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First results of greater amberjack (Seriola dumerili) larval rearing in mesocosm
Aquaculture 250 (2005) 155 – 161 www.elsevier.com/locate/aqua-online
First results of greater amberjack (Seriola dumerili) larval rearing in mesocosm N. PapandroulakisT, C.C. Mylonas, E. Maingot, P. Divanach Institute of Aquaculture, Hellenic Center for Marine Research, P.O. Box 2214, 71003, Heraklion, Crete, Greece Received 19 April 2004; received in revised form 12 November 2004; accepted 1 February 2005
Abstract Species diversification is considered a major approach for the sustainable development of aquaculture. The greater amberjack (Seriola dumerili) has particular characteristics–advantages making it an appropriate candidate: high growth rate, large size, and established worldwide market. In the present study, the mesocosm method for larval rearing was applied, since it has been shown to be effective in the larval rearing of several species so far. This method is a semi-intensive technology, based on daily exogenous food addition, but also having the capacity of some endogenous productivity. Greater amberjack eggs were obtained from wild-caught fish matured in captivity in 6 years, after induced spawning with implants containing gonadotropinreleasing hormone agonist (GnRHa). A total of 9800 eggs survived after embryo appearance and were incubated in a 40-m3 tank with natural seawater of 40 psu. Rearing lasted 40 days. After mouth opening on day 2 post hatching, exogenous feeding with rotifers, Artemia nauplii and inert feed was initiated, while endogenous produced copepods contributed as food for the larvae from day 7 post hatching onwards. During rearing, larvae grew with an exponential rate of 0.073 day 1 in terms of total length (TL), and reached 39.9 F 5.4 mm and 0.5 F 0.1 g body weight at the end of the trial. All larvae inflated their swim bladder and completed metamorphosis at about 5 mm and 8 mm TL, respectively. Schooling behavior was first observed when larvae reached 9–10 mm TL, while aggression against the smallest individuals was first noticed the same period. The final population of about 350 individuals (3.5% survival) was transferred at the end of the trial for subsequent on-growing. The results obtained indicate the reliability of the technology for the larval rearing of the greater amberjack, and also its appropriateness for diversification with difficult marine species. D 2005 Elsevier B.V. All rights reserved. Keywords: Seriola dumerili; Mesocosm
1. Introduction
T Corresponding author. E-mail address: [email protected] (N. Papandroulakis). 0044-8486/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2005.02.036
The greater amberjack (Seriola dumerili) (Risso 1810) is a marine pelagic species with circumglobal distribution (Andaloro and Pipitone, 1997; Cummings et al., 1999; Thompson et al., 1999; Liu, 2001). It has
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a rapid growth rate (Thompson et al., 1999), reaching 6 kg in 2.5 years in culture (Jover et al., 1999; Mazzola et al., 2000; Pastor et al., 2000), excellent flesh quality and high worldwide demand (Nakada, 1999), and therefore has a great potential for the world aquaculture industry. The greater amberjack is reported to adapt easily to the captive environment, but its reproduction has proven difficult in culture conditions. Almost all research and commercial culture activities are based on wild-caught juveniles or eggs produced from hormone-induced mature breeders obtained from the wild (Tachihara et al., 1993; Jover et al., 1999; Nakada, 1999; Lazzari et al., 2000; Mazzola et al., 2000; Pastor et al., 2000; Garcia et al., 2001). Recently, successful maturation and spawning has been achieved with the use of gonadotropin-releasing hormone agonist (GnRHa) loaded into controlled-release devices (Mylonas et al., 2004). However, for the successful propagation of any species, larval rearing is still considered as the most critical step (Dhert et al., 1998) and, therefore, the development of appropriate tools is essential. Today, the range of available hatchery techniques is diverse (Divanach and Kentouri, 2000). The main classifications are based on the rearing density (intensive, extensive) and the use of phytoplankton in the water (clear, green, pseudo-green). In intensive hatcheries, larvae are reared at high densities under strict conditions and the pre-requisite for success is a high level of knowledge of their specific biological needs. However, the biological requirements of only few marine species are adequately known, so as to be reared at an industrial scale with intensive rearing methods. In extensive hatcheries, on the other hand, larvae are reared at low densities in large tanks under more natural (or, at least, less strict) conditions with an endogenous bloom of wild marine zooplankton. As a result, the probability of success is much higher than using the intensive approach and the extensive method has been already employed for more than 20 fish species (Divanach and Kentouri, 2000). Still, the challenge for industrial application of extensive methods is to increase their low productivity. The mesocosm is a semi-intensive technology that facilitates larval rearing of several species, solving the biological problems and many of their technical, human and economical consequences. In the present work, a mesocosm was used for the rearing of the
greater amberjack and preliminary data, the first ever obtained from this species in the Mediterranean, on the potential of rearing this difficult species are presented.
2. Materials and methods Eggs were obtained from a pair of broodstock (male: 16.7 kg, 92 cm total length; female: 12.5 kg, 89 cm total length) kept in captivity for 6 years, and induced to spawn using delivery systems loaded with GnRHa at a dose of 500 Ag fish 1 (Mylonas et al., 2004). A total of 9800 eggs survived after the appearance of embryo and were used for the rearing using the intensive mesocosm method (Divanach and Kentouri, 2000). Eggs were incubated in a 40-m3 tank, initially filled with surface seawater (salinity 40 psu), filtered at 300 Am in order to allow the entry of nano- and micro-plankton and to exclude predatory organisms. Water for any subsequent renewal was pumped from a littoral well (salinity 35 psu, temperature 21 F1 8C). The rate of water renewal started at 15% daily, increased to 50% after 17 days post hatching (dph), 100% at 25 dph and 150% at the end of the rearing at 40 dph. Water temperature ranged from 23.5 F 1 8C at the beginning to 21 F1 8C at 30 dph and remained constant until the end of the trial. Aeration was provided in the tanks by means of 5 wooden diffusers distributed in the perimeter and the center of the tank during the autotrophic stage. After the first feeding, only one diffuser was placed at the center of the tank. Phytoplankton (Chlorella minutissima) was added twice daily in the culture tank, in order to maintain a green medium at a concentration of 200 F 100 103 cells ml 1 for a period of 20 dph. Dissolved oxygen ranged between 6.0 and 7.0 mg l 1. A surface skimmer was installed between 2 and 15 dph to keep the surface free from lipids, a requisite for swimbladder inflation. The photophase was 24L/0D from mouth opening until 30 dph and natural for the remaining period. Light intensity varied according to weather conditions, ranging during the day from 1000 on cloudy days to 5000 lux (lx) on sunny days. During the night, when continuous photophase was applied, light intensity was about 250 lx. Temperature, salinity and dissolved oxygen were monitored daily in the tank.
N. Papandroulakis et al. / Aquaculture 250 (2005) 155–161 Table 1 Succession of food items for the larval rearing of the greater amberjack (Seriola dumerili) using the intensive mesocosm method Food
Delivery period Amount (days post hatching)
Phytoplankton 2–20 (Chlorella minutissima) Enriched rotifers 2–27 (Brachionus plicatilis) Enriched Artemia sp. 11–40 Artificial diet Frozen sea bream (Sparus aurata) eggs
11–40 26–40
100–200 cells ml 1 in culture water 2 to 3 individuals ml 1 in culture water 0.1 to 0.5 individuals ml 1 in culture water 2 to 30 g day 1 20 to 50 g day 1
The phytoplankton organism (Chlorella minutissima) was isolated from Heraklion bay since 1992 and mass-produced in photobioreactors (Hatziathanassiou et al., 2001). Cultured rotifers Brachionus plicatilis were enriched prior to distribution to the larvae with Chlorella minutissima and commercial products (DHA Protein Selco, INVE) in 500-l cylindro-conical tanks at a density of 300 to 500 individuals ml 1. Larvae were initially fed with enriched rotifers, followed by enriched Instar II Artemia sp. (A1 DHA Selco, INVE), artificial diet (Lansy, INVE), and sea bream (Sparus aurata) eggs (Table 1). Endogenously produced copepods (Harpacticoida, Tisbidae), developed on tank’s walls from 7 dph onwards, also contributed as food items for the larvae. Food was distributed manually in the tank twice daily at the beginning while after 17 dph, distribution of Artemia nauplii was performed 4–5 times daily. The concentration of prey in the larval tank was estimated, by sub-sampling of water taken from three places of the tank from the entire water column (Kentouri et al., 1994), prior to food delivery so that the appropriate quantity was added in order to reach the required concentration (Table 1). After 20 dph feeding with Artemia was also performed during night. Application of the above procedure allowed the concentration of zooplankton to be higher than 1.5 and 0.1 individuals ml 1 for rotifers and Artemia respectively during the rearing period. The artificial diet was provided manually at the beginning, prior to zooplankton distribution, when larvae were hungry and better accepted the new diet. Later, when larvae
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were accustomed to the diet, the artificial diet was distributed with automatic feeders every 15 min for 18 h day 1. Frozen fish eggs were delivered manually 3–4 times daily. Larval growth was monitored by daily measurements of total length (TL) and growth rate was estimated with regression analysis. Sampling was performed during feeding using a cup or, at later stages, a net for the capture of the individuals. At the end of the rearing period, juveniles were collected, counted and transferred to nursery tanks for subsequent operations. Measurements of wet weight and TL were taken from a sample of 50 individuals.
3. Results The produced eggs of greater amberjack were pelagic, spherical with a diameter of 1.03 F 0.02 mm, with a single oil droplet of 0.26 F 0.01 mm diameter and a segmented yolk. Embryo appeared about 10 h after fertilization (Fig. 1a) and hatching (Fig. 1b) occurred 30–34 h after spawning at 23.5 F 1 8C. The newly hatched larvae have TL of 2.88 F 0.22 mm (Fig. 2a). Yolk absorption took place 72 h after hatching, while the mouth opened 6 h earlier. Swim bladder inflation occurred about 120 h after hatching (3.87 F 0.23 mm TL; Fig. 2b) together with the absorption of the oil droplet (not visible under stereoscope). By 12–13 dph, at TL of 5.53 F 0.52
a
b Fig. 1. Stages of embryonic development of greater amberjack: a. Appearance of embryo; b. Hatching.
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a
b
c
d
e
Total Length (mm)
Fig. 2. Morphological changes of Seriola dumerili larva: a. Newly hatched larva (2.87 F 0.17 mm TL); b. 5-day-old larva (pre flexion stage; 3.87 F 0.23 mm TL); c. 12-day-old larva (flexion stage; 5.29 F 0.24 mm TL); d. 20-day-old larva (post flexion stage; 8.55 F 0.83 mm TL); e. Juvenile 40 days post hatching (35.63 F 6.52 mm TL).
mm, tail flexion took place (Fig. 2c). Almost 20 dph post larvae had a mean TL of 8.53 F 1.41 mm (Fig. 2d). At the end of the rearing period, 40 dph, juveniles (Fig. 2e) had TL of 39.88 F 5.44 mm and 0.5 F 0.1 g body weight. During rearing, individuals grew, in terms of TL (Fig. 3), with an exponential rate of 0.072 day 1 (r 2 = 0.94; n = 339; p b 0.001). Two growth periods however can be distinguished; the first from the beginning until 20 dph when larvae exhibit an exponential growth rate of 0.054 day 1 (r 2 = 0.75; n = 186; p b 0.001) and the second until the end of the trial with a relevant growth rate of 0.080 day 1 (r 2 = 0.75; n = 153; p b 0.001). All individuals had a functional swim bladder while only three of them (b1%) presented developmental abnormalities (operculum and skull). The final population at the end of the trial was 350 individuals (3.5% survival). One day after mouth opening almost 50% of the population was feeding on rotifers while all larvae contained rotifers in their stomachs a day later. Larvae were fed on copepods when they reached about 5.0 mm TL (11 dph) as it was evidence from their behavior (hunting near tank’s walls) and the gradual disappearance of the copepods in about 5 to 6 days. Post larvae did not accept well dry food and were better adapted when feed was distributed after hydration for 3–5 min. Trials with frozen fish (bogue, mackerel) were also unsuccessful. On the other hand post larvae accepted excellently the frozen fish eggs. At the end of the studied period moist feed, containing 50% frozen fish and 50% artificial diet (Lansy, INVE), was tested which was easily accepted by the
50 40 30 20 10 0 0
5
10
15
20
25
30
35
40
Time (days) Fig. 3. Total length (mean F S.D.) of greater amberjack larvae during the rearing (n = 8).
N. Papandroulakis et al. / Aquaculture 250 (2005) 155–161
juveniles. Schooling behavior was first observed when larvae reached 9–10 mm TL, while aggression against the smallest individuals was first noticed at the same period.
4. Discussion Lack of sufficient methodologies for the larval rearing of new species, for which a limited amount of biological information are available, has delayed diversification in marine finfish production for some time. Extensive rearing methods are more natural, mostly empirical and represent an easy way of establishing the first needs of unknown species. However, due to the very low productivity of these methods their industrial application is unfeasible at this stage. On the other hand, intensive methods require total control of the process and a high level of biological knowledge, which in most cases is not available when the first larval rearing trials are undertaken with novel species. These problems lead to the employment of semi-intensive rearing methods by many farms (Divanach, 2002; Papandroulakis et al., 2004), in order to address the early production of new species. The mesocosm technology employed in the present study is an intermediate between intensive and extensive methods of rearing, and can thus be considered as semi-intensive technique of mass production. The mesocosm is a relatively recent method, defined in the early 90s after studying the originally applied models (Grice and Reeves, 1982; Bever et al., 1985; Divanach, 1985; Kentouri, 1985; Lalli, 1990). It requires indoor or semi-outdoor infrastructures, designed for maximum utilization of solar energy. Both natural and artificial conditions are combined during the rearing, thus making the method independent of any climatic and/or seasonal changes. Two variants of the mesocosm exist according to the origin and quality of the food chain. In the extensive variant, the food chain is basically endogenous and complemented with exogenous input when symptoms of overgrazing appear. In the intensive variant, the food chain is basically exogenous, but exhibits a limited capacity of endogenous production, due to both the low density of larvae and the presence of phytoplankton in the environment. In both cases, the
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technology is characterized by a partial food autarky, and human errors during the rearing are less likely to have lethal effects on the larval population. The results achieved with the mesocosm methodology for the greater amberjack larval rearing are comparable to previous studies for the rearing of the species. Embryonic development followed the stages described by Tachihara et al. (1993). With a survival rate from embryonated eggs to 40 dph of about 3.5% and minimal occurrence of developmental abnormalities (b 1%), the results are better than the ones achieved by El-Zibdeh et al. (1996) and comparable with the ones presented by Ostrowski et al. (2001). In terms of survival rate, compared with results from rearing of other Seriola species, the results obtained in this trial are better than the ones for Seriola mazatlana (Benetti, 1997), comparable with those for Seriola lalandi (Tachihara et al., 1994, 1997) but lower than those for Seriola quinqueradiata (Benetti et al., 2001). Regarding growth performance, the greater amberjack in the present grew better than in the studies of El-Zibdeh et al. (1996), and comparably to the yellowtail kingfish (S. lalandi; Tachihara et al., 1994, 1997). The difference in growth performance observed between the first and the second half of the trial could be related to the food delivered to the larvae, both in terms of quality and quantity. At the beginning of the rearing, when feeding was based on enriched rotifers and Artemia, larvae did not grow well, although they consumed the delivered food. Enrichment of zooplankton, however, was done according to methods established for other species (gilthead sea bream, Sparus aurata and European sea bass, Dicentrarchus labrax) that have different nutritional requirements than the greater amberjack. Furthermore, the administration of food was based also on protocols established for these two species. Although the zooplankton concentration before each daily first feeding was well above values suitable for other species (N 1.5 and N 0.1 individuals ml 1 rotifers and Artemia, respectively), such prey densities might have not been entirely adequate in meeting the requirements of a species with high metabolic rate, such as the greater amberjack. This hypothesis is also supported by observations on the behavior of the greater amberjack larvae, which were more actively hunting during the morning after the first feeding,
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than during the rest of the day. Furthermore, we believe that the consumption of the endogenously produced copepods, which could have partially supported the population at this stage, was not sufficient to satisfy adequately the requirements of the larvae. During the second half of the rearing, on the contrary, when frozen sea bream eggs were delivered to the larvae and they adapted better to hydrated feed, growth was better. In addition, Artemia administration during the night could have also contributed to the better performance exhibited by the larvae. There is no doubt that many more studies of the nutritional requirements of the greater amberjack larvae are required, in order to achieve successful rearing. Improvements in the methodology, mostly related to food availability and quality of the diet, will certainly improve the results. For example, a more frequent distribution of food and an earlier application of feeding during the night could increase food availability and, thus, the performance of the population. Improvement of the weaning diets is also required, as the acceptability of the already available diets was not satisfactory. Emphasis should be given mostly on the texture of the diet as from our observations individuals accept easier diets after hydration, a process that does not affect its composition. Similar observations (unpublished data) have been made recently with species such as the common dentex (Dentex dentex) and dusky grouper (Epinephelus marginatus). The applicability of the mesocosm method for the larval rearing of new species is comparable to that of extensive techniques, which have been used successfully for fry production of 25 fish species and 5 hybrids (Divanach and Kentouri, 2000). Although the majority of these species have been reared by applying the mesocosm technology in its extensive form, species such as the common dentex (Koumoundouros et al., 1999), common pandora (Pagellus erythrinus), brown meagre (Sciaena umbra), and dusky grouper (Papandroulakis et al., 2003) were also produced using mesocosm of the intensive form. The mesocosm technology differs from other rearing techniques in terms of required infrastructures, environment of rearing, and food sources used. Food, from both endogenous and exogenous origin, ensures a good matching of larval energy requirements, while
minimizing the possibility of quality deficiencies or the risk of over grazing of the food chain. This partial autarky is very important for the effective application of the technology. The results obtained by the present study indicate the reliability of the technology for larval rearing in species diversification programs, and is a potential tool for production of difficult marine species. In addition, the rearing of the great amberjack larvae from cultured breeders, although of limited success, is expected to rekindle the interest for this species of high potential in the Mediterranean region.
Acknowledgements We would like to thank the technical staff at the Mesocosm hatchery of HCMR and especially Mr S. Stefanakis for their assistance during the rearing. Also two unknown reviewers for valuable comments on the manuscript.
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Liu, C.H., 2001. Early osteological development of the yellowtail Seriola dumerili (Pisces: Carangidae). Zool. Stud., 40, 289 – 298. Mazzola, A., Favaloro, E., Sara, G., 2000. Cultivation of the Mediterranean amberjack, Seriola dumerili (Risso, 1810), in submerged cages in the Western Mediterranean Sea. Aquaculture, 181, 257 – 268. Mylonas, C.C., Papandroulakis, N., Smboukis, A., Divanach, P., 2004. Induction of spawning of cultured greater amberjack (Seriola dumerili) using GnRHa implants. Aquaculture, 237, 141 – 154. Nakada, M., 1999. Yellowtail and related species culture. In: Stickney, R. (Ed.), Encyclopedia of Aquaculture. Wiley, pp. 1007 – 1036. Ostrowski, A.C., Laidley, C.W., Molnar, A., Zimmerman, J., Apeitos, A., 2001. Current status of greater amberjack Seriola dumerilii culture research at the Oceanic Institute. Aquaculture—2001: Book of Abstracts, 143 JM Parker Coliseum, Louisiana State University, Baton Rouge, LA 70803, USA. World Aquaculture Society 2001, p. 501. Papandroulakis, N., Kentouri, M., Stefanakis, S., Papadakis, I., Maingot, E., Sfakaki, E., Divanach, P., 2003. Rearing of three Mediterranean species (Pagellus erythrinus, Sciaena umbra, Epinephelus marginatus) with the Mesocosm technology. Proceedings of the 7th Panhellenic Conference of Oceanography and Fisheries. Hersonisson (Greece) 6–9 May 2003, pp. 340 – 341. Abstract only. Papandroulakis, N., Kentouri, M., Maingot, E., Divanach, P., 2004. Mesocosm. A reliable technology for larval rearing. Application Diplodus puntazzo and Diplodus sargus sargus. Aquac. Int., NS-4, 1 – 11. Pastor, E., Grau, A., Riera, F., Pou, S., Massuti, E., Grau, A.M., 2000. Experiences in the culture of new species in the dEstacion de AcuiculturaT of the Balearic Government (1980–1998). In: Basurco, B. (Ed.), Mediterranean Marine Aquaculture Finfish Species Diversification, Cahiers Options Me´diterrane´ennes, vol. 47. C.I.H.E.A.M, Zaragoza, Spain, pp. 371 – 379. Tachihara, K., Ebisu, R., Tukashima, Y., 1993. Spawning, eggs, larvae and juveniles of the purplish amberjack Seriola dumerilii. Bull. Jpn. Soc. Sci. Fish., 59, 1479 – 1488. Tachihara, K., El-Zibdeh, M.K., Ishimatsu, A., 1994. Effect of triidothyronine (T3) injection on seed production survival rate of goldstriped amberjack (Seriola lalandi). In: Watanabe, Y., Yamashita, Y., Oozeki, Y. (Eds.), Survival Strategies in Early Life Stages of Marine Resources, Proceedings of an International Workshop, Yokohama, Japan, pp. 39 – 48. Tachihara, K., El-Zibdeh, M.K., Ishimatsu, A., Tagawa, M., 1997. Improved seed production of goldstriped amberjack Seriola lalandi under hatchery conditions by injection of triiodothyronine (T3) to broodstock fish. J. World Aquac. Soc., 28, 34 – 44. Thompson, B.A., Beasly, M., Wilson, C.A., 1999. Age distribution and growth of greater amberjack Seriola dumerili, from the north-central Gulf of Mexico. Fish. Bull., 97, 362 – 371.
First results of greater amberjack (Seriola dumerili) larval rearing in mesocosm N. PapandroulakisT, C.C. Mylonas, E. Maingot, P. Divanach Institute of Aquaculture, Hellenic Center for Marine Research, P.O. Box 2214, 71003, Heraklion, Crete, Greece Received 19 April 2004; received in revised form 12 November 2004; accepted 1 February 2005
Abstract Species diversification is considered a major approach for the sustainable development of aquaculture. The greater amberjack (Seriola dumerili) has particular characteristics–advantages making it an appropriate candidate: high growth rate, large size, and established worldwide market. In the present study, the mesocosm method for larval rearing was applied, since it has been shown to be effective in the larval rearing of several species so far. This method is a semi-intensive technology, based on daily exogenous food addition, but also having the capacity of some endogenous productivity. Greater amberjack eggs were obtained from wild-caught fish matured in captivity in 6 years, after induced spawning with implants containing gonadotropinreleasing hormone agonist (GnRHa). A total of 9800 eggs survived after embryo appearance and were incubated in a 40-m3 tank with natural seawater of 40 psu. Rearing lasted 40 days. After mouth opening on day 2 post hatching, exogenous feeding with rotifers, Artemia nauplii and inert feed was initiated, while endogenous produced copepods contributed as food for the larvae from day 7 post hatching onwards. During rearing, larvae grew with an exponential rate of 0.073 day 1 in terms of total length (TL), and reached 39.9 F 5.4 mm and 0.5 F 0.1 g body weight at the end of the trial. All larvae inflated their swim bladder and completed metamorphosis at about 5 mm and 8 mm TL, respectively. Schooling behavior was first observed when larvae reached 9–10 mm TL, while aggression against the smallest individuals was first noticed the same period. The final population of about 350 individuals (3.5% survival) was transferred at the end of the trial for subsequent on-growing. The results obtained indicate the reliability of the technology for the larval rearing of the greater amberjack, and also its appropriateness for diversification with difficult marine species. D 2005 Elsevier B.V. All rights reserved. Keywords: Seriola dumerili; Mesocosm
1. Introduction
T Corresponding author. E-mail address: [email protected] (N. Papandroulakis). 0044-8486/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2005.02.036
The greater amberjack (Seriola dumerili) (Risso 1810) is a marine pelagic species with circumglobal distribution (Andaloro and Pipitone, 1997; Cummings et al., 1999; Thompson et al., 1999; Liu, 2001). It has
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a rapid growth rate (Thompson et al., 1999), reaching 6 kg in 2.5 years in culture (Jover et al., 1999; Mazzola et al., 2000; Pastor et al., 2000), excellent flesh quality and high worldwide demand (Nakada, 1999), and therefore has a great potential for the world aquaculture industry. The greater amberjack is reported to adapt easily to the captive environment, but its reproduction has proven difficult in culture conditions. Almost all research and commercial culture activities are based on wild-caught juveniles or eggs produced from hormone-induced mature breeders obtained from the wild (Tachihara et al., 1993; Jover et al., 1999; Nakada, 1999; Lazzari et al., 2000; Mazzola et al., 2000; Pastor et al., 2000; Garcia et al., 2001). Recently, successful maturation and spawning has been achieved with the use of gonadotropin-releasing hormone agonist (GnRHa) loaded into controlled-release devices (Mylonas et al., 2004). However, for the successful propagation of any species, larval rearing is still considered as the most critical step (Dhert et al., 1998) and, therefore, the development of appropriate tools is essential. Today, the range of available hatchery techniques is diverse (Divanach and Kentouri, 2000). The main classifications are based on the rearing density (intensive, extensive) and the use of phytoplankton in the water (clear, green, pseudo-green). In intensive hatcheries, larvae are reared at high densities under strict conditions and the pre-requisite for success is a high level of knowledge of their specific biological needs. However, the biological requirements of only few marine species are adequately known, so as to be reared at an industrial scale with intensive rearing methods. In extensive hatcheries, on the other hand, larvae are reared at low densities in large tanks under more natural (or, at least, less strict) conditions with an endogenous bloom of wild marine zooplankton. As a result, the probability of success is much higher than using the intensive approach and the extensive method has been already employed for more than 20 fish species (Divanach and Kentouri, 2000). Still, the challenge for industrial application of extensive methods is to increase their low productivity. The mesocosm is a semi-intensive technology that facilitates larval rearing of several species, solving the biological problems and many of their technical, human and economical consequences. In the present work, a mesocosm was used for the rearing of the
greater amberjack and preliminary data, the first ever obtained from this species in the Mediterranean, on the potential of rearing this difficult species are presented.
2. Materials and methods Eggs were obtained from a pair of broodstock (male: 16.7 kg, 92 cm total length; female: 12.5 kg, 89 cm total length) kept in captivity for 6 years, and induced to spawn using delivery systems loaded with GnRHa at a dose of 500 Ag fish 1 (Mylonas et al., 2004). A total of 9800 eggs survived after the appearance of embryo and were used for the rearing using the intensive mesocosm method (Divanach and Kentouri, 2000). Eggs were incubated in a 40-m3 tank, initially filled with surface seawater (salinity 40 psu), filtered at 300 Am in order to allow the entry of nano- and micro-plankton and to exclude predatory organisms. Water for any subsequent renewal was pumped from a littoral well (salinity 35 psu, temperature 21 F1 8C). The rate of water renewal started at 15% daily, increased to 50% after 17 days post hatching (dph), 100% at 25 dph and 150% at the end of the rearing at 40 dph. Water temperature ranged from 23.5 F 1 8C at the beginning to 21 F1 8C at 30 dph and remained constant until the end of the trial. Aeration was provided in the tanks by means of 5 wooden diffusers distributed in the perimeter and the center of the tank during the autotrophic stage. After the first feeding, only one diffuser was placed at the center of the tank. Phytoplankton (Chlorella minutissima) was added twice daily in the culture tank, in order to maintain a green medium at a concentration of 200 F 100 103 cells ml 1 for a period of 20 dph. Dissolved oxygen ranged between 6.0 and 7.0 mg l 1. A surface skimmer was installed between 2 and 15 dph to keep the surface free from lipids, a requisite for swimbladder inflation. The photophase was 24L/0D from mouth opening until 30 dph and natural for the remaining period. Light intensity varied according to weather conditions, ranging during the day from 1000 on cloudy days to 5000 lux (lx) on sunny days. During the night, when continuous photophase was applied, light intensity was about 250 lx. Temperature, salinity and dissolved oxygen were monitored daily in the tank.
N. Papandroulakis et al. / Aquaculture 250 (2005) 155–161 Table 1 Succession of food items for the larval rearing of the greater amberjack (Seriola dumerili) using the intensive mesocosm method Food
Delivery period Amount (days post hatching)
Phytoplankton 2–20 (Chlorella minutissima) Enriched rotifers 2–27 (Brachionus plicatilis) Enriched Artemia sp. 11–40 Artificial diet Frozen sea bream (Sparus aurata) eggs
11–40 26–40
100–200 cells ml 1 in culture water 2 to 3 individuals ml 1 in culture water 0.1 to 0.5 individuals ml 1 in culture water 2 to 30 g day 1 20 to 50 g day 1
The phytoplankton organism (Chlorella minutissima) was isolated from Heraklion bay since 1992 and mass-produced in photobioreactors (Hatziathanassiou et al., 2001). Cultured rotifers Brachionus plicatilis were enriched prior to distribution to the larvae with Chlorella minutissima and commercial products (DHA Protein Selco, INVE) in 500-l cylindro-conical tanks at a density of 300 to 500 individuals ml 1. Larvae were initially fed with enriched rotifers, followed by enriched Instar II Artemia sp. (A1 DHA Selco, INVE), artificial diet (Lansy, INVE), and sea bream (Sparus aurata) eggs (Table 1). Endogenously produced copepods (Harpacticoida, Tisbidae), developed on tank’s walls from 7 dph onwards, also contributed as food items for the larvae. Food was distributed manually in the tank twice daily at the beginning while after 17 dph, distribution of Artemia nauplii was performed 4–5 times daily. The concentration of prey in the larval tank was estimated, by sub-sampling of water taken from three places of the tank from the entire water column (Kentouri et al., 1994), prior to food delivery so that the appropriate quantity was added in order to reach the required concentration (Table 1). After 20 dph feeding with Artemia was also performed during night. Application of the above procedure allowed the concentration of zooplankton to be higher than 1.5 and 0.1 individuals ml 1 for rotifers and Artemia respectively during the rearing period. The artificial diet was provided manually at the beginning, prior to zooplankton distribution, when larvae were hungry and better accepted the new diet. Later, when larvae
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were accustomed to the diet, the artificial diet was distributed with automatic feeders every 15 min for 18 h day 1. Frozen fish eggs were delivered manually 3–4 times daily. Larval growth was monitored by daily measurements of total length (TL) and growth rate was estimated with regression analysis. Sampling was performed during feeding using a cup or, at later stages, a net for the capture of the individuals. At the end of the rearing period, juveniles were collected, counted and transferred to nursery tanks for subsequent operations. Measurements of wet weight and TL were taken from a sample of 50 individuals.
3. Results The produced eggs of greater amberjack were pelagic, spherical with a diameter of 1.03 F 0.02 mm, with a single oil droplet of 0.26 F 0.01 mm diameter and a segmented yolk. Embryo appeared about 10 h after fertilization (Fig. 1a) and hatching (Fig. 1b) occurred 30–34 h after spawning at 23.5 F 1 8C. The newly hatched larvae have TL of 2.88 F 0.22 mm (Fig. 2a). Yolk absorption took place 72 h after hatching, while the mouth opened 6 h earlier. Swim bladder inflation occurred about 120 h after hatching (3.87 F 0.23 mm TL; Fig. 2b) together with the absorption of the oil droplet (not visible under stereoscope). By 12–13 dph, at TL of 5.53 F 0.52
a
b Fig. 1. Stages of embryonic development of greater amberjack: a. Appearance of embryo; b. Hatching.
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a
b
c
d
e
Total Length (mm)
Fig. 2. Morphological changes of Seriola dumerili larva: a. Newly hatched larva (2.87 F 0.17 mm TL); b. 5-day-old larva (pre flexion stage; 3.87 F 0.23 mm TL); c. 12-day-old larva (flexion stage; 5.29 F 0.24 mm TL); d. 20-day-old larva (post flexion stage; 8.55 F 0.83 mm TL); e. Juvenile 40 days post hatching (35.63 F 6.52 mm TL).
mm, tail flexion took place (Fig. 2c). Almost 20 dph post larvae had a mean TL of 8.53 F 1.41 mm (Fig. 2d). At the end of the rearing period, 40 dph, juveniles (Fig. 2e) had TL of 39.88 F 5.44 mm and 0.5 F 0.1 g body weight. During rearing, individuals grew, in terms of TL (Fig. 3), with an exponential rate of 0.072 day 1 (r 2 = 0.94; n = 339; p b 0.001). Two growth periods however can be distinguished; the first from the beginning until 20 dph when larvae exhibit an exponential growth rate of 0.054 day 1 (r 2 = 0.75; n = 186; p b 0.001) and the second until the end of the trial with a relevant growth rate of 0.080 day 1 (r 2 = 0.75; n = 153; p b 0.001). All individuals had a functional swim bladder while only three of them (b1%) presented developmental abnormalities (operculum and skull). The final population at the end of the trial was 350 individuals (3.5% survival). One day after mouth opening almost 50% of the population was feeding on rotifers while all larvae contained rotifers in their stomachs a day later. Larvae were fed on copepods when they reached about 5.0 mm TL (11 dph) as it was evidence from their behavior (hunting near tank’s walls) and the gradual disappearance of the copepods in about 5 to 6 days. Post larvae did not accept well dry food and were better adapted when feed was distributed after hydration for 3–5 min. Trials with frozen fish (bogue, mackerel) were also unsuccessful. On the other hand post larvae accepted excellently the frozen fish eggs. At the end of the studied period moist feed, containing 50% frozen fish and 50% artificial diet (Lansy, INVE), was tested which was easily accepted by the
50 40 30 20 10 0 0
5
10
15
20
25
30
35
40
Time (days) Fig. 3. Total length (mean F S.D.) of greater amberjack larvae during the rearing (n = 8).
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juveniles. Schooling behavior was first observed when larvae reached 9–10 mm TL, while aggression against the smallest individuals was first noticed at the same period.
4. Discussion Lack of sufficient methodologies for the larval rearing of new species, for which a limited amount of biological information are available, has delayed diversification in marine finfish production for some time. Extensive rearing methods are more natural, mostly empirical and represent an easy way of establishing the first needs of unknown species. However, due to the very low productivity of these methods their industrial application is unfeasible at this stage. On the other hand, intensive methods require total control of the process and a high level of biological knowledge, which in most cases is not available when the first larval rearing trials are undertaken with novel species. These problems lead to the employment of semi-intensive rearing methods by many farms (Divanach, 2002; Papandroulakis et al., 2004), in order to address the early production of new species. The mesocosm technology employed in the present study is an intermediate between intensive and extensive methods of rearing, and can thus be considered as semi-intensive technique of mass production. The mesocosm is a relatively recent method, defined in the early 90s after studying the originally applied models (Grice and Reeves, 1982; Bever et al., 1985; Divanach, 1985; Kentouri, 1985; Lalli, 1990). It requires indoor or semi-outdoor infrastructures, designed for maximum utilization of solar energy. Both natural and artificial conditions are combined during the rearing, thus making the method independent of any climatic and/or seasonal changes. Two variants of the mesocosm exist according to the origin and quality of the food chain. In the extensive variant, the food chain is basically endogenous and complemented with exogenous input when symptoms of overgrazing appear. In the intensive variant, the food chain is basically exogenous, but exhibits a limited capacity of endogenous production, due to both the low density of larvae and the presence of phytoplankton in the environment. In both cases, the
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technology is characterized by a partial food autarky, and human errors during the rearing are less likely to have lethal effects on the larval population. The results achieved with the mesocosm methodology for the greater amberjack larval rearing are comparable to previous studies for the rearing of the species. Embryonic development followed the stages described by Tachihara et al. (1993). With a survival rate from embryonated eggs to 40 dph of about 3.5% and minimal occurrence of developmental abnormalities (b 1%), the results are better than the ones achieved by El-Zibdeh et al. (1996) and comparable with the ones presented by Ostrowski et al. (2001). In terms of survival rate, compared with results from rearing of other Seriola species, the results obtained in this trial are better than the ones for Seriola mazatlana (Benetti, 1997), comparable with those for Seriola lalandi (Tachihara et al., 1994, 1997) but lower than those for Seriola quinqueradiata (Benetti et al., 2001). Regarding growth performance, the greater amberjack in the present grew better than in the studies of El-Zibdeh et al. (1996), and comparably to the yellowtail kingfish (S. lalandi; Tachihara et al., 1994, 1997). The difference in growth performance observed between the first and the second half of the trial could be related to the food delivered to the larvae, both in terms of quality and quantity. At the beginning of the rearing, when feeding was based on enriched rotifers and Artemia, larvae did not grow well, although they consumed the delivered food. Enrichment of zooplankton, however, was done according to methods established for other species (gilthead sea bream, Sparus aurata and European sea bass, Dicentrarchus labrax) that have different nutritional requirements than the greater amberjack. Furthermore, the administration of food was based also on protocols established for these two species. Although the zooplankton concentration before each daily first feeding was well above values suitable for other species (N 1.5 and N 0.1 individuals ml 1 rotifers and Artemia, respectively), such prey densities might have not been entirely adequate in meeting the requirements of a species with high metabolic rate, such as the greater amberjack. This hypothesis is also supported by observations on the behavior of the greater amberjack larvae, which were more actively hunting during the morning after the first feeding,
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than during the rest of the day. Furthermore, we believe that the consumption of the endogenously produced copepods, which could have partially supported the population at this stage, was not sufficient to satisfy adequately the requirements of the larvae. During the second half of the rearing, on the contrary, when frozen sea bream eggs were delivered to the larvae and they adapted better to hydrated feed, growth was better. In addition, Artemia administration during the night could have also contributed to the better performance exhibited by the larvae. There is no doubt that many more studies of the nutritional requirements of the greater amberjack larvae are required, in order to achieve successful rearing. Improvements in the methodology, mostly related to food availability and quality of the diet, will certainly improve the results. For example, a more frequent distribution of food and an earlier application of feeding during the night could increase food availability and, thus, the performance of the population. Improvement of the weaning diets is also required, as the acceptability of the already available diets was not satisfactory. Emphasis should be given mostly on the texture of the diet as from our observations individuals accept easier diets after hydration, a process that does not affect its composition. Similar observations (unpublished data) have been made recently with species such as the common dentex (Dentex dentex) and dusky grouper (Epinephelus marginatus). The applicability of the mesocosm method for the larval rearing of new species is comparable to that of extensive techniques, which have been used successfully for fry production of 25 fish species and 5 hybrids (Divanach and Kentouri, 2000). Although the majority of these species have been reared by applying the mesocosm technology in its extensive form, species such as the common dentex (Koumoundouros et al., 1999), common pandora (Pagellus erythrinus), brown meagre (Sciaena umbra), and dusky grouper (Papandroulakis et al., 2003) were also produced using mesocosm of the intensive form. The mesocosm technology differs from other rearing techniques in terms of required infrastructures, environment of rearing, and food sources used. Food, from both endogenous and exogenous origin, ensures a good matching of larval energy requirements, while
minimizing the possibility of quality deficiencies or the risk of over grazing of the food chain. This partial autarky is very important for the effective application of the technology. The results obtained by the present study indicate the reliability of the technology for larval rearing in species diversification programs, and is a potential tool for production of difficult marine species. In addition, the rearing of the great amberjack larvae from cultured breeders, although of limited success, is expected to rekindle the interest for this species of high potential in the Mediterranean region.
Acknowledgements We would like to thank the technical staff at the Mesocosm hatchery of HCMR and especially Mr S. Stefanakis for their assistance during the rearing. Also two unknown reviewers for valuable comments on the manuscript.
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