA DUMERILI Risso 1810) Juveniles. Aquaculture Research 49, 908-918.

Fernández-Montero, Á., Torrecillas, S., Izquierdo, M., Caballero, M.J., Milne, D.J., Secombes, C.J., Sweetman, J., Da Silva, P., Acosta, F., Montero, D., 2019. Increased parasite resistance of greater amberjack (Seriola dumerili Risso 1810) juveniles fed a cMOS supplemented diet is associated with upregulation of a discrete set of immune genes in mucosal tissues. Fish & Shellfish Immunology 86, 35-45.

Jerez, S., Fakriadis, I., Papadaki, M., Martín, M., Cejas, J., Mylonas, C.C., 2018. Spawning induction of first-generation (F1) greater amberjack Seriola dumerili in the Canary Islands, Spain using GnRHa delivery systems. Fishes 3, 1-22.

Lovatelli, A., Holthus, P.F., 2008. Capture-based aquaculture; Global overview. Food and Agriculture Organization of the United Nations, Rome, 298 pp.

Mylonas, C.C., Fakriadis, I., Papandroulakis, N., M., P., Sigelaki, I., 2018. Broodstock management and spawning induction of greater amberjack, Seriola dumerili reared in sea cages in Greece, 11th International Symposium on Reproductive Physiology of Fish, Manaus, Brazil.

Ottolenghi, F., Silvestri, C., Giordano, P., Lovatelli, A., New, M.B., 2004. Capture-based Aquaculture. The fattening of eels, groupers, tunas and yellowtails. Food and Agriculture Organization of the United Nations, Rome, 308 pp.

Pousis, C., Mylonas, C.C., De Virgilio, C., Gadaleta, G., Santamaria, N., Passantino, L., Zupa, R., Papadaki, M., Fakriadis, I., Ferreri, R., Corriero, A., 2018. The observed oogenesis impairment in greater amberjack Seriola dumerili (Risso, 1810) reared in captivity is not related to an insufficient liver transcription or oocyte uptake of vitellogenin. Aquaculture Research 49, 243-252.

Reinders, M.J., Banović, M., Guerrero, L., Krystallis, A., 2016. Consumer perceptions of farmed fish: A cross-national segmentation in five European countries. British Food Journal 118, 2581-2597.

Roo, J., Hernández-Cruz, C.M., Mesa-Rodriguez, A., Fernández-Palacios, H., Izquierdo, M.S., 2019. Effect of increasing n-3 HUFA content in enriched Artemia on growth, survival and skeleton anomalies occurrence of greater amberjack Serioladumerili larvae. Aquaculture 500, 651-659.

Sarih, S., Djellata, A., La Barbera, A., Fernández-Palacios Vallejo, H., Roo, J., Izquierdo, M., Fernández-Palacios, H., 2018. High-quality spontaneous spawning in greater amberjack (Seriola dumerili, Risso 1810) and its comparison with GnRHa implants or injections. Aquaculture Research 49, 3442-3450.

Sarih, S., Djellata, A., Roo, J., Hernández-Cruz, C.M., Fontanillas, R., Rosenlund, G., Izquierdo, M., Fernández-Palacios, H., 2019. Effects of increased protein, histidine and taurine dietary levels on egg quality of greater amberjack (Seriola dumerili, Risso, 1810). Aquaculture 499, 72-79.

Zupa, P., Fauvel, C., Mylonas, C.C., Pousis, C., Santamaría, C.A., Papadaki, M., Fakriadis, I., V., C., 2017a. Rearing in captivity affects spermatogenesis and sperm quality in greater amberjack, Seriola dumerili (Risso, 1810). Journal of Animal Science 95, 4085-4100.

Zupa, R., Rodríguez, C., Mylonas, C.C., Rosenfeld, H., Fakriadis, I., Papadaki, M., Pérez, J.A., Pousis, C., Basilone, G., Corriero, A., 2017b. Comparative study of reproductive development in wild and captive-reared greater amberjack Seriola dumerili(Risso, 1810). PLoS ONE 12, e0169645.

This 5-year-long project (2013-2018) has received funding from the European Union's Seventh Framework Programme for research, technological development and demonstration (KBBE-2013-07 single stage, GA 603121, DIVERSIFY). The consortium includes 38 partners from 12 European countries –including 9 SMEs, 2 Large Enterprises, 5 professional associations and 1 Consumer NGO- and is coordinated by the Hellenic Center for Marine Research, Greece. Further information may be obtained from the project site at 'www.diversifyfish.eu'.

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