Aquaculture in the Middle East and North Africa: Status and Research

ENVIRONMENTAL SCIENCE, ENGINEERING AND TECHNOLOGY

AQUACULTURE IN THE MIDDLE EAST AND NORTH AFRICA

STATUS AND RESEARCH NEEDS

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AQUACULTURE IN THE MIDDLE EAST AND NORTH AFRICA

STATUS AND RESEARCH NEEDS

AZAD ISMAIL SAHEB AND SALAM AL-ABLANI EDITORS

Nova Science Publishers, Inc. New York

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Aquaculture in the Middle East and North Africa : status and research needs editors, Azad Ismail Saheb and Salam Al-Ablani. p. cm. Includes index. ISBN 978-1-62081-718-6 (eBook) 1. Aquaculture--Research--Middle East. 2. Aquaculture--Research--Africa, North. I. Saheb, Azad Ismail. II. Al-Ablani, Salam. SH125.A354A78 2011 639.8072--dc22 2011005657

Published by Nova Science Publishers, Inc. † New York

CONTENTS

Preface vii Chapter 1 Fish Diseases in Israeli Mariculture: New Research Challenges 1 Angelo Colorni and Arik Diamant Chapter 2 Parasitic Protozoans – Increasing Menace in Mariculture Facilities and Marine Aquarium in Kuwait 11 I. S. Azad and Ahmed Al-Marzouk Chapter 3 Status of Aquaculture Health Management in the Islamic Republic of Iran 19 Mehdi Soltani Chapter 4 Diseases in Wild and Cultured Fish in Turkey 31 Ercument Genc Chapter 5 Principle Fish Pathogens in Tunisian Aquaculture 41 Cherif Nadia and Hammami Salah Chapter 6 Breeding the Silver Pomfret, Pampus Argenteus (Euphrasen), for Aquaculture: Achievements and Challenges 49 Sulaiman M. Almatar and Charles M. James Chapter 7 Some Metocean Aspects for the Selection of Suitable Mariculture Sites in the Arabian Gulf 87 S. Neelamani Chapter 8 Industry Perspective of Aquaculture in the Middle East – Status and Issues 103 C. Regunathan Chapter 9 Aquaculture in Israel: Current Status and Innovative Approaches 155 W. M. Koven, S. Harpaz, J. Van Rijn and N. Mozes vi Contents

Chapter 10 Aquaculture Status and Needs in the Islamic Republic of Iran 191 Mehdi Soltani Chapter 11 Review of Moroccan Aquaculture 209 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla Chapter 12 Aquaculture in the Kingdom of Saudi Arabia: Growth, Prospects and Problems 257 Feisal Bukhari Chapter 13 Aquaculture in Turkey – Status and Needs 275 Hayri Deniz Index 319

PREFACE

World population at present stands at approximately 7 billion and is expected to cross the 9 billion mark by the middle of this century. Though, food for the growing population is believed to be adequately produced the quality of food remains a question. Food quality depends on the quality of protein, and the aquatic food, especially the fish, has to be ensured to improve the quality of living. The harvest from the seas and fishable waters has been on the decline. Aquaculture, whether through traditional practices or through high technology industries, has provided practical and economically feasible solutions to rescue the declining wild catches of food fish . Currently, the aquaculture industry contributes to over 50% of the fish landed in the market on a global scale. Interestingly, Asia holds the lion’s share by contributing more than 77% of the world fish production. However, contribution to aquaculture by the Middle East and North Africa, popularly known as the MENA region, is not so encouraging as only five countries; Egypt, Iran, Israel, Nigeria and Iraq and Turkey have a traditional inclination to aquaculture. The remaining countries in the MENA contribute to less than 1% of the world aquaculture production. Research in the field of aquaculture has been a traditional strong hold in Israel, Kuwait, Iran, Turkey, Morocco, Tunisia and Egypt. The challenges in the path of developing aquaculture as a food production sector have to be addressed by the experts in the region. An account of aquaculture status and research needs in the Middle East and North Africa is presented here with several renowned aquaculture experts of the region contributing either detailed chapters, or expert commentaries on aquaculture health. Expert commentaries in this book are devoted to a special topic of aquaculture health, thus emphasizing the importance of health of cultured aquatic species in an intensive congregated holding facility. Israel is one of the countries in the region with considerable aquaculture accomplishments both in the productivity and research related fields. Aquaculture of the gilthead seabream, Sparus aurata, European seabass (Dicentrarchus labrax), the white grouper (Epinephelus aeneus), the grey mullet (Mugil cephalus) and the bluefin tuna (Thunnus thynnus) during the last 30 years has contributed significantly to the progress achieved by Israel in this sector. Diseases have been seen as the stumbling blocks in the path of aquaculture and recent efforts have been aimed at obtaining the best protection for farmed fish and shellfish. This expert commentary gives an account of the disease condition and related interventions carried out in Israel. The commentary on ciliated protozoans in mariculture and aquarium facilities in Kuwait gives an over view of the increasing menace caused by this important group of parasites viii Preface which is assuming an alarming proportions in aquarium facilities. A special mention is made in the commentary of the silver pomfret (Pampus argenteus) as a new host for the scuticociliate, Uornema spp. Also, various host manifestations in the case of some of the important protozoan infections and future directions in the field of health management research are discussed. Iran is one of the important countries in the Middle East with considerable tradition of aquaculture and contribution to aquaculture in the MENA region. The expert commentary discusses aspects of health management of important aquaculture species in Iran which covers freshwater and marine fish and shellfish species. Poor environmental conditions, inappropriate health management strategies and outbreaks by some devastating infectious diseases such as WSD, IHN, IPN and streptococcosis are the major constraints that cause severe losses each year. Although both veterinary and fishery organizations approved some rules and legislations to improve health management criteria, there is a risk of exotic and economically important diseases that can be imported through the importation of eyed-eggs, larvae, brood stock and ornamental species into the country. However, some viral diseases including IHN, IPN and WSD have become a part of the endemic disease spectrum in the aquaculture sector. Followed by, is the commentary on aquaculture health in Turkey. Contribution by Turkey to the global aquaculture production and to that of the MENA region is note worthy. Cage culture of important sea fishes has flourished in Turkey in the recent past. Out of a current production of 780, 000 tonnes about a fifth comes from aquaculture. Currently, many researchers focus their efforts on new trends in fish health. One of them is eco-parasitology which discusses the recently described phenomenon of conspicuous metal accumulation by parasites and how this might be applied to environmental monitoring. They also suggest how environmental science and parasitology might profit from each other in the near future. The commentary on the health aspects in Tunisian aquaculture explains the recent problems faced by the sector in that country. This chapter takes note of the problems encountered by the Tunisian aquaculture sector due to the rapid extension of the rearing activity in some Tunisian regions, particularly in the field of pathology. This specialized database specifically describes some of the viral, bacterial and parasitic disease-related information and focuses on the available data of these pathogens which have either devastating effects on fish production in terms of high mortalities or reduction in growth of farmed fish. Focusing on studies related to improving diagnostic technique, the record provided the opportunity to have comprehensive information on the isolated and identified microorganisms. Eight full-length chapters were contributed by experts from different countries in the MENA region. Each of these chapters provides valuable information on the status and challenges faced by the aquaculture sector in the region. The first chapter deals with the fast depleting wild fish species, silver pomfret (Pampus argenteus), and gives full details of the successful attempt of captive breeding and larval rearing of the species. The Mariculture and Fisheries Department of Kuwait Institute for Scientific Research (KISR) provided a significant break-through in breeding and larval rearing of the very valued and fancied fish species not only in the region but also a widely liked species in the Asian countries. KISR succeeded, for the first time in 1998, in the larval rearing and grow-out culture of silver pomfret based on eggs collected from the wild. The egg collection trips from the wild enabled to study extensively the spawning frequency, fecundity, Preface ix type of spawning and availability of gravid fish in Kuwait waters. Over the years research has focused on refinements in hatchery larval rearing and grow-out production. Aquaculture site selection for marine fish farming is a challenging task. The chapter on “Some metocean aspects of site selection for cage culture in the Arabian Gulf” gives a newer dimension to the array topics selected for this book. The site selection is based on many aspects like the waves, climate, current intensity, tidal variation, quality of marine water, possibility for better flushing of the ambient water, water temperature and salinity, influence of the discharges from power stations, desalination and municipal wastes, ease of accessibility of the aquaculture cage site, ease and availability of suitable manpower, machines, materials, electric power etc. Developments of Mariculture in the Arabian Gulf may reduce the dependency on the imports of fish varieties. Mariculture must be economically feasible, efficient and pollution free. Thus, it is essential to select suitable sites from the view of different influencing environmental aspects. Information on aquaculture in the perspective of private entrepreneurs is lacking. This chapter on the status of aquaculture in the Gulf region on a private sector perspective desribes the aspects that a private sector looks at when it come to commercialization of aquaculture technologies The chapter deals with various aspects of financial supports, research back-up, interests of the private sector to take up aquaculture as a business venture etc., in the light of information on the policies and the regulations governing the activities in different countries. In Israel the aquaculture production technologies and the extensive research outputs have contributed tremendously to the rapid growth of aquaculture not only in the freshwater but also in the marine sectors. This chapter brings out an array of information on various aspects of aquaculture in Israel and discusses the problems. In Israel, water and land scarcity as well as potential environmental damage associated with the marine fish cage culture have been the driving forces behind the development of recirculation systems. A low-head recirculation concept was developed to produce the Mega-Flow system. This approach is based on providing water circulation and water aeration by means of airlifts. Iran has long been one of the traditionally aquaculture-oriented countries in the Middle East, where it has made tremendous progress in the field of aquaculture in the last 2-3 decades. Artificial propagation of sturgeon (Acipenseridae) fingerlings for restocking the Caspian Sea, aquaculture of species such as Rutilus frisii kutum, Caspian trout (Salmo trutta caspius), bream (Abramis brama), pike-perch (Stizostedion lucioperca), rainbow trout (Oncorhynchus mykiss) and four cyprinids species for restocking other suitable inland water bodies by the Iranian Fishery Organization (Shilat) were the major Fishery and aquaculture related developments. This chapter explains the recent trends and research developments in the field. Morocco is one of the few countries in North Africa that has forged ahead in the aquaculture sector. Freshwater aquaculture in Morocco started in 1924 through restocking of hatchery-produced juveniles of ecologically and socio-economically valued fishes. After the 90's, the private sector, with the support of the HCEFLCD, exhibited limited aquaculture investment in small areas. Marine aquaculture began in Morocco in the 50's and oyster farming was the first marine aquaculture activity. There after the country has witnessed several revolutionary changes in the field of aquaculture. The chapter on Aquaculture in Morocco deals with various facets of aquaculture development in the country and the challenges faced by the production and research wings. x Preface

Saudi Arabia is passing through amazing series of developments in aquaculture and the name of National Prawn Company is seen as a result of the increasing importance given to the seafood production. Several sea fish have been brought under the mariculture developments and thus, the sector is growing at a promising pace. This chapter explains the status and research needs of the sector in Saudi Arabia. The chapter on Aquaculture in Turkey focuses on the aquaculture development activities carried out in that country. Aquaculture is playing an increasingly important role in the Turkish economy, as fishery products are the only products of animal origin that are exported to the European Union. Many factors related to the political, economical and legal aspects have not been congenial for the future aquaculture developments. However, increasing fish consumption particularly in the domestic market is the main driving force for the development of aquaculture. The market potential for aquaculture products makes this sector one of the most attractive sectors for investment. Eight full-length chapters with detailed information on important aquaculture countries in the Middle East and North Africas and five expert commentaries covering various fish and shellfish health related aspects make this book an interesting reference material for researchers, teachers and administrators in the region. The authors are thankful to all the authors who contributed full-length chapters and expert commentaries. This book would not have been a reality without the active support from the authors.

Chapter 1

FISH DISEASES IN ISRAELI MARICULTURE: NEW RESEARCH CHALLENGES

Angelo Colorni∗ and Arik Diamant National Center for Mariculture Israel Oceanographic and Limnological Research Eilat, Israel

ABSTRACT

The gilt-head seabream Sparus aurata has been cultured for the last 30 years in Eilat (Israeli Red Sea) and the progress made in the farming of European seabass (Dicentrarchus labrax), the white grouper (Epinephelus aeneus), the grey mullet (Mugil cephalus) and the bluefin tuna (Thunnus thynnus) have all contributed to the aquaculture progress achieved by Israel. Diseases have been seen as the stumbling blocks in the path of aquaculture and recent efforts have been aimed at obtaining the best protection of farmed fish and shellfish. This commentary gives an account of the disease condition and related interventions carried out in Israel.

INTRODUCTION

Because of its euryhaline and eurythermal characteristics and general robustness, the gilthead seabream Sparus aurata has been cultured for the last 30 years in Eilat (Israeli Red Sea) and still dominates the production of the Israeli marine fish farming industry. However, significant progress has also been made in the farming of the European seabass Dicentrarchus labrax, the domestication of the white grouper Epinephelus aeneus and grey mullet Mugil cephalus, and first steps were taken in the study of the reproduction physiology of the Atlantic bluefin tuna (Thunnus thynnus). While a better understanding of the physiological requirements of new species in captivity is gradually achieved, health management remains a

∗ E-mail: [email protected] 2 Angelo Colorni and Arik Diamant high priority of Israeli mariculture, as progress of the veterinary aspects traditionally lags behind other technological advances of the culture practices. Awareness of the detrimental impact of fish farm operations on the environment has increased in recent years, as it is becoming clear that no matter how sophisticated technologies may be, uncontrolled environmental impact will ultimately render fish farm operations unsustainable. Until recently, most Israeli mariculture activities have been conducted in the Red Sea near the southern city of Eilat. The economic success of intensive mariculture in the region was due, to a large extent, to the fact that the cost of effluent treatment was never included. This approach is nearing its timely end. In inland fish farms that have been operating for some years with no effluent treatment, certain diseases kept re- appearing with astounding regularity. Since sea water inlets and outlets are oftentimes not overly distant from each other, we hypothesize that certain pathogen agents that are "amplified" during epizootics are released at significant amounts into the sea, and that over time, a low-level, "chronic" infection establishes in the local wild fish fauna, which then acts as an infection reservoir, establishing a stable source of contagion. Following a global trend, stricter policies regulating effluent discharge are gradually being enacted and enforced in Israel. Also, the need for developing alternative, environment-friendly and economically viable culture systems has become increasingly urgent (Shpigel et al. 1993; Cataudella 1999; Neori et al. 2000; Blancheton 2001). Ending a decade-long controversy, the Israeli government ruled to discontinue marine cage farming in the Red Sea because it was deemed detrimental to the local coral reefs. In the summer of 2008, the last of the sea-cages was removed from the Gulf of Eilat. Attempts are now under way to develop technologically advanced, storm-resistant submersible cages along the Mediterranean coast, to expand brackish water aquaculture, while the suitability of geothermal water for aquaculture is investigated, and polyculture practices encouraged. The elimination of sea-cage farming from the Red Sea has led to intensive RandD of inland recirculation aquaculture systems (RAS). The margins of tolerance in these systems are often extremely narrow and the consequences of even minor environmental deteriorations can be catastrophic. Although environmental pollution can be significantly reduced and the feasibility of an organic mariculture looks more promising, new health management problems related to the nature of these closed systems have appeared. The geographic latitudes, the cultured species and the husbandry methods employed greatly influence the type and severity of diseases. "Routine" pathogens such as Lymphocystis Disease Virus (LDV), “Pasteurella” (Photobacterium damselae ssp.) piscicida, Vibrio spp., etc., periodically still cause significant economic losses in Israeli mariculture, and one-time sporadic diseases (caused by Mycobacterium marinum, Streptococcus iniae, Lactococcus garvieae, Enteromyxum leei, Kudoa iwatai) seem to be on the rise. A particularly worrisome example is the emergence of encephalitis viruses (causing VER - Viral Encephalopathy and Retinopathy), which has put severe constraint not only on sea bass and grouper cultures, but also affected those of grey mullet, barramundi and red drum (Ucko et al. 2004). Two parasitoses, sustained by Amyloodinium ocellatum, a cosmopolitan dinoflagellate protophyton, and Cryptocaryon irritans, a ciliate protozoan found in marine fishes in tropical, subtropical and temperate seas - both virtually unknown in sea-cage culture - appear to be the main hazard to fish health in RAS, where their control is particularly challenging. Undoubtedly, physico-chemical factors, such as salinity, total organic matter, temperature, solar radiation, sedimentation, etc., as well as persistence of antibiotics and other residues from chemical treatments, all play a role according to the nature Fish Diseases in Israeli Mariculture 3

of each particular pathogenic agent. Under the artificial conditions of intensive mariculture, pathogen-host specificity has been known to break down on occasion (Colorni 1994; Colorni and Diamant 2005). Outside their natural hosts, certain bacteria are known to enter a starvation mode and a viable, albeit non-culturable (VBNC) state, while encysted stages of some parasites have developed asynchronous excystment strategies that enhance their infection dynamics. In any event, interaction of pathogens with the bacterial flora and microfauna in the bottom sediment or a fish pond biofilter clearly determines the fate of the disease agents. The ability of these pathogens to survive, remain infective and propagate in these artificial ecosystems has yet to be properly studied. Multitrophic (integrated) marine systems that incorporate fish, invertebrates and algae are a focus of investigation in Israel. Major efforts are now being invested in reducing capital and operational costs, which are typically considerably greater in RAS than in traditional flow-through systems.

BACTERIAL DISEASES

Sophisticated biotechnologies have been (or are currently being) developed and many microbial pathogens are today identified on a molecular basis. A direct PCR method for detection and identification of Mycobacterium marinum based on the 16S rRNA gene sequence was developed already sixteen years ago in Israel (Knibb et al. 1993), and the same methodology is available for several other bacterial fish pathogens (Hiney and Smith 1998; Zlotkin et al. 1998). A highly specific PCR assay for detecting Amyloodinium ocellatum dinospores was developed by Levy et al. (2007). In a study by Kvitt et al. (2008), PCR primers based on the DNA polymerase gene sequence were employed for the detection of Lymphocystis Disease Virus (LCDV) in gilthead sea bream Sparus aurata, and for monitoring the course of the disease from onset to full clinical recovery. In spontaneously infected fish, LCDV DNA was detected in skin and different internal organs, and a correlation was found between PCR intensity and the persistence of the virus in organs of recovered fish with no residual clinical symptoms. In experimentally infected fish, PCR detection was achieved almost two weeks before appearance of clinical signs. LCDV remained detectable in skin, caudal fin and eyeball for up to four weeks after external signs of infection had cleared. Randomly Amplified Polymorphic DNA (RAPD) and Amplified Fragment Length Polymorphism (AFLP) are DNA fingerprinting techniques which detect DNA restriction fragments by means of random PCR amplification. By using whole-genome structures rather than single gene sequences, both techniques have provided a generally higher level of precision in genotyping. AFLP in particular has become a useful genetic and epidemiological tool for detecting strain variation, e.g., in Photobacterium damselae ssp. piscicida (Kvitt et al. 2002), whereas for Lactococcus garvieae more discriminative results were achieved with RAPD (Colorni et al. 2003). Comparison of the 16S rRNA sequence of Streptococcus iniae isolates from Mediterranean Sea and Red Sea fish with that of S. iniae isolates from Israeli freshwater rainbow trout revealed 6 nucleotide differences (over a total of approximately 1500 nucleotides), which corresponds to 99.6% homology. Therefore, despite phenotypic, biochemical and pathogenetic similarities, Israeli marine and freshwater isolates were demonstrated to be distinct strains (Colorni et al. 2002). Both the AFLP and RAPD methods demonstrate high discriminative properties, the former differentiating among 4 Angelo Colorni and Arik Diamant closely related bacterial strains (Janssen et al. 1996; Blears et al. 1998), and the latter among group-A streptococci (Gardiner et al. 1995) and even S. iniae serotypes (Bachrach et al. 2001). Using Restriction Fragment Length Polymorphism (RFLP) of whole rRNA genes, Eldar et al. (1997) showed that Israeli isolates from tilapia and trout could be differentiated from U.S. S. iniae isolates from tilapia, and also showed that the S. iniae ATCC 29178T type strain (originally isolated from skin lesions of an Amazon River freshwater dolphin, Inia geoffrensis, held in captivity in San Francisco, California) (Pier and Madin 1976) belongs to a ribotype different from those of the piscine isolates.

PARASITIC DISEASES

Some Myxosporeans, upon gaining access to Sparus aurata and Dicentrarchus labrax cultures may cause serious harm. Others are quite innocuous, and may only under heavy infections become pathogenic. One of the most serious of the group is Enteromyxum leei, which was initially reported in cultured S. aurata from southern Cyprus (Diamant 1992). Subsequently, it emerged in Israel (Diamant et al. 1994) and soon afterwards was reported from additional countries around the Mediterranean (Le Breton and Marques, 1995; Sakiti et al. 1996; Fioravanti et al. 2004). Enteromyxosis is a chronic disease that leads to anorexia and severe emaciation. Affected fish eventually succumb with a typical bony dorsal ridge and bloated abdomen appearance. The parasite causes mass disintegration of gut mucosa. Diagnosis by spore morphology in fresh fecal smears (Figure 1) is straightforward in advanced cases, whereas early stages may be detected with a highly specific PCR-based assay (Palenzuela 2006). The host range for E. leei includes several non-sparid families, but detection has generally been limited to fish kept in captivity (Padrós et al. 2001). This disease is today widespread and the pathogen is probably present in the entire Mediterranean basin (Diamant et al. 2006). In recent years, an increase in the prevalence of Kudoa (the first myxosporean parasite reported from Sparus aurata) was observed in both land-based and sea-cage facilities in Eilat (Diamant et al. 2005). Infections with the same Kudoa species occurred in cultured European sea bass Dicentrarchus labrax and grey mullet Mugil cephalus kept in the same farms, as well as in 10 species of wild Red Sea reef fish, indicating that the parasite is non-specific and may parasitize a wide range of host species (Diamant et al. 2005). All affected species harbored similar 1-2 mm (up to 5 mm) whitish, spherical, or oval polysporous plasmodia, each filled with millions of spores, each containing 4 polar capsules (Figures 2, 3) The parasite establishes multiple site infections and is most commonly found in the muscles and intracranial adipose tissue of the brain and eye periphery, but also in subcutaneous adipose tissue, neural tissue, mouth, eye, mesenteries, peritoneum, swim bladder, intestinal musculature, heart, pericardium, kidney, and ovary. On the basis of the spore morphology, the parasite was identified as Kudoa iwatai Egusa and Shiomitsu, 1983, a species previously known only from fish of east-Asian Pacific waters. Ultrastructural features were comparable to those of previously studied Kudoa species. The 18S rDNA from 7 Red Sea isolates was sequenced and compared with the sequence of the same gene from K. iwatai isolated from cultured red sea bream, Pagrus major from Japan.

Fish Diseases in Israeli Mariculture 5

Figure 1. Enteromyxum leei live spores in Figure 2. Spore-packed young Kudoa iwtai fresh fecal wet mount from Oreochromis plasmodium in Sparus aurata. Nomarski mossambicus. Nomarski interference interference microscopy (Bar = 20μm). microscopy (Bar = 10μm).

Figure 3. Kudoa iwtai spores from S. aurata. Figure 4. Ceratomyxa sparusaurati spores from the Nomarski interference microscopy (Bar = gall bladder of S. aurata. Nomarski interference 20μm). microscopy (Bar = 20μm).

6 Angelo Colorni and Arik Diamant

The phylogenetic position of K. iwatai within the genus was determined using sequence analysis of all related taxa available in GenBank. The 3 isolates of K. iwatai clustered together in a newly formed, highly supported clade. The absence of records of Kudoa iwatai from the extensive Mediterranean sea bream and sea bass production industries supports these findings, implying that it is indeed not a Mediterranean species. K. iwatai appears to be an Indo-Pacific species that extended its natural host range in the Red Sea to include the gilthead sea bream, European sea bass, and grey mullet imported for mariculture from the Mediterranean. Nevertheless, it is important to note that should K. iwatai gain access to the Mediterranean, it may become a significant problem in sea bream and sea bass cultures. A third myxosporean that infects S. aurata is Ceratomyxa sparusaurati (Figure 4), which targets the gall bladder (Sitjà-Bobadilla et al. 1995). This parasite is usually rather innocuous, but may sometimes produce heavy infections that result in biliary system pathology. Since quarantine restrictions, especially in the past, have rarely been enforced, certain pathogens have been translocated over considerable geographic distances, usually with hatchery seed shipped from one locality to be cultured in another, or with adults caught in the wild to be used as broodstock. Therefore, rapid and accurate molecular diagnosis of pathogens is of great epidemiological importance. Precise taxonomic positions is often essential for the development of effective curative strategies. Significant headway has been made in recent years and identification may today be determined with much greater confidence. At the same time, the increase in precision has created frequent and widespread need for major taxonomic shifts and re-classifications. For example, Pasteurella piscicida has been renamed Photobacterium damselae ssp. piscicida (Gauthier et al. 1995), Myxidium leei Diamant, Lom and Dyková, 1994, has been changed to Enteromyxum leei (see Palenzuela et al. 2002), and Cryptocaryon irritans (Phylum Ciliophora), considered for half a century as the “seawater counterpart” of Ichthyophthirius multifiliis, was moved from the family Ichthyophthiriidae to the newly formed Cryptocaryonidae and re-classified to a different subphylum level (Wright and Colorni 2002).

NEW APPROACHES

As a new sub-discipline of fish immunology, the emerging field of antimicrobial research known as “host-defense peptide” biology seeks to understand how various life forms defend themselves by using endogenous, gene encoded, 10-50 amino acid peptides endowed with powerful, broad-spectrum antimicrobial properties. These molecules act rapidly and nonspecifically, stemming or preventing colonization of a wide range of potentially pathogenic microorganisms by affecting membrane permeability, inhibiting the synthesis of specific membrane proteins, or interfering with DNA synthesis (Kelley 1996; Schröder 1999). Recently detected, purified and characterized in fish, endogenous antibiotics (“endobiotics”) are peptides located in the epithelial surfaces of skin, gills and alimentary tract (Park et al. 1997; Cole et al. 1997, 2000; Robinette et al. 1998; Lauth et al. 2002; Noga et al. 2002). An important family of endobiotics, originally detected in hybrid striped bass, are “piscidins”, 22-amino acid peptides expressed in mast cells of gill, skin and gut and visceral blood vessels in various families of fish in the suborder Percoidei, including Dicentrarchus labrax (Silphaduang and Noga 2001; Noga and Silphaduang 2003). Their three members display a Fish Diseases in Israeli Mariculture 7

broad antibacterial spectrum and at least one of them is effective against protistan ectoparasites such as the dinoflagellate Amyloodinium ocellatum and the ciliate Cryptocaryon irritans (Colorni et al. 2008). Potentiating the natural, nonspecific, non-adaptive defenses of the host (such as histone-like polypeptides in S. aurata and piscidins in D. labrax) will limit use and dependence on treatment drugs and chemicals (antibiotics in particular) and is the innovative strategic course that fish health research has taken in the past few years. The factors affecting modulation (up- and down-regulation) of piscidins are being studied.

REFERENCES

Bachrach G, Zlotkin A, Hurvitz A, Evans DL, Eldar A (2001) Recovery of Streptococcus iniae from diseased fish previously vaccinated with a Streptococcus vaccine. Appl. Environ. Microbiol. 67, 3756-3758. Blancheton JP, Gaumet F, Gasset E, Conte M (2001) Recirculation systems for Mediterranean fish production: state of the art and prospects. International Aquaculture Conference, Verona, Italy, April 26-27, Abstract p. 30. Blears MJ, De Grandis SA, Lee H, Trevors JT (1998) Amplified fragment length polymorphism (AFLP): a review of the procedure and its applications. J. Ind. Microbiol. Biot 21, 99-114. Cataudella S (1999) Some remarks on responsible aquaculture. International Aquaculture Conference, Verona, Italy, February 11-12, Abstract p. 27. Cole AM, Darouiche RO, Legarda D, Connel N, Diamond G (2000) Characterization of a fish antimicrobial peptide: gene expression, subcellular localization, and spectrum of activity. Antimicrob Agents Chemother 44, 2039-2045. Cole AM, Weis P, Diamond G (1997) Isolation and characterization of pleurocidin, an antimicrobial peptide in the skin secretions of winter flounder. J. Biol. Chem. 272, 12008- 12013. Colorni A (1994) Hyperparasitism of Amyloodinium ocellatum (Dinoflagellida: Oodinidae) on Neobenedenia melleni (Monogenea: Capsalidae). Dis. Aquat. Org. 19, 157-159. Colorni A, Diamant A (2005) Hyperparasitism of trichodinid ciliates on monogenean gill flukes of marine fish. Dis. Aquat. Org. 65, 177-180. Colorni A, Diamant A, Eldar A, Kvitt H, Zlotkin A (2002) Streptococcus iniae infections in Red Sea cage-cultured and wild fishes. Dis. Aquat. Org. 49, 165-170. Colorni A, Ravelo C, Romalde JL, Toranzo AE, Diamant A (2003) Lactococcus garvieae in wild Red Sea wrasse Coris aygula (Labridae). Dis. Aquat. Org. 56, 275-278. Colorni A, Ullal A, Heinisch G, Noga EJ (2008) Activity of the antimicrobial polypeptide piscidin 2 against fish ectoparasites. J. Fish Dis. 31, 423-432. Diamant A (1992) A new pathogenic histozoic Myxidium (Myxosporea) in cultured gilt-head sea bream Sparus aurata L. Bull. Eur. Ass Fish Pathol, 12, 64-66. Diamant A, Lom J, Dyková I (1994) Myxidium leei n. sp., a pathogenic myxosporean of cultured sea bream Sparus aurata. Dis. Aquat. Org., 20, 137-141. Diamant A, Palenzuela O, Alvarez-Pellitero P, Athanassopoulou E, Golomazou E, Albiñana G, Padrós F, Crespo S, Lipshitz A, Ghittino C, Agnetti F, Marques A, Le Breton A, Raymond JF (2006) Epizootiology Of Enteromyxum Leei (Myxozoa: Myxosporea) in 8 Angelo Colorni and Arik Diamant

Mediterranean Mariculture Systems. 5th International Symposium On Aquatic Animal Health, American Fisheries Society, San Francisco, California, USA, Sept. 2006. Diamant A, Ucko M, Paperna I, Colorni A, Lipshitz A (2005) Kudoa iwatai (Myxosporea: Multivalvulidae) from wild and cultured fishes in the Red Sea: re-description, ultrastructure and molecular phylogeny. J. Parasitol. 91, 1175-1189. Eldar A, Frelier PF, Asanta L, Varner PW, Lawhon S, Bercovier H (1997) DNA restriction length polymorphysm of rRNA genes (rybotyping) allows distinction between Israeli and US S. iniae trout and tilapia isolates. FEMS Microbiol. Lett. 151, 155-162. Fioravanti M L, Caffara M, Florio D, Gustinelli A, Marcer F (2004). Nuove osservazioni sulle mixosporidiosi marine. Abstract, p. 33. XI Convegno Nazionale della Società Italiana di Patologia Ittica, Finale Ligure (Savona, Italy), 7-9 October 2004. Gardiner D, Hartas J, Currie B, Mathews JD, Kemp DJ, Sriprakash KS (1995) Vir-typing: a long-PCR typing method for group A streptococci. PCR Methods Appl. 4, 288-293. Gauthier G, Lafay B, Ruimy R, Breittmayer V, Nicolas JL, Gauthier M, Christen R (1995) Small-subunit rRNA sequences and whole DNA relatedness concur for the reassignment of Pasteurella piscicida (Snieszko et al.) Janssen and Surgalla to the genus Photobacterium as Photobacterium damsela subsp. piscicida comb. nov. Int. J. Syst. Bacteriol 45, 139-144. Hiney M, Smith P (1998) DNA-based diagnostics in aquaculture: can we overcome the problems of interpretation in the field? In: AC Barnes, GAD Davidson, MP Hiney, D McIntosh (eds), Methodology in fish research, Fisheries Research Services, Aberdeen, Scotland, UK, p 143-159. Janssen P, Coopman R, Huys G, Swings J, Bleeker M, Vos P, Zabeau M, Kersters K (1996) Evaluation of the DNA fingerprinting method AFLP as a new tool in bacterial taxonomy. Microbiology 142, 1881-1893. Kelley KJ (1996) Using host defenses to fight infectious diseases. Nature Biotechnol. 14, 587-590. Knibb W, Colorni A, Ankaoua M, Lindell D, Diamant A, Gordin H (1993) Detection and identification of a pathogenic marine Mycobacterium from the European seabass, Dicentrarchus labrax using polymerase chain reaction and direct sequencing of 16S rDNA sequences. Mol. Mar Biol. Biotech. 2, 225-232. Kvitt H, Heinisch G, Diamant A (2008) Detection and phylogeny of Lymphocystivirus in sea bream Sparus aurata based on the DNA polymerase gene and major capsid protein sequences. Aquaculture 275(1-4), 58-63. Kvitt H, Ucko M, Colorni A, Batargias C, Zlotkin A, Knibb W (2002) Photobacterium damselae ssp. piscicida: detection by direct amplification of 16S rRNA gene sequences and genotypic variation as determined by amplified fragment length polymorphism (AFLP). Dis Aquat Org 48, 187-195. Lauth X, Shike H, Burns JC, Westerman ME, Ostland VE, Carlberg JM, Van Olst JC, Nizet V, Taylor SW, Shimizu C, Bulet P (2002) Discovery and characterization of two isoforms of moronecidin, a novel antimicrobial peptide from hybrid striped bass. J. Biol. Chem 277, 5030-5039. Le Breton A, Marques A (1995) Occurrence of a histozoic Myxidium infection in two marine cultured species: Puntazzo puntazzo C. and Pagrus major. Bull. Eur Ass Fish Pathol, 15, 210-212. Fish Diseases in Israeli Mariculture 9

Levy MG, Poore MF, Colorni A, Noga EJ, Vandersea MW, Litaker RW (2007) A highly specific PCR assay for detecting the fish ectoparasite Amyloodinium ocellatum. Dis Aquat Org 73(3), 219-226. Neori A, Shpigel M, Ben-Ezra D (2000) A sustainable integrated system for culture of fish, seaweed and abalone. Aquaculture 186, 279-291. Noga EJ, Silphaduang U (2003) Piscidins: a novel family of peptide antibiotics from fish. Drug News and Perspect 16, 87:92. Noga EJ, Fan Z, Silphaduang U (2002) Host site of activity and cytological effects of histone- like proteins on the parasitic dinoflagellate Amyloodinium ocellatum. Dis. Aquat Org 52, 207-215. Padrós F, Palenzuela O, Hispano C, Tosas O, Zarza C, Crespo S, Alvarez-Pellitero P (2001) Myxidium leei (Myxozoa) infections in aquarium-reared Mediterranean fish species. Dis Aquat. Org., 47(1), 57-62. Palenzuela O (2006) Myxozoan infections in Mediterranean mariculture. Parassitologia, 48, 27-29. Palenzuela O, Redondo MJ, Álvarez-Pellitero P (2002) Description of Enteromyxum scophthalmi gen. nov., sp. nov. (Myxozoa), an intestinal parasite of turbot (Scophthalmus maximus L.) using morphological and ribosomal RNA sequence data. Parasitology 124, 369-379. Park CB, Lee JH, Park IY, Kim MS, Kim SC (1997) A novel antimicrobial peptide from the loach, Misgurnus anguillicaudatus. Fed. Eur. Biochem. Soc. Lett. 411, 173-178. Pier GB, Madin SH (1976) Streptococcus iniae sp. nov., a beta hemolytic streptococcus isolated from an Amazon freshwater dolphin, Inia geoffrensis. Int. J. Syst. Bacteriol. 26, 545-553. Robinette D, Wada S, Arroll T, Levy MG,, Miller WL, Noga EJ (1998) Antimicrobial activity in the skin of the channel catfish Ictalurus punctatus : characterization of broadspectrum histone-like antimicrobial proteins. Cell Mol. Life Sci. 54, 467-475. Sakiti N, Tarer V, Jacquemin D, Marques A (1996) Présence en Méditerranée occidentale d'une Mixosporidie histozoïque pathogène dans les élevages du daurade, Sparus aurata. Ann Sci Nat-Zool (Ser 13) 17, 123-127. Schröder JM (1999) Epithelial peptide antibiotics. Biochem. Pharmacol 57, 121-134. Shpigel M, Neori A, Popper DM, Gordin H (1993) A proposed model for “environmentally clean” land-based culture of fish, bivalves and seaweeds. Aquaculture 117, 115-128. Silphaduang U, Noga EJ (2001) Peptide antibiotics in mast cells of fish. Nature 414, 268-269. Sitjà-Bobadilla A, Palenzuela O, Àlvarez-Pellitero (1995) Ceratomyxa sparusaurati n. sp. (Myxosporea: Bivalvulida), a New Parasite from Cultured Gilthead Seabream (Sparus aurata L.) (Teleostei: Sparidae): Light and Electron Microscopic Description. J. Eukaryot. Microbiol 42, 529 – 539. Ucko, M., Colorni A., Diamant A. (2004) Nodavirus infections in Israeli mariculture. J. Fish Dis 27, 459-469. Wright ADG, Colorni A (2002) Taxonomic reassignment of Cryptocaryon irritans, a marine fish parasite. Europ. J. Protistol. 37, 375-378. Zlotkin A, Eldar A, Ghittino C, Bercovier H (1998) Identification of Lactococcus garvieae by PCR. J. Clin. Microbiol. 36, 983-985.

Chapter 2

PARASITIC PROTOZOANS – INCREASING MENACE IN MARICULTURE FACILITIES AND MARINE AQUARIUM IN KUWAIT

I. S. Azad∗ and Ahmed Al-Marzouk Mariculture and Fisheries Department (MFD) Kuwait Institute for Scientific Research (KISR) Salmiya, Kuwait

Aquaculture or confinement as experienced by the aquarium fish provide ample scope for the obligate and facultative fish parasites to cause considerable damage to the host fish on which they thrive. Protozoan parasites constitute an important group of fish parasites which are often associates with severe host mortalities. The myxozoans, the sporozoans (eg. Myxosoma sp), the ciliates (eg. Holotrichus – Icththyoptherius sp; freshwater “ich”, Cryptocaryon sp. the marine “ich” the scuticociliates – Uronema sp. and peritrichus- Trichodina sp.) and the flagellates (Icthyobodo sp. and Amyloodinium sp.) are some of the important protozoan ichthyoparasites. These parasites are seen even in marine fish both in commercial aquaculture and fish hobbyist’s holding facilities. Protozoan parasitic problems especially those by the ciliates regularly cause disease problems in the on-shore fish hatchery and rearing facilities of Mariculture and Fisheries Department (MFD) in Kuwait. Marine Aquarium of Scientific Centre, the major tourist attraction in Salmiya, Kuwait, also regularly reports of parasitic problems due to the “marine ich”, the scuticociliate and the Trichodinia sp. in its different exhibit fish species such as zobaidy (silver pomfret), the goatfish, the sea horse etc. Three major disease outbreaks due to the ciliates were noticed under the MFD facilities of KISR during the period 2003-2007. An out break due to the marine ich – Cryptocaryon sp. during 2003-04 and again during 2006; an episode of silver pomfret mortalities in April 2005 due to the scuticociliate and Amyloodinium-related bluefin bream (Sparidentax hasta) mortalities during June 2007 were recorded by the fish health scientists of MFD.

∗ Corresponding author: [email protected]; Phone: +965-25711295; Fax: +965-25711293 12 I. S. Azad and Ahmed Al-Marzouk

All these episodes were severe on cultured silver pomfret adults and sub-adults and the bream, respectively. The incidences of scuticociliatosis were associated with a raise in the water temperature, increased bacterial load and the sensitivity of the fish species. The flagellated protozoan (Amyloodinium) was suspected to be due to the protozoan spore- contaminated forage fish, minor mullet. Sporadic incidences of marine ich infestations were also recorded from the breams and groupers in the facilities of both, MFD and Marine Aquarium of Scientific Centre, Kuwait.

Cryptocaryon Sp.

The marine ich has been reported to cause severe mortalities in silver pomfret, orange spotted grouper (Epinephelus coioides) and the silvery-black porgy (Sparidentax hasta) in the on-shore rearing facilities of the Mariculture and Fisheries Department of KISR, Kuwait [1,2]. Severity of infection was coinciding with a raise in the water temperatures during May- June and with deteriorated water quality (total heterotrophic bacterial counts exceeding 105 CFU/ml in the water supply). Upon an earliest detection of the parasite, freshwater bath or 5- 7 day treatment with copper sulphate (25 ppm for 2-3 h immersion) was found to be satisfactory in controlling the spread of the disease. However, it was almost impossible to stop the mortalities once the disease was blown-up. Tank-cultured orange spotted grouper (E. coioides) in on-shore tank facilities of was infested by C. irritans resulting in about 50% mortality [2]. Similar out breaks were reported in these facilities stocked with bluefin bream (S. hasta) during 2004-05. The parasite appeared again in 2008 causing 30-40% larval mortality in one of the bluefin bream larval rearing tanks (Figure 1). The marine ‘ich’ belongs to the group of holotrichous ciliates and is an obligate parasite infecting almost all types of fish [3,4] unlike the scuticociliate which prefers soft-skinned and small-scaled fish such as tuna [5] and silver pomfret [6]. C. irritans, the prime causative of marine ‘ich’ disease, is known to have a wide geographical distribution with records from the Indo-Pacific, the Persian Gulf, the Red Sea, the Atlantic Ocean and the Caribbean Sea7. Marine aquaculture and marine aquariums have been often reported have suffered severe losses due to the marine ‘ich’. Red sea bream tiger puffer and the flounder were found to be severely infested with the marine ‘ich’ [8, 9], thus widening the species range that could become susceptible to this devastating protozoan parasite. Aquaculture stress and the crowding seem to provide the right environment for the proliferation and pathogenesis of marine ‘ich’. Dangers of threats due to outbreaks were predicted long ago by Mathews and co-workers [10] due to the growing ornamental fish industry and the expanding mariculture activities. Clinically, infestation by the parasite is termed “white spot’ disease due to the clear white spots caused by the colonisation of the parasite on the skin. Corneal opacity is another clinical manifestation induced by the marine ‘ich’. Heavy infestation of the gill epithelium leading to respiratory stress and failure could be the major cause of mass mortalities in cultured fish.

Parasitic Protozoans 13

Figure 1. Marine “itch” in adult cultured sobaity (Cryptocaryon irritans). Note the different stages of the parasite life cycle.

Scuticociliatosis

Another group of holotrichous ciliates is the scuticociliatida that has been reported from a variety fish species causing mild to very severe infestations. Tuna, flat fish, silver pomfret, seahorse, goatfish etc., have been known to be affected by the opportunistic bacterivore ciliate. The hymenostomatid protozoan infestations have been reported by many researchers world over [11, 12]. In 1980, nine species of saltwater aquarium fish suffered mortalities due to Uronema marinum [11]. Cultured striped trumpeter (Latris lineata) and southern bluefin tuna (Thunnus maccoyii) suffered from myositis and encephalitis, respectively due to Uronema sp [13, 14]. Mortalities of fish due to scuticociliatosis have been recorded from a variety of fish species such as the olive flounder Paralichthys olivaceus [15,16,17], turbot Scophthalmus maximus [18,19,20], seabass Dicentrarchus labrax [21], southern bluefin tuna Thunnus maccoyii [5], American lobster Homarus americanus [22], blue crab Callinectes sapidus [23] and seahorse Hippocampus erectus [24]. Preliminary observations on the 14 I. S. Azad and Ahmed Al-Marzouk diseases of cultured silver pomfret were reported in 2004 from Kuwait [25] and later, in 2007, a detailed investigation on scuticociliate-associated mortality of silver pomfret (Figure 2) was

reported [6].

Figure 2. Scuticociliatosis due to Uronema spp. in silver pomfret (2a) and seahorse (3) noticed in cultured fish and aquarium exhibit, respectively.

Earliest detection of the parasite and separation of normal fish in a group from the affected group was found to be more successful compared to the combination of treatments such as daily formalin bath [6]. The affected fish were found to become more serious sources of infection and the ciliate was more virulent after it leaves an infected fish as evidences through the reduced protease activity of the parasite when repeatedly cultured in vitro on bacteriological medium compared to a live challenge [26]. The parasite was found to invade almost all the organs including the brain, making it almost impossible to control the disease spread once it becomes serious. The marine aquarium exhibit fish and sea horses in the Scientific Centre, Salmiya of Kuwait were also found to be severely affected by the scuticociliate during the summer months of April during 2005. The infested sea horse showed lethargy, rubbing behaviour and bleached tail (Figure 3). Though, bath treatment with formalin, copper sulphate, hydrogen peroxide and even freshwater has been recommended, vaccination could provide a more effective and long-lasting solution to this major parasitic disease.

Amyloodinium (Marine Velvet Disease)

The marine velvet disease is caused by the dianoflagellate, Amyloodinium ocellatum. It’s an ectoparasite found on skin and gills and causes severe mortalities in cultured and aquarium fish [27]. The ‘velvet-like’ appearance is characteristic of the parasite infestation. Other clinical signs include anorexia, irritability and splashing behavior. Histopathological lesions Parasitic Protozoans 15 include gill inflammation, haemorrhages and hyperplasty. Elevation of temperature is frequently associated with mortalities due to severe infections in mariculture and sea aquaria. The life cycle starts with the infective stage (dinospore) that attaches to the host, transforming into a feeding (trophont) stage. The grown trophont detaches from the host cell, falls off and enters the reproductive (tomont) stage producing dinospores. Thousands of feeding stages develop fast on the infected fish gill leading to asphyxiation and morality (Figure 4). Edward Noga’s laboratory has been working extensively on this species and other parasitic protozoans and the team has demonstrated in 1981 that A.oscellatum can be propagated on fish hosts such as clown fish (Amphiprion oscellaris). They also showed that the parasite can be acclimatized and propagated on fish gill cell lines [28,29]. Histone like proteins, in the mucus of trout and hybrid bass infected with the flagellate, were noticed and these proteins showed a clear anti-Amyloodinium characters indicating that non-specific immune responses are elicited by the host due to infection by the flagellate [30].

Figure 4. Flagellate infestation by Amyloodinium spp. in cultured sobaity (Sparidenatx hasta) in Kuwait. 16 I. S. Azad and Ahmed Al-Marzouk

These parasites are of immense importance from the health management point of view especially in the backdrop of expanding aquaculture activities in the coastal environments. Prophylactic and therapeutic health management measures need to be developed in such a way that the longer interests of the host and the environment have to be given equal priority. In this context, immune modulation using immunostimulation and vaccination strategies need to be intensified to meet the challenges of diseases.

ACKNOWLEDGMENTS

The authors are thankful to Dr. Sulaiman Almatar, DM/MFD, KISR, Dr. Khalid Abdul Al-Elah for their help and cooperation.

REFERENCES

[1] Rasheed, V. (1989a). Vibriosis outbreaks among cultured seabream Acanthopagrus cuvieri broodstock in Kuwait. Aquaculture 76,189-197. [2] Rasheed, V. (1989b). Diseases of cultured brown-spotted grouper Epinephelus tauvina and silvery black porgy Acanthopagrus cuiveri in Kuwait. J. Aquat. Anim. Health. 1,102-107. [3] Bunkley-Williams, Lucy and Ernest H. Williams, Jr. (1994). Disease caused by Trichodina spheroidesi and Cryptocaryon irritans (Ciliophora) in wild coral reef fishes" J. Aqua. Anim. Health 6,360-361. [4] Diggles B.K. and Lester R.J.G. (1996). Infections of Cryptocaryon irritans on wild fish from southeast Queensland, Australia. Dis. Aquat Org 25,159–167. [5] Munday, B.L., O’Donoghue, P.J., Watts, M., Rough. K.andHawkesford, T.( 1997). Fatal encephalitis due to the scuticociliates Uronema nigricans in sea-caged southern bluefin tuna Thunnus maccoyii. Dis. Aquat. Org. 30: 17-25. [6] Azad, I.S., Al-Marzouk, A., James, C.M., Almatar, S.and Al-Gharabally,H. (2007). Scuticociliatosis-associated mortalities and histopathology of natural infection in cultured silver pomfret (Pampus argenteus Euphrasen) in Kuwait. Aquaculture, 262, 202-210. [7] Colorni, A and Burgess. P. (1997). Cryptocaryon irritans Brown 1951, the cause of 'white spot disease' in marine fish: an update. Aquarium Sciences and Conservation 1,217-238. [8] Yoshinaga,T.and Nakazoe,J. (1997) Effects of light and rotation culture on the in vitro growth of ciliate causing the scuticociliatosis of Japanese flounder. Fish Pathol 32,227– 228. [9] Hirazawa, N., Oshima, S.I., Hara, T., Mitsuboshi, T and Hata, K (2001). Antiparasitic effect of medium-chain fatty acids against the ciliate Cryptocaryon irritans infestation in the red sea bream Pagrus major. Aquaculture 198,219–228. [10] Matthews, B.F., Matthews, R.A. and Burgess, P.J. (1993). Cryptocaryon irritans Brown, 1951 (Ichthyophthiriidae): the ultrastructure of the somatic cortex throughout the life cycle. J. Fish Dis. 16,339–349. Parasitic Protozoans 17

[11] Cheung, P.J., Nigrelli, R.F., Ruggieri, G.D.( 1980). Studies on the morphology of Uronema marinum Dujardin (Ciliatea: Uronematidae) with description of histopathology of the infection in marine fishes. J. Fish Dis. 3, 295-303. [12] Bassleer, G.( 1983). Uronema marinum, a new and common parasite on tropical saltwater fishes. Fresw. Mar. Aquarium. 6, 78-81. [13] Langdon, J.S. (1992). Pathology of fish skin, gills, heart and musculoskeletal system. In: Fin Fish Workshop, University of Sydney Post Graduate Committee in Veterinary Science, Proceedings. 182, 111-130. [14] Watts, M., Burke, C.M.and Munday, B.L. (1996). The development of fluorescent antibody stain to identify Uronema sp. (Ciliophora: Scuticociliata). Bull. Eur. Assn. Fish Pathol. 16,104-108. [15] Yoshinaga (1993). Isolation and in vitro cultivation of an unidentified ciliate causing scuticociliatosis in Japanese flounder (Paralichthys olivaceus). Gyobyo Kenkyu 28,131- 134. [16] Jee, B.Y., Kim, Y.C.and Park, M.S. (2001). Morphology and biology of parasite responsible for scuticociliatosis of cultured olive flounder Paralichthys olivaceus. Dis. Aquat. Org. 47, 49-55. [17] Kwon, S.R., Kim, C.S. and Kim, K.H. (2003). Differences between short and long term cultures of Uronema marinum (Ciliophora: Scuticociliatida) in chemiluminescence inhibitory activity, antioxidative enzyme and protease activity. Aquaculture 221, 107- 114. [18] Dyková, I.and Figueras, A.( 1994). Histopathological changes in turbot Scophthalmus maximus due to histophagus ciliate. Dis Aquat Org. 18, 5-9. [19] Sterud, E., Hansen, MK.and Mo, T.A.(2000). Systemic infection with Uronema-like ciliates in farmed turbot Scophthalmus maximus (L). J. Fish Dis. 23, 33-37. [20] Iglesias, R., Paramá, A., Alvarez, MF., Leiro, J., Fernández, J.and Sanmartin, M.L.(2001). Philasterides dicentrarchi (Ciliophora, Scuticociliatida) as causative agent of scuticociliatosis in farmed turbot Scophthalmus maximus in Galicia (NW Spain). Dis. Aquat. Org. 46, 47-55. [21] Dragesco, A., Drajgesco, J., Coste, F., Gasc, C., Romestand, B., Raymon, J.andBouix,G.(1995). Philasterides dicentrarchi, n. sp. (Ciliophora, Scuticociliatida), a histophagous opportunistic parasite of Dicentrarchus labrax (Linnaeus 1758), a reared marine fish. Eur. J. Parasitol. 31, 327-340. [22] Cawthorn, R.J., Lynn, D.H., Despres, B., MacMillan, R., Maloney, R., Loughlin, M.and Bayer, R.(1996).Description of Anophyoides haemophila n. sp. (Scuticociliatida: Orchitophryidae), a pathogen of American lobsters Homarus americanus. Dis. Aquat. Org. 24, 143-148. [23] Messick, G.A.andSmall, E.B. (1996). Mesanophrys chesapeakensis n. sp., a histopahagous ciliate in blue crab, Callinectes sapidus, and associated histopahtology. Invertebr. Biol. 115, 1-12. [24] Thompson, C.L.Jr.and Moewus, L. (1964). Miamiensis avidus n. g. n. s., a marine facultative parasite in the ciliate order Hymenostomatida. J. Protozool. 11, 378-381. [25] Al-Marzouk, A., Durumdez, R.and Al-Gharabally, H. (2004). Efforts to control outbreaks of diseases among cultured silver pomfret Pampus argenteus in Kuwait. J. Aquacult. Trop. 19, 103-110. 18 I. S. Azad and Ahmed Al-Marzouk

[26] Ahmed Al-Marzouk and I.S. Azad. (2007). Growth kinetics, protease activity and histophagous digestibility of Uronema sp. infesting cultured silver pomfret (Pampus argenteus Euphrasen) in Kuwait. (Accepted for publication) Diseases of Aquatic Organisms. 76: 49-56. [27] Noga, E.J. andLevy, M.G. (1995). Dinoflagellate parasites of fish. In: Woo PTK (ed) Fish diseases. I: Protozoan and metazoan infections. CAB International, Oxford, p 1– 25. [28] Noga, E.J. (1987). Propagation in cell culture of the dinaoflagellate Amyloodinium, an ectoparasite of marine fishes. Science News Series, 236 (4806): 1302-1304. [29] Noga, E.J. (1989). Culture conditions affecting the in vitro propagation of Amyloodinium ocellatum. Dis. Aquat. Org. 6: 137–143. [30] Noga, E.J., Fan, Z. and Silphaduang, U.( 2001). Histone-like proteins from fish are lethal to the parasitic dinoflagellate Amyloodinium ocellatum. Parasitology 123: 57–65.

Chapter 3

STATUS OF AQUACULTURE HEALTH MANAGEMENT IN THE ISLAMIC REPUBLIC OF IRAN

Mehdi Soltani∗ Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran and Center of Excellence of Aquatic Animal Health, University of Tehran Tehran, Iran

ABSTRACT

Despite the rapid development of this industry during the recent years, it is faced with several constraints including lack of modern technology, insufficient financial resources, and negative impact of environmental pollution and occurrence of devastating infectious diseases. Poor environmental conditions, inappropriate health management strategies and outbreaks by some devastating infectious diseases such as white spot viral disease (WSD),infectious heamatopoeitic necrosis (IHN), infectious pancreatic necrosis (IPN) and streptococcosis/lactococcosis are the major constraints faced causing considerable losses each year. Although both veterinary and fishery organizations approved some rules and legislations to improve health management criteria, there is a risk of exotic and economically important diseases that can be imported through the importation of eyed-egg, larvae, brood stock and ornamental species into the country. However, some viral diseases including IHN, IPN and WSD have become a part of endemic diseases in the aquaculture sector.

INTRODUCTION

Iran commenced her aquaculture development processes from the early 1970's with the technical assistance from the former Soviet Union for the artificial propagation of sturgeon (Acipenseridae) fingerlings for restocking the Caspian Sea. Since then, the capacity to mass produce other species such Rutilus frisii kutum, Caspian trout (Salmo trutta caspius), bream (Abramis brama), pike-perch (Stizostedion lucioperca), rainbow trout (Oncorhynchus mykiss)

∗ Email address: [email protected] (Mehdi Soltani, DVM, PhD, professor of aquatic animal health). 20 Mehdi Soltani and four cyprinids species for restocking other suitable inland water bodies was rapidly acquired by the Iranian Fishery Organization (Shilat). Aquaculture has since expanded to culture of food fish in raceways (trout) and ponds (cyprinids). Other species such as Hamor and Barbus sharpeyi are also being targeted for future culture. Development projects on the farming of penaeid shrimp (Feneropeneaus semisulcatus and F. indicus) in the Persian Gulf region and along the southeastern area of the Caspian Sea are currently underway. Iran has also initiated projects to evaluate the feasibility of culturing Artemia cyst, grouper, pearl oyster, and aquatic plants. Also, for a sustainable aquaculture new species of fish and shrimp such as tilapia, sea bass and F. vannamei have been imported inside the country. Although aquaculture sector has been rapidly developed during the recent years in Iran, it has been faced with several problems including outbreaks by some economically important contagious diseases, use of insufficient technology, inadequate financial resources and negative impact of environmental pollution. Diseases and poor health management are one of the major bottlenecks for the development of the aquaculture sector worldwide including Iran. Trans-boundary movement of live aquatic animals in the region is one of the principal reasons for increased occurrence and spread of several serious diseases inside the country. Examples of diseases and pathogens introduced to new areas and hosts leading to serious consequences in Iran region include WSD, IHN, IPN, and viral encephalopathy and retinopathy also called viral nervous necrosis (VNN). Continued mass mortalities of common carp, silver carp and grass carp in the north and southwest parts of country since last decade, and recent detection of spring viremia (SVC) and koi herpesvirus (KHV) are sad reminders of the dangers associated with trans-boundary spread of pathogens. Careful examination of the history and spread of these diseases in Iran indicate how irresponsible or ill-considered movements of live animals can impact Iranian aquaculture and wild fisheries resources. Sound health management protocols incorporating principles of biosecurity, at the pond, farm, national, and regional levels, is increasingly becoming crucial for ensuring successful and sustainable aquaculture. Some of the most serious problems faced by the aquaculture sector in Iran are mainly those pathogens and diseases introduced and spread through movements of hatchery produced stocks, new species for aquaculture, and the ornamental fish trade.

The aim of this paper was to review the health status of aquaculture industry in Iran.

HEALTH MANAGEMENT OF AQUACULTURE SECTOR IN IRAN

Coldwater Fish Farming

Infectious hematopoeitic necrosis (IHN) was first identified as one of the main causative agents of fry trout mortality syndrome in rainbow trout farming in 2002 (Figures 1 and 2). Further serological and molecular studies of geographical distribution of the disease outbreaks shows that almost all major trout producing are infected. Molecular and serological studies have been also confirmed the occurrence of infectious pancreatic necrosis (IPN) in a number of farmed trout. Annual losses due to both IHN and IPN is estimated about 3 million US dollars in trout hatcheries. Although, the incidences by spring viremia of carp (SVC) and Status of Aquaculture Health Management in the Islamic Republic of Iran 21 viral hemorrhagic septicemia (VHS) are suspected in trout farming, more works are required to clarify these important viral diseases in Iran aquaculture.

Figure 1. Cytopatic effect of IHNVon third passage on EPC. (Photo by R. Falahi).

Figure 2. Electron micrograph of IHNV in pelleted materials of EPC cells showing bullet shaped viral particles (×32000) (Photo by Dr R. Falahi).

At the moment Lacotococcus garveiae and Streptococcus iniae outbreaks are one of main bacterial diseases in farmed rainbow trout in different parts of Iran where the trout farms are located. The first reports of disease outbreak in Iran appeared during 2000-2001. Later on S. iniae was identified as the cause of some mass mortality in Fars, Mazandaran, Charmah-va- bakhteyri and Kohgiloyeh-va-Boyerahmad regions. Further studies showed that besides the S. iniae, L. garvieae also plays a serious role in disease outbreaks in farmed trout in different parst of the country including Lorstan, Mazandaran, Charmah-va-bakhteyri, Fars, Kohgiloyeh-va-Boyerahmad, Kermanshoh and Kordestan. Data obtained on the clinical observations as well as traditional and molecular bacteriology provides adequate information on the epizootiology of disease zoonotic bacterial disease in trout aquaculture in Iran. Clinically, in most cases the affected farms show a chronic to subacute disease and the most diseased fish showed bilateral exophthalmia together with cataract and in some cases a complete loss of the eyes. Sluggish in movement, darkening of body, mild abdominal 22 Mehdi Soltani distention, prolaps of anal area, hemorrhage in the intestine and accumulation of bloody fluid in the abdominal cavity are also clinically observable signs (Figures 3 and 4). Total mortality is varied from 5 to 70%. The peak of outbreaks occurred during late spring till late summer when water temperature is increased. In most cases the affected fish are in the fattening/marketing sizes >100g. Total annual loss due to the disease outbreak is estimated 15 million US dollars. The results of epizootiological studies have shown that several parameters can act as the predisposing factors including high water temperature above 15 ºC overcrowding, overfeeding and over handling of the affected farmed fish. Also, poor biosecurity such as contaminations of the water sources at the up-stream of rivers and poor quarantine conditions can accelerate the disease outbreak inside the country. Recent molecular epidemiology of diseased farms of seven provinces with major trout production during 2008 till 2009 resulted in identification of 59.2% outbreaks by S. iniae and 40.8% by L. garvieae. Regional distribution of disease outbreak showed that the highest and lowest infected trout farms were Mazandaran (33.3%) and Kermanshah (1.9%) regions, respectively. In addition to, the regional distribution of infection by S. iniae shows that trout farming in Mazandaran (29.7%) and Fars (25%) states were more affected than other examined states. Furthermore, infection by L. garvieae was higher in Mazandran (39%) and Lorestan (25%) regions than other studied states, while no infection by L. garvieae was detected in Gilan region. Phylogenetic analysis of the S. iniae isolates resulted in a maximum similarity to some strains reported from Taiwan and all Brazilian strains and, one strain showed had high similarity with ATCC 29178 strain, all reported Chinese and some Taiwanian strains. Also, analysis of S. iniae LctO gene sequence showed that this isolate clustered within the S. iniae group. The sequence analysis of L. garvieae strains also showed that they have maximum similarity to all Japanese and Chinese strains, but one strain has lower sequence similarity values with all other recorded strains. The results of this study clearly show that trout farming in Iran is severely affected by both species of S. iniae and L. garvieae and therefore required serious preventive criteria. Also, genetic diversity of 44 strains of L. garvieae recovered from mortality of farmed trout in different provinces of the country were studied using random amplified polymorphic DNA (RAPD) analysis, and four profile patterns consisting of 560- 1330 bp in 5 bands, 56--1260bp in 5 bands, 560-1260bp in 4 bands and 560-1200bp in 5 bands were obtained. The phylogenetic tree of the RAPD product using UPMGA software included these strains in three different clusters with four different genetic groups. The results of this study clearly showed that L. garvieae strains from the diseased rainbow trout in the north part of Iran are geneticly different from those in the west part of country, although there is some genetic similarity between some strains of these two regions of Iran. A local polyvalent vaccine to both isolates of S. iniae and L. garvieae has been commercially produced with a satisfactory efficacy. Also, infections by Cytophaga/Flexibacter like-bacteria was occurred in farmed rainbow trout of different size causing saddle back lesions and a mortality up to 16%. The epizootiological studies of such outbreaks shows that unsuitable long transportation, poor water quality, long exposure to the sunlight and nutritional deficiency particularly vitamin deficiency are probably the main predisposing factors involved in the occurring of infections by Gram negative filamentous bacteria.

Status of Aquaculture Health Management in the Islamic Republic of Iran 23

Figure 3. Typical bilateral exophthalmia caused by L. garvieae in fattening rainbow trout in a fish farm in north Tehran province (Photo by Dr Mehdi Soltani).

Figure 4. Hemorrhage of intestine of a diseased rainbow trout affected by L. garvieae (Photo by Dr Mehdi Soltani).

The first outbreak of yersiniosis with a total mortality of 10-20% was reported in some farmed rainbow trout in Iran during summer 1997 and 2000. The disease outbreaks can become a serious problem mainly in those trout farmings that use the rivers as their water sources. In addition, infection by Ichthiophtirius multifiliis is sometimes an obstacle in trout recirculation biofilteration systems. Infection by Saprolegnia genera is also the most important fungal infectious diseases currently occur in rainbow trout, sturgeon and cyprinids hatcheries. The losses due to saprolegniosis in trout hatcheries is more than other species because of low water temperature and longer period of hatching period required for rainbow trout. In trout culture, an increase in levels of unionized ammonia, trite, carbon dioxide, low dissolved oxygen, high level of total suspended/dissolved solids and high fluctuation in water temperature are the main environmental problems encountered the industry. Such water quality parameters are more serious in trout recirculation systems.

Warm Water Fish Farming

Infection caused by Flavobacterium psychrophilum-like bacteria has been frequently reported from silver carp farming during the winter seasons in south country. Also, for many 24 Mehdi Soltani years the cyprinid farming including grass carp and silver carp are suffering from significant morbidity and mortality when water temperature increased. Various etiological agents including motile Aeromonas bacteria, Aeromonas hydrophila and Aeromonas veronii, a reoviral like virus and poor water quality conditions have been so far discriminated as the main cause of such losses. Also, recent surveillance for detection of SVC and koi herpesvirus (KHV) resulted in a few positive cases by polymerase chain reaction test in a couple of carp farms in southwest country and therefore, required further attention. Many protozoans and metazoans have been reported from different species of fish including both wild and cultured fish by several workers. Among them infections by Ichthiophtirius multifiliis, Trichodina sp., Diplostomum spataceum, Dactylogyrus sp., Lernea sp. and Botirocephalus sp. are the more economically important parasitic infections currently occurs in the farmed cyprinid industry.

Sturgeon Farming

Despite the value of sturgeon species as a part of aquaculture activity in Iran minimum data are available on the health status particularly infectious diseases of these valuable species both in wild and cultured conditions. The most available data has been focused on the identification of the external and internal parasites in these species. Cucullanus sphaerocephalus, Skrjabinopsolus semiarmatus, Leptorhynchoides plagicephalus, Pseudotracheliastes stellatus, Diclybothrium armatum, Nitzschia storionis, Eustrongyluides excisus, Anisakis sp., Amphilina foliace and Corynosoma stroumosum .have been reported by various workers from different species of sturgeons including Persian sturgeon (Acipenser persicus) and great sturgeon (Huso huso). Motile Aeromonas, Edwardsiell sp., Ichthiophthirius multifiliis, Trichodina, monogenic trematods and Saprolegnia spp. are the main causative agents identified so far in sturgeon aquaculture. There is no information on the possible viral diseases in these fishes. Similar to trout and carp culture systems, an increase in levels of unionized ammonia, nitrite, carbon dioxide, low dissolved oxygen, high level of total suspended/dissolved solids and high fluctuation in water temperature are also the main environmental problems encountered the sturgeon industry.

Ornamental and Other Fish species

Despite the frequent importation of different species of ornamental fish from different regions including East Asia, minimum data are available on their health status. Infections by Edwardsiella tarda, Aeromonas hydrophila, Aeromonas veronii, Flavobactria, some protozoa and trematods such as I. multifiliis, Trichodina , Dactylogyrus and Gyrodactylus occur infrequently in some ornamental species such as Oscar, catfish, goldfish, guppy and goramy. Also, occasional outbreaks causing extensive ulcerative lesions on the skin of some species including gold fish have been observed in some parts of country such as Gilan province and the so far microbilogical works has shown in no bacterial or fungal isolation. Therefore, further studies are required to clarify the causative agents of such gold fish ulcerative disease particularly Koi herpes viral disease (Figure 5). Status of Aquaculture Health Management in the Islamic Republic of Iran 25

Figure 5. EUS-like lesiosns on the skin of gold fish in north Iran. No bacterial or fungal agents were recovered. ( photo by Dr Mehdi Soltani).

The first outbreak by nodavirus was seen in wild golden grey mullet (Liza auratus) in the Caspian Sea causing mass mortalities have been observed in the fish population in southern coastal sea since 2002. Clinical signs were neurological abnormalities such as erratic swimming behavior, spiral swimming, belly-up at rest and over inflation of the swim bladder. In histopathological works signs of necrosis and vacuolation of the brain, nervous opticus and retina were evident and cytopathic effect of nodavirus characterized by vacuolation was observed in SSN-1 cell line at 25ºC, 5 days after inoculation with the filtered supernatant of 4 the brain and eye of affected fish. The recovered virus from cell line exhibited 10 TCID50 per mL when titrated. Indirect immunoflorescent antibody test showed nodavirus antigens in retina and positive-CPE SSN-1 cells (Figures 6 and 7). Also, RT-PCR product of approximately 289 bp was amplified from the brain and retina of the collected samples including the SSN-1 positive samples. Therefore, with this isolation and characterization of nodavirus from golden grey mullet, the possible infection in other valuable species e.g. sturgeons of the Caspian Sea warranted more attention and research works.

Figure 6. Transmission electron micrograph of the section of eye tissue of the affected L. auratus showing nodavirus particles (25-30 nm in size) in retina (arrow) (mag. x 7650). 26 Mehdi Soltani

Figure 7. Indirect immunoflurecent antibody test showing nodaviral antigens in SSN1 Cell line 6 days post-inoculation (x 400).

Shrimp Farming

The first outbreaks of white spot viral disease causing a rapid and high mortality occurred in farmed Feneropeneaus indicus in Abadan region, south Iran during June till July 2002 causing remarkable losses. The second outbreak was also seen two years later in Busheher province. The third outbreak was seen in Chaabahar region, south Iran causing remarkable losses. Outbreaks by baculoviral agents such as Monodon baculovirus have been also occurred in shrimp farming in south country. However, the exact impact of such viral diseases in Iran shrimp industry remains unknown. The risk for the occurrence of other economically important shrimp viral diseases such as Tura viral disease, yellow head viral disease and infectious hypodermal and heamatopoeitc necrosis viral diseases in Iran shrimp farming is high because of probably low level of quarantine and inadequate inspection measurements. Also, vibriosis caused by Vibrio anguillarum, Vibrio harveyi, Vibrio alginolyticus and Vibrio parahemolyticus is infrequently involved in F. indicus, F. vannamei and F. semisulcatus in south Iran. Also, since the beginning of shrimp larviculture in Iran 1995 on the coast of the Persian Gulf in southern Iran, more than 30% of larval and post-larval shrimp (mainly at zoeal stages 1-3) eliminations have been attributed to the development of a red-pink color at the bottom of the rearing tanks. In particular, the province of Bushehr has been the most affected area. This phenomenon referred to as “the red spot syndrome accounts for up to 95% of shrimp mortality. Recent bacteriological and molecular studies resulted in isolation and characterization of high virulent of red-pink producing Pseudomonas strains..

Status of Aquaculture Health Management in the Islamic Republic of Iran 27

Nutritional and Environmental Health Problems

Several fish and shrimp feed plants have been established inside the country so far mostly by the private sector. However, still some of these plants are unable to produce the standard feed both in quality and quantity. For instance, the quality and quantity of protein, carbohydrate, lipid, mineral and other trace elements are quite variable from one factory to another. Therefore, use of such low level fish feed can cause some nutritional deficiency and an increasing in cost benefit for the fish/shrimp farmers. At present, deficiency by some vitamins such as ascorbic acid and pentatonic acid, low level of some essential amino acids such niacin, lysine and metionin, high level of lipid and low level of protein in the diets are most frequent nutritional deficiencies can be seen in trout farming. Use of some immunostimulators such glucans has been started in aquaculture industry particularly in both trout and shrimp farming. There are also some attempts to use some herbal plant essences Zataria multiflora as food additive to improve both growth performance and health condition in trout farming. The residuals of some antibiotics such as oxytetracycline (OTC), enrofloxacin (EN) and erythromycin (ET) are increasing in trout farming because of frequent usage of these chemotherapeutants in the industry. For instance, screening of 17 trout farming by high performance liquid chromatography resulted in detection of OTC (5.8%) (0.75 to 7.13 µg/g), EN (35%) (0.5- 0.73 µg/g) and ET (29.4%) (23.38 -181.38 µg/g). Although the obtained results showed that the residual of these antibiotics were in acceptable levels, the detection of ET and EN in 29-35% of fish farms requires a serious constant monitoring of antibiotic residuals in trout farming. Pollution of the aquaculture environment by chemical and toxic substances is a cause for growing concern in aquaculture industry in Iran. The immediate concern is human health and welfare, but the effect of pollution on aquatic organisms such as fish also has wide consequences on the ecosystem. Effects of pollutions on fish and water quality have been demonstrated in rainbow trout industry particularly in those fish farms with river as water sources. The main sources of pollution are industrial and domestic wastewaters such as waters from power stations, from desalinating facilities, treated and untreated waters from domestic and industrial factories, contaminated sludge, and runoff waters from industrial and agricultural activities. Several pesticides and herbicides such as organophosphate toxicants are used in the agriculture industry worldwide to control plant and animal pests including insecticides, fungicides, acaricides, herbicide and algaecides. The main source of pollution of water bodies with pesticides is the melt waters, rain waters and underground waters. Results of a number of studies showed that such toxic chemicals can affect fish health conditions at various levels including the fish immune system resulting in an increase in fish susceptibility to infectious disease. For instance the increasing pollution has caused a remarkable impact on aquatic species particularly sturgeons in the Caspian Sea and entering river waters which are the major aquaculture sources in north Iran.

Disease Control and Aquaculture Veterinary Medicine

Usually strategies that may be adapted to control fish and shellfish diseases, such as viral diseases, range from no action to test and slaughter. These may also include intermediate appropriate interventions for halting mortality. These include surveillance, therapy, and 28 Mehdi Soltani modification of physical /environmental conditions, alteration of production schemes, vector control, carrier elimination, quarantine and mass vaccination of target species which is under investigation. In Iran, because of a number of gaps in our current knowledge about the outbreaks of viral diseases in both fish and prawn farming, the use of one or a combination of some of these strategies is vital. At the moment because of no confirmation for devastating diseases, e.g. VHS, SVC, VNN and KHV in Iran aquaculture, the use of current surveillance on epizootiology of exotic diseases and quarantine legislation are critical.

Control of Exotic Disease Risks

The exotic viral disease risks exist in aquaculture species in Iran because of poor control measures in quarantine, husbandry management, and vaccination and chemotherapy activities. Husbandry measures should be based on recognition of a number of potential risk factors that help transmission and persistence of disease. e.g. the risk of importing diseases with the imported fish stock that may act as agents of IPN, IHN, VNN, VHS, herpesvirus and iridovirus carriers or vectors. Importation of aquatic animals and a particular ornamental fish species are the main risk factors for both farmed rainbow trout and cyprinids in Iran. Evaluation of brood stock health is also an important disease control measure. However, there are currently no particular available tests for brood stock of cyprinids, sturgeons and rainbow trout in Iran. Information on larval health is also critical and recently the veterinary organization has approved some rules and regulations to minimize the transmission of vectors, carriers and affected larval or brood stock inside the country.

Recommendations and Prospective

The main aquaculture activities planned to achieve the aquaculture goals in Iran are to: 1. develop individual and complex aquaculture of warm water species, 2. enhance the aquaculture management through the improving water quality criteria, feed quality etc 3. Employ new and modern technologies such as recirculation systems and cage culture, 4. Improve the integrated aquaculture to reduce the environmental pollutions, 5. Support sufficient financial resources 6. Improve the aquaculture marketing and 7. Improve the health management criteria. Although both veterinary and fishery organizations approved some roles and legislations to prevent outbreaks by contagious infectious diseases in Iran aquaculture, there is still a risk of exotic and economically important infectious diseases that can be imported through the importation of eyed-egg, larvae, brood stock and ornamental species into the country. This is because of: insufficient routine screening programs for disease detection, no adequate data collection from fish/shrimp farmers and no sufficient training/education plans for many fish/shrimp farmers to get more familiar with the impact of predisposing factors, eradication, quarantine and other aspects of health conditions in their farmed animals. Therefore, the use of current surveillance on epizootiology of contagious diseases and quarantine legislation are highly recommended.

Status of Aquaculture Health Management in the Islamic Republic of Iran 29

REFERENCES

Esmaeili, F., Soltani, M. and Sayari, M. (2001) Occurrence of Flavobacterium psychrophilum-like infection in silver carp (Hypophthalmychthy molitrix). Iranian Journal of Fisheries Sciences, 10(2),103-111. Fallahi, R.; Soltani, M.; Karegar, R.; Zorrieh Zahra, M.E.J.; Shchelkunov, I.; Hemmatzadeh, F.and Nouri,A. (2003). Isolation and identification of the IHNV-like agent from farmed Rainbow trout (Oncorhynchus mykiss) from Iran. Archives of Razi, 56: Gorogi, A. (1996) Identification of blood and intestinal parasites of Huso huso in southern part of the Caspian Sea. Iranian Journal of Fisheries Sciences, 4, 43-47. Hosseinzadeh, H. (2003) Status of aquaculture in Iran: Past, present and future. Aquaculture Fisheries Society Symposium,. By the American Fisheries Society, pp.9. Khoshbavar-Rostami, H.A., Soltani, M.and Hassan, H.M.D. (2004), Acute toxicity and some hematological and biochemical changes in giant sturgeon (Huso huso) exposed to diazinon. Bulletin of the European Association of Fish Pathologists, 24(2),92-99. Khoshbavar-Rostami, H.A., Soltani, M. and Hassan, H.M.D. (2006a). Some hematological and biochemical changes in blood serum of Beluga (Huso huso) after chronic exposure to diazinon, Iranian Journal of Fisheries Sciences, 5(2),53-66. Khoshbavar-Rostami, H.A., Soltani, M. and Hassan, H.M.D. (2006b) Immune response of great sturgeon (Huso huso) subjected to long –term exposure to Sublethal concentration of the organophosphate, diazinon. Aquaculture. 256,.88-94. Khoshbavar-Rostami, H.A., Soltani, M., Hassan,H.M.D. (2006c). Immune response of great sturgeon to Aeromonas hydrophila bacteria. Journal of Fish Biology, 70, 1931-1938. Rohani, K., Payghan, R. and Jehanshahi, A.A. (1996) Isolation of a Reovirus from grass carp in Khosestan province. Pajohesh va Sazandegi, 3, 104-105. Sattari, M. (1999) parasites of sturgeons from the southwest of the Caspian Sea. PhD dissertation, Faculty of Veterinary Medicine, University of Tehran, 280p (in Persian). Sattari, M, Mokhayer, B. and Shafii, S. (2006) Parasitic worms of Persian sturgeon (Acipenser persicus) from the southwest of the Caspian Sea. European Association of Fish Pathologists, 26, 131-136. Soltani, M. and Rostami, M. (1997) A Cytophag/Flexibacter like bacterium (CFLB) infection in farmed rainbow trout in north Iran. Journal of Veterinary Research (previously Journal of Faculty of Veterinary Medicine, University of Tehran), 52(3), 13-22. Soltani, M., Fadaii Fard and Mehrabi, M. (1999) First report of a yersiniosis-like infection in Iranian farmed rainbow trout. Bulletin of The European Association of Fish Pathologists, 19(4),173-177. Soltani, M., Sharifpour, I. and Ismaeili F. (1999) The effect of some environmental variables on the course of infection by Vibrio harveyi in white Indian shrimp (Penaeus indicus). Journal of Veterinary Research (previously Journal of Faculty of Veterinary Medicine, University of Tehran), 55(4), 9-13. Soltani, M. and Tarahomi, M. (2000) Pathogenicity of Yersinia ruckeri-like isolates recovered from farmed rainbow trout in Tehran province. In second Convention of Iranian Veterinary Clinics, Book of Abstracks, p.37. Soltani, M., Kakoolaki, Sh. and Kisami, M. (2000) Isolation and identification of dominant Vibrio species in farmed prawn of Heleh station, Busheher, Journal of Veterinary 30 Mehdi Soltani

Research (previously Journal of Faculty of Veterinary Medicine, University of Tehran), 55(2), 28-32. Soltani, M. and Ebrahimzadeh Mousavi, H.A. (2000) Isolation of Aeromonas hydrophila and Aeromonas veronii from the farmed grass carp (Ctenopharyngodon idella) mortality in Gilan and Tehran provinces. Iranian Journal of Veterinary Medicine (previous name: Journal of the School of Veterinary Medicine, Shahid Chamran University Ahwaz, 4, 24- 29. Soltani, M. and Kalbassi, M.R. (2001) Protection of Persian sturgeon (Acipenser persicus) fingerling against Aeromonas hydrophila septicemia using different agntigsn. Bulletin of European Association of Fish Pathologists, 21, 235-239. Soltani, M. (2003) The status of aquaculture health management in Iran. Aquaculture Europe 2003, Trondhim, Norway. Extended Abstracts and short communications, European Aquaculture Society, p.321-322. Soltani,M, Jamshidi Sh and Sharifpour, I (2005). Streptococcosis caused by Streptococcus iniae in farmed rainbow trout (Onchorhynchus mykiss) in Iran: Biophysical characteristics and pathogenesis, Bulletin of the European Association of Fish Pathologists, 25, 95-106. Soltni, M., Alishahi, M., Mirzargar, S. and Nikbakhat, GH. R. (2007) Vaccination of rainbow trotu against Streptococcus iniae infection: comparison of different routes of admistration and different vaccines. Iranian Journal of Fisheries Sciences, 7(1): 129- 140. Soltani, M. (2008) Lacotoccosis caused by Lacotococcusgarvieae in farmed rainbow trout (Onchorhyncus mykiss) in Iran. The 7th Symposium on Diseases in Asian Aquaculture, Taiwan, Book of Abstracts, p.163. Soltani, M. Nikbakht, Gh, Ebrahimzadeh Mousavi, H.A and Ahmadzadeh H. (2008) Epizootic outbreaks of lactococcosis caused by Lactococcus garvieae in farmed rainbow trout (Oncorhynchus mykiss) in Iran. Bulletin of the European Association of Fish Pathologists, 28(5),207-212. Soltani, M., (2010) Streptococcosis/ lactococcosis in rainbow trout (Oncorhynchus mykiss) aquaculture in Iran- what should I do? 2nd International conference of aquatic animal health and management, Tehran, Iran, pp.1-6 Soltani, M.; Ahmadi, M.R.;Yavari, H. and Mirzargar, S.S.(2010) Red-pink colony- producing Pseudomonas sp. is the causative agent of mass mortality in larvae and postlarvae of raised in hatcheries in south Iran Pseudomonas Litopenaeus vannamei International Journal of Veterinary Research, 4(2):89-94. Soltani, M., Ghasemi, M, Rohani, M., Sharifpour, I. and Zoriehzahra, J.E. (2010) Isolation and identification of betnodavirus causing mass mortalities in golden grey mullet (Liza auratus) in the Caspian Sea. International Journal of veterinary Research, 4(3):201- 208. Tokhmafashan, M,, Shariff, M. Hassan, and Wang, Y.G. (2004) Identification of Penaus monodon baculovirus (MBV) in cultured Penaus semisulcatus in Isamic Republic of Iran. Iranian Journal of Fisheries Sciences, (1), 25-32. Tokhmafashan, M., Akbari, S., Tamjidi, B., Laloi, F. and Soltani, M (2004) Occurrence of white spot syndrome disease in farmed Penaus indicus in Iran, Applied Fisheries and Aquaculture, IV (1), 42-47. In: Aquaculture in the Middle East and North Africa ISBN:978-1-61209-834-0 Editors: Azad Ismail Saheb and Salam Al-Ablani © 2012 Nova Science Publishers, Inc.

Chapter 4

DISEASES IN WILD AND CULTURED FISH IN TURKEY

Ercument Genc∗ Fish Diseases Lab., Faculty of Fisheries, Mustafa Kemal University, Iskenderun, Hatay, Turkey

ABSTRACT

In this chapter, the current status of major health problems in freshwater and marine aquacultures as well as in wild fishes in Anatolia/Turkey is examined. Information is presented as the form of agent-host list. The agent-host list is organized on a common systematic basis and provides information for each disease agents on various regions of Turkey. Occurrences of different health problems are increasing due to the intensive culture facilities and also negative changes in the environment including the global warming. Moreover, the statistical data warns us about the overfishing problem. This means that fish stocks are decreasing and also the number of threatened fish species is increasing day by day. This review summarizes information on the fish disease agents of Turkish fishes contained in the Turkish literature dating from the earliest available records to the end of 2010.

INTRODUCTION

The land of Turkey is a large and shaped as a rectangular peninsula. It is a bridge connecting the Middle East and Europe, and it shares the history and characteristics of both those distinct parts of the world. Turkey extends more than 1.600 kilometers from west to east and approximately less than 800 kilometers from north to south. Total land area is about 779.452 square kilometers, of which 755.688 square kilometers are in Asia and 23.764 square kilometers are in Europe. The European part of Turkey, known as the Thrace (Trakya), is separated from the Asian part of Turkey by the Bosporus Strait (Istanbul), the Sea of Marmara, and the Dardanelles Strait (Canakkale). The Asian part of the country is known by a variety of names like the Asia Minor, and the Anatolia (Anadolu) (Anonymous, 2005).

∗ E-mail: [email protected] 32 Ercument Genc

Turkey is surrounded by sea on three sides, the Black Sea in the north, the Mediterranean Sea in the south, and the Aegean Sea in the west. Utilizing this advantage, Turkey has been known as a country of fishery products since ancient times. Differences in terms of temperature, salt content etc. in these seas, provide fish and fishery products of different species and delicious tastes. Knowledge-based aquaculture in Turkey was started with rainbow trout in 1970s. Currently Aquaculture remains to be a popular and vital sector in Turkey (Deniz 2000, Deniz et al. 2000, Genc et al. 2003). Marine aquaculture in Turkey started with efforts to produce sea-bream in 1983. This was followed with sea-bass in 1987 and with salmon in 1989. The first commercial activity towards producing sea bream and sea bass was launched in 1985 with a hatchery in Izmir province (Sanli 2002). However, collecting wild larvae (in 1985 to 1993) for rearing in aquaculture environments harmed the natural stocks. As a consequence, the government set some criteria for commercially successful and sustainable aquaculture to better direct efforts to build the first modern hatchery in the Aegean part of Turkey. The total production of fishery products in Turkey was 772,000 tons in 2007. Fishery production decreased by 16.32% in 2008 with a total of 646,000 tons. Approximately 494,000 tons of this amount were reached by catching and 152,000 tons were produced by aquaculture. In 2008, production through catching decreased by 21.87%, while production through aquaculture increased by 8.8% with respect to the previous year (TURKSTAT 2009). As a result, more than $ 414 million was gained from the exports of this sector in 2008. Main export markets of Turkey are the European Union, the USA, and Japan. Major Turkish export products in this sector are fresh fish, followed by the fresh and canned crustaceans and mollusks. On the other hand, a great number of fish farms have arisen due to the recognition of large water resources and request of consumers demanding fishery products available to them throughout the year. The most common species produced by aquaculture are trout, sea bream, and sea bass. Fresh water fishing and fish farming has accelerated the progress in the sector. Turkey is already in a position to become the major trout supplier of EU countries and the USA (IGEME 2009).

DIAGNOSIS AND CONTROL MEASUREMENTS IN TURKISH FISHERIES AND AQUACULTURE

Recently, biologists, agri-aquaculture engineers and veterinerians have been studied on detection (prevalences, intensities, abundance, parasite-host relationships) (Moravec and Genc 2004, Genc et al. 2005a, b, Genc et al. 2006, Genc et al. 2007a, b, Oral and Genc 2008, Bozkurt and Genc 2009, Kalay et al. 2009, Konas et al. 2010, Bircan-Yildirim et al 2010a), diagnosis (heamatological, and molecular) (Ögüt 2001, Yavuzcan 2004, Şahan et al. 2007) and development of prevention technologies: chemoterapy, vaccines, immunostimulants (Ispir and Dörücü 2005) for fish diseases in Turkey. All activities in fisheries and aquaculture are governed by the fisheries law No:1380, enacted in 1971. Local authorities under the Ministry of Agriculture and Rural Affairs in 81 provinces are responsible for implementing fishing and aquatic animal health regulations. Additionally, all animal health control issues are regulated by the law of animal health control No: 3285, enacted in 1986. In accordance with the law, aquaculture health control circulars Diseases in Wild and Cultured Fish in Turkey 33 are published and announced annually in the official journal about the control for these diseases. Based on these laws, notifiable diseases are determined by the Animal Health Information Organization and approved by the Ministry (Table 1.).

Table 1. The notifiable diseases list for aquatic animals in Turkey

Aquatic animal Notifiable diseases Fish VHS IHN SVC BKD Shellfish Bonamiasis Marteliosis Crustacean Crayfish plaque disease

Diagnosis of presence of a disease is carried out by a laboratory accredited by the Ministry. The Bornova Veterinary Control and Research Institute (BVCRI) is responsible for diagnosis of aquatic animal diseases as the National Reference Laboratory (ISO 17025) in Turkey. Currently, Turkey follows the World Organization for Animal Health (OIE) principles regarding aquatic animal diseases and diagnostic methods. On the other hand, for the last 15 years Turkey has been trying to adapt EC rules and following most of EC regulations (91/67/EC, 93/53/EC, 95/70/EEC and 2001/183/EC) related on aquatic animal diseases and diagnostic methods. When fish on a farm are suspected of being infected with a list of diseases, official regulations are immediately applied to confirm the presence of disease, including clinical examination and taking samples necessary for laboratory examination. If a laboratory report confirms a disease in fish, an official veterinarian prepares a report for the Animal Health Control Commission which declares the outbreak. The commission passes an official decision about the outbreak in order to control and eradicate the disease. Then a cordon and quarantine can be set up by this commission (Ozyer 2008). Some important bacterial, viral, and parasitic agents that cause significant economic losses in cultured fishes such as sea bass (Dicentrachus labrax), sea bream (Sparus aurata), and rainbow trout (Oncorhynchus mykiss) are listed in Table 2. Pathogenic ciliates, flagellates, dinoflagellates, monogenean, digenean, cestoda, nematodes, crustacea, isopoda, copepoda and bivalvia groups from the wild and cultured aquatic animals in Turkish seas and inland waters were reported up to 1931 by Monod (1931). Early reviews on parasites of Turkish fishes were made by Oktener (2003) and Oktener et al. (2004). After these reviews, new parasites and hosts were reported (Kayis et al. 2009). This information is considered as a useful data for the aqaculturists and fish disease researchers in Turkey and also in the Middle East. On the parasitic disease agents Kayis et al. (2009) pointed out that protozoans can seriously affect cultured and wild fish populations. Moreover, Genc et al. (2005c) claimed that many parasite species, especially helminthes, possess complex life cycles involving trophic transmission from one host to the next by the consumption of infected intermediate hosts. Therefore, control of fish parasites requires knowledge of the parasites, their hosts, and their prevalence and also distribution (Mitchum, 1995). 34 Ercument Genc

Table 2. Cultured finfish diseases*

Diseases of cultured seabass and seabream Bacterial Vibriosis; Listonella anguillarum, V. alginolyticus Pasteurellosis; Pasteurella piscicida Photobacterium damsela subsp. piscidia Myxobacteriosis; Tenacibaculum maritimum Streptococcosis; Streptococcus iniae, S. uberis Motil aeromonas septicaemia; A. hydrophilia Winter diseases; Pseudomonas anguilliseptica Clamidiosis; Clamidia like organism Viral Lymphocystis is common in juvenile seabream IPNV was isolated from seabass VHSV was isolated from turbot in the Black Sea Nervous necrosis virus (VNN) symptoms were observed in seabass. However there is not yet identification report. Parasitic Cryptocaryon irritans, Isopoda sp., Trichodina sp., Dactylogyrus sp.,Gyrodactylus spp., Lernanthrophus sp., Caligus sp., Ichtyobodo necatrix,Microcotyle sp., Amyloodinium sp., Ceratomyxa sp., Myxosporodean, Eimeria sp. Diseases of Cultured rainbow trout Bacterial ERM; Yersinia ruckeri, Lactococcosis; L. garivieae, Motil aeromonas septicaemia; A. hydrophilia, Hitra diseases; V. salmonicidia, RTFS; Flavabacterium psychophlium; BKD (Host: Salmo trutta labrax) Renibacterium salmoninarum Viral IPN, VHS Parasitic Ichtyopthyrius multifilis, Trichodina sp., Gyrodactylus spp., Oodinium sp. *Modified from Ozyer (2008).

CONCLUSION

It is a great concern that the incidence of infectious diseases in aquaculture leads to significant economic losses and also causes problems in the ever developing sector in some parts of the world (Direkbusarakom et al. 1998) including Turkey and the Middle East region. This reality forced us to carry out collaborative studies on wild and cultured fish diseases and also growth promoters in aquaculture. Altinok and Kurt (2003) implied that under optimum conditions, even the fish looking healthy (without a clinical sign or lesion) can carry pathogens that create serious risks for the spread of contagious diseases in fish populations. Therefore, to detect pathogen carrier fish, a cost-effective, sensitive, and specific system such as a molecular diagnosis is required for surveillance and monitoring fish populations. Diseases in Wild and Cultured Fish in Turkey 35

Rapid growth and high disease resistance are two of the most important concerns in aquaculture production. In the last several decades, antibiotic growth promoters have been included in animal feeds worldwide at sub-therapeutic concentrations as a standard practice because of their positive effects on weight gain, feed utilization, and survival (Genc et al. 2007c, d). On the other hand, the use of antimicrobial agents in aquaculture has resulted in an increase of high resistant bacterial strains (Smith et al. 1994, Cabello, 2006). The use of synthetic antibiotics threats the consumer health, non-target organisms, and the environment (Muniruzzaman and Chowdhury 2004, Abutbul 2005). Moreover the main disadvantage of chemotherapotics is cost and the risk of higher residues should be encountered. One of the best prevention methods in aquaculture are good husbandry and appropriate vaccination (Cagirgan and Tanrikul 1998). The treatment of bacterial fish diseases with natural products might be a safe second option for the ecological/organic aquaculture. As a result, the prophylactic measurements should be considered. Hence, the global demand for safe food has prompted the search for natural food additives, new alternative profilaxy and treatments. Besides disease resistant (specific pathogen free) strains development, vaccine development, dietary supplements, including probiotics and prebiotics, such as mannan oligosaccharides (MOS) (Dugenci et al. 2003, Yilmaz et al. 2007, Mazlum et al. 2011) and other immunostimulants (beta glucans, yeast, ect.), have received heightened attention for producing healthy and safe fishes. Currently, many researchers focus their efforts on two new trends in fish health. One of them is eco-parasitology. This type studies discuss the recently described phenomenon of conspicuous metal accumulation by parasites and how this might be applied to environmental monitoring. They also suggest how environmental science and parasitology might profit from each other in the near future. Approximately 130–150 papers have been published since 1980 that are directly concerned with the relationship between pollution and parasitism, mainly in the aquatic environment (Suresh 2004, Genc et al. 2008, Dural et al. 2010a, b). Another research topic is welfare of fishes. Some researchers focus their efforts on fish welfare in aquaculture and fisheries (Kumlu and Yanar 1999, Yanar and Kumlu 2001, Yanar and Genc, 2004, Huntingford et al. 2006, Bircan-Yildirim et al. 2010b) in Turkey. The fish welfare can be explained as painless and stress-free state of being. Tsantilas et al. (2006) speculated that this term has been questioned by producers. Fishes need a stable environment of being so that they can survive, develop, and reproduce. The absence of such stability is termed as stress. There are various causes of producing stress (inadequate conditions of farming, high stocking-density, unbalanced food, unsuitable water quality, disease prevention and treatment methods, techniques of killing and transport). Thus, nowadays, fish welfare is actually regulated legally in several countries as well as in Turkey.

REFERENCES

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Genc, E., Genc, M.A., Genc, E., Cengizler, I. and Can, M.F. (2005c). Seasonal variation and pathology associated with helminthes infecting two serranids (teleostei) of Iskenderun Bay (north-east Mediterranean Sea), Turkey. Tr. J. Fisheries Aquatic Sci., 5, 29-33. Genc, E., Sahan, A., Altun, T. Cengizler, I. and Nevsat, E. (2005b). Occurrence of the swimbladder parasite Anguillicola crassus (Nematoda, Dracunculoidea) in European eels (Anguilla anguilla) in Ceyhan River, Turkey. Tr. J. Vet. Anim. Sci., 29, 661-663. Genc, E., Sangun, M.K., Dural, M., Can, M.F. and Altunhan, C. (2008). Element concentrations in the swimbladder parasite Anguillicola crassus (nematoda) and its host the European eel, Anguilla anguilla from Asi River (Hatay-Turkey). Environ. Monitor. Assess.141, 59-65. Genc, E., Sereflisan, M., Erol, C. and Kara, A. (2007b). Iskenderun Korfezi’ndeki Sarikuyruk (Seriola dumerili Risso, 1810) (Teleostei: Carangidae) Yetistiriciliginde, Kitlesel Olumlere Neden Olan Zeuxapta seriolae (Meserve, 1938) (Monogenea: Heteraxinidae) Olgusu. XIV. National Fisheries Semp., 04-07 September, Mugla, Turkey (In Turkish). http://www.akuademi.net/su/?XIV.SU.UR.SEMP.2007:Hastaliklar_2:hp07. Genc, E., Yıldirim, Y.B., Basusta, N. and Cekic, M. (2006). Seasonal variation of Hysterothylacium aduncum (Rudolphi, 1082) (Nematoda, Ascaridoidea, Anisakidae) infection in common guitarfish, Rhinobatos rhinobatos (Linné, 1758) (Chondrichthyes, Rhinobatidae) in Iskendeun Bay (North-easthern Mediterranean Sea) Turkey. Workshop on Mediterranean Cartilagınous Fish with Emphasis on Southern and Eastern Mediterranean. (Eds: Basusta, N., Keskin, C., Serena, F., Seret, B.) Turkish Marine Research Foundation, Istanbul, 23, 10-16. Genc, M.A., Aktas, M., Genc, E. and Yılmaz, E. (2007c). Effects of dietary mannan oligosaccharide on growth, body composition and hepatopancreas histology of Penaeus semisulcatus (De Haan 1844). Aquacult Nut. 13, 156-161. Genc, M.A., Tekelioglu, N. and Altun, A. (2003). Developments in marine aquaculture in Turkey. A Regional workshop on fisheries, aquaculture and environment. 29-30 April’03, Tishreen University, Lattakia, Syria. Genc, M.A., Yılmaz, E., Genc, E. and Aktas, M. (2007d). Effects of dietary mannan oligosaccharides (mos) on growth, body composition, and intestine and liver histology of the hybrid tilapia (Oreochromis niloticus x O. aureus). Isr J. Aquacult-Bamid., 59, 10-16. Huntingford, F. A., Adams, C., Braithwaite, V. A., Kadri, S., Pottinger, T. G., Sandøe P. andTurnbull, J. F. (2006). Current issues in fish welfare. J Fish Biol., 68, 332-372. IGEME 2009. Turkish Agriculture and Food Industry. Undersecretariat of The Prime Ministry For Foreign Trade, Export Promotion Center of Turkey. 7 pp. Ispir, Ü. and Dörücü, M. A. (2005). Study on the effects of levamisole on the immune system of rainbow trout (Oncorhynchus mykiss, Walbaum). Tr. J. Vet Anim Sci., 29, 1169-1176. Kalay, M. Dönmez, A.E., Koyuncu, C.E., Genc, E. and Şahin, G. (2009). Seasonal Variation of Hysterothylacium aduncum Infection in Sparid Fishes in the Northeast Mediterranean Sea. Tr. J. Vet .Anim Sci., 33, 517-523. Kayis, S., Ozcelep, T., Capkin, E. and Altinok, I. (2009). Protozoan and Metazoan Parasites of Cultured Fish in Turkey and their Applied Treatments. Isr J Aquacult – Bamid., 61, 93-102. Konas, E., Genc, E., Kaya, G. and Erol, C. (2010). Occurrence of Trypanosoma sp. in wild African sharptooth catfish (Clarias gariepinus Burchell, 1822) from Asi River (north- eastern Mediterranean), Turkey. Tr. J. Zool. 34, 271-273. 38 Ercument Genc

Kumlu, M. and Yanar, M. (1999). Effects of the anesthetic quinaldine sulphate and muscle relaxant diazepam on sea bream juveniles (Sparus aurata). Isr J. Aquacult-Bamid, 51, 143-147. Mazlum, Y., Yilmaz, E., Genc, M.A. and Guner, O. (2011). A preliminary study on the use of mannan oligosaccharides (MOS) in freshwater crayfish, Astacus leptodactylus Eschscholtz, 1823 juvenile diets. Aquacult Int., DOI 10.1007/s10499-010-9345-4. Mitchum D.L. (1995). Parasites of Fishes in Wyoming. Wyoming Game and Fish Dept., Wyoming. 43pp. Monod, T. (1931) Crustaces de Syrie. In: A Gruvel, Les etats de Syrie. Bibliographie Faunae Française, 3, 397–435. Moravec, F. and Genc, E. (2004). Redescription of three Philometra spp. (Nematoda: Philometridae) from the gonads of marine perciform fishes of Iskenderun Bay (North- East Mediterranean), Turkey. Acta Prasitologica, 49, 31-40. Muniruzzaman, M. and Chowdhury, M.B.R. 2004. Sensitivity of fish pathogenic bacteria to various medicinal herbs. Bangladesh J. Vet Med., 2, 75-82. Ögüt, H. (2001). Modeling of fish disease dynamics: A new approach to an old problem. Tr. J. Fish Aquat Sci., 1:67-74. Oktener A. (2003). A checklist of metazoan parasites recorded in freshwater fish from Turkey. Zootaxa, 394,1-28. Oktener A., Yalcin M. and Kocyigit, E. (2004). Turkiye’deki baliklarda kaydedilen protozoan parazitler. Anadolu Univ. J. Sci. Technol., (in Turkish) 5, 297-305. Oral, M. and Genc, E. (2008). Re-evaluation of parasitism in Dusky Grouper (Ephinephelus marginatus Lowe 1834) in Iskenderun Bay, Turkey using Self Organizing Map (SOM). J FisheriesSciences.com. 2, 293-300. Ozyer, B.O. (2008). Legislation and health situation in aquaculture in Turkey. Ittiopatologia, 5, 236-238. Şahan, A., Altun, T., Çevik, F., Cengizler, İ., Nevşat, E. and Genc, E. (2007). Comparative study of some haematological parameters in European eel (Anguilla anguilla L., 1758) caught from different regions of Ceyhan River (Adana, Turkey). E.U. J. Fish Aquat Sci., 24, 167-171. Sanli, M. (2002). Environmental impacts of fish farms. M.Sc. Thesis, Environmental Sciences Program, Graduate School of Natural and Applied Sciences of Dokuz Eylül University. Izmir, Turkey. Smith, P., Hiney, M.P. and Samuelsen, O.B. (1994). Bacterial resistance to antimicrobial agents used in fish farming: A critical evaluation of method and meaning. Annu Rev Fish Dis. 4, 273-313. Sures, B. (2004). Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends Parasitol., 20, 170-177. Tsantilas, H., Athanassopoulou, F., Galatos, A.D. and Bitchava, K. (2006). Welfare of fish. J. Hellenic Vet. Med. Soci., 57, 140-148. TURKSTAT 2009. Fisheriy 2008. Turkish Statistical Istitude Prime Ministry Republic of Turkey. Press Pelease No: 125, 16 July 2009. URL: http://www.turkstat.gov.tr/ PreTablo.do?tb_id=47andust_id=13. Yanar, M. and Kumlu, M. (2001). The anaesthetics effects of quinaldine sulphate and/or diazepam on sea bass (Dicentrarchus labrax) juveniles. Tr. J. Vet. Anim. Sci., 25, 184- 189. Diseases in Wild and Cultured Fish in Turkey 39

Yanar, M., and Genc, E. (2004).Anaesthetic effects of quinaldine sulphate together with the use of diazepam on Oreochromis niloticus L. 1758 (Cichlidae) at different temperatures. Tr. J. Vet. Anim Sci., 28, 1001-1005. Yavuzcan, H. Y. 2004. An Overwiev of vaccine and immunostimulant use in Turkish aquaculture sector. 6th International Symposium on Fish Immunology, 24-29, May, Turku, Finland. Yilmaz, E., Genc, M.A. and Genc, E. (2007). Effects of dietary mannan oligosaccaharides (mos) on growth, body composition, intestine and liver histology of rainbow trout, Onchoryncus mykiss (Walbaum), Isr. J. Aquacult-Bamid., 59,183-189.

Chapter 5

PRINCIPLE FISH PATHOGENS IN TUNISIAN AQUACULTURE

Cherif Nadia1 and Hammami Salah2

ABSTRACT

This chapter takes note of the problems encountered by the Tunsian aquaculture sector due to the rapid extension of the rearing activity in some Tunisian regions, particularly in the fi1eld of pathology. This specialized database specifically describes some of the viral, bacterial and parasitic disease-related information and focuses on available data of these pathogens which have either devastating effects on fish production in terms of high mortalities, or reduction in growth of farmed fish. Focusing on studies related to diagnostic technique improving, the record provided the opportunity to have comprehensive information on the isolated and identified microorganisms.

INTRODUCTION

Mediterranean finfish farming has been dominated by the culture of sea bass (Dicentrarchus labrax, Moronidae) and gilthead sea bream (Sparus aurata, Sparidae) (Rigos and Katharios, 2009). Africa contributes with 5.54 million MT (4.5%) to the world harvest of aquatic organisms (Ababouch, 2000). Fisheries represent a vital sector for many countries in Africa, for domestic food supply, employment opportunities and foreign exchange earnings. Despite the low level of African fish production and export in comparison with the other continents, fish represent the major protein source in many countries (36-58% of animal proteins in Cote d'Ivoire, Congo, Senegal, Angola), in addition, fishing is a vital activity for Senegal, Mauritania, Morocco, Ghana, Tunisia and other countries (Ababouch, 2000). Tunisia occupies a central place in the Mediterranean Sea and disposes approximately 1 300 km of littoral length, in addition to 7 lagoons, covering a total surface of 105 200 ha and

1 Veterianry Research Institute of Tunisia. 20 Rue de Jebel Lakdhar. La Rabta. 1006 Tunisia 2 National Center of Zoosanitary surveillence. Charles Nicolle Avenue,Belvédère. Tunis* 42 Cherif Nadia and Hammami Salah an exceptional continental shelf of a few 88 000 Km2. This geographic distribution of the Tunisian waters, as well as their varieties, resulted in the development of rich ecosystems. Furthermore, Tunisia has 41 maritime fishing ports including 10 large ports permitting the shelter of the trawlers, the tuna boats, the light fishing boats and the units of inshore fishing. The fishing sector, with its annual production of 100 thousand tons in 2008, is placed at the second position within the agriculture product exportation after the olive oil. Regarded as a strategic activity that can support the fishing sector, aquaculture benefits in Tunisia of a particular interest. Wright now, few private farms are producing fish aquaculture (mainly Sea bass and Sea bream). Additional farms are working on blue fin tuna fattening since 2003. Private projects assuring the production of clams, mussels and cupped oysters have been also initialized. Actually thirty four dams are in exploitation in the North and the middle of Tunisia. The dam’s water contains the following species: Mullet, Pike perch, Carp, Barbell, catfish and Black-bass. In addition to this activity, 3 Chinese carp species (Silver carp, Bighead carp and grass carp) are bred in a Technical Aquaculture Center. In addition to the technical and economic parameters which are very important to control for the promotion of aquaculture, market investigations require specific norms of competitiveness, which has urged authorities to establish a global and coherent strategy for the development of the sector. Towards this end, Tunisia realized the Master Plan for Aquaculture, carrying out ambitious objectives and directly involving the whole staff. The open design of many aquaculture systems allows the transmission of infectious pathogens from the environment or wild fish into aquaculture animals. In addition, the greatest risk for the spread of diseases lies with the careless, cross-boundary movement of living animals or fry destined directly for aquaculture facilities. All the trans-located animals would have had the potential to carry pathogens. Disease interaction between farmed and wild populations is fundamental to disease emergence and it is believed that diseases in farmed populations have their origin in wild populations of the same or similar species (Hastein and Lindstad 1991; Amos and Thomas 2002; Olivier 2002). The most ominous would be viral and parasitic diseases (Flegel T.W., 2006).

VIRAL DISEASES

The presence of viruses in lower vertebrates proved to be of veterinary and public interest, especially RNA viruses causing severe diseases in fish aquaculture which became worldwide of economical importance. Some DNA viruses induce diseases resulting in important economic losses in fish farms. During the last 20 years, understanding of the virology of the lower vertebrates has been substantially improved and viral diseases are considered to be of socio-economic and/or public health importance within countries, and significant to the international trade in aquatic animals and aquatic animal products. Of special mention are the Nodaviruses of marine fish which represent a potential threat of the expanding industry in Tunisia. Viral encephalopathy and retinopathy (VER), a disease caused by infection with a betanodavirus, occurs mainly in larval and juvenile marine finfish in more than 30 species worldwide (Gagne et al., 2004). It is a particular problem where stocking density is high and has caused severe losses in hatcheries. At least one species of betanodavirus, Red Spotted Grouper Nervous necrosis Virus occurs in Tunisia (Cherif et al., Principle Fish Pathogens in Tunisian Aquaculture 43

2009). Sea bream has been initially reported as an asymptomatic carrier of the disease (Castric et al., 2001). However, it has been shown that sea bream can be experimentally susceptible to nodavirus, depending upon the temperature and route of infection (Aranguren et al., 2002). Also, sea bream is often cultured in the Mediterranean in the vicinity of sea bass and other susceptible species, raising the possibility of cross infection. The spread of viral nervous necrosis (VNN) might be attributed to either vertical or horizontal transmission. While these viruses have apparently spread within the natural ranges of affected species as a result of commerce, VER has also been reported in these species in countries where they do not naturally occur and to which they have been exported. In Tunisia, the main cultured species involved has been Dicentrarchus labrax, which suffers mass mortality of larval and juvenile fish. Moreover, no VER symptoms were observed in sea bream species Sparus aurata reared next to sea bass tanks displaying disease signs. However, using RT-PCR and IFAT, Nodavirus was isolated from the above species (Chérif et al., 2009). The control of the disease in based on the virus detection in infected animals. Molecular techniques, particularly, the recent introduction of several real-time PCR detection systems is providing great impulse for the upgrading of previous PCR diagnostic assays (DallaValle et al., 2005).

BACTERIAL DISEASES

Vibriosis is primarily a disease of marine fish, both in commercial production systems and natural waters throughout the world including Tunisia. Stress and overcrowding often are associated with the disease outbreak. The research and the identification of pathogenic bacteria within farmed sea bass and sea bream in Tunisia was conducted during several years. Most frequently was isolated vibrions belonging the genus Vibrio alginolyticus and Vibrio parahaemolyticus which were obtained from different samples, sea water and fish (larvae and adults) (Bahkrouf et al.1995, Kahla-Nakbi et al., 2006 ). Vibrio alginolyticus was also isolated from the internal organs of diseased gilthead sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax) cultured in two fish farms located on the Tunisian Mediterranean coast, from 2003 to 2005. After phenotypic characterisation, a selection of 34 isolates from gilthead sea bream and sea bass were molecularly typed by repetitive intergenic consensus PCR (ERIC-PCR) showing a high polymorphism among the isolated strains (19 genotypes). (Kahla Nakbi et al ., 2006 and Snoussi et al., 2008). Furthermmore, Khemiss et al. (2009) demonstrated that Vibrio vulnificus causes cell damage to the intestine of sea bream.

PARASITIC DISEASES

On the gills and bronchial arch of eleven sparidae species, from different Tunisian lagoons, nine lernaeopodidae species (copepods parasites) have been obtained. It has been revealed that they belong to three genera based on their morphology (Ben Hassine OK et al., 1978). In addition, Plectanocotyle major sp. n. (Monogenea: Polyopisthocotylea: Plectanocotylidae) is described from Chelidonichthys obscurus (Bloch and Schneider, 1801) 44 Cherif Nadia and Hammami Salah collected from the Mediterranean coasts (Tunisia and France) (Boudaya et al., 2006). Pseudodiplectanum syrticum n. sp. (Monogenea: Diplectanidae) was described from the gills of Synapturichthys kleinii (Risso) collected from the Gulf of Gabès in the Mediterranean Sea off Tunisia. (Derbel et al., 2007). Besides, two gadiform species with an ecological and economical importance in the Mediterranean fishing industry, Phycis blennoides and Phycis phycis, were selected for a research study. A total of 592 fresh specimens belonging to the Gadiformes genus were obtained from local commercial fisheries. The investigation was centred on anisakid parasites of 272 specimens of the greater forkbeard (P. blennoides) and 320 of the forkbeard (P. phycis) captured off the Mediterranean coasts of Tunisia (eastern Mediterranean Sea). As a result, four species of nematodes were identified: Anisakis simplex s.1., Anisakis physeteris, Hysterothylacium aduncum and Hysterothylacium fabri. (Farjallah et al., 2006). Larval forms of the genus Anisakis were reported infecting several fish species from the North African coasts of central Mediterranean Sea. Polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analysis was used to investigate the occurrence of larval forms of different Anisakis species in teleost fishes from North African coasts of the Mediterranean Sea and to establish the geographical and host range of these parasites in this area. A total of 282 Anisakis larvae were identified by PCR-RFLP from 13 teleost fish species and one cephalopod species captured at different sites off the Algerian, Tunisian and Libyan coasts. (Farjallah et al., 2008). Six species of digeneans (Proctoeces maculatus (Looss, 1901), Helicometra fasciata (Odhner, 1902), Helicometra pulchella (Odhner, 1902), Macvicaria alacris (Looss, 1901), Peracreadium genu (Nicoll, 1909) and Zoogonus rubellus (Olson, 1868)) were found for the first time in labrid fish (Symphodus tinca (Linnaeus, 1758), Labrus merula (Linnaeus, 1758) and Labrus viridis (Linnaeus, 1758)) from the Bay of Bizerte (Tunisia). Except for P. maculatus and Z. rubellus, which are limited to the rectum, these helminths colonize the entire digestive tract. The study of the seasonal prevalence, abundance and mean intensity shows that three parasites, P. maculatus, H. fasciata and P. genu are present throughout the year while H. pulchella, M. alacris and Z. rubellus are less frequent and appear only in spring (H. pulchella and M. alacris) or in spring and summer (Z. rubellus). The levels of infection and digenean faunal diversity in labrid fish from the Tunisian coasts are generally lower than those from localities within the western Mediterranean. (Gargouri et al., 2009). A xenoma-inducing microsporidian species was found to infect the liver of the teleost fish, peacock wrasse Symphodus (Crenilabrus) tinca. Minimal estimates of the prevalence of the parasite in fishes caught along Tunisian coasts were as high as 43 % for Bizerte samples (over 2 yr) and 72% for Monastir samples (over 3 yr). (Mansour et al., 2005). Fifteen specimens of Pteromylaeus bovinus (Geoffroy St. Hilaire) from the Tunisian coast were examined for ectoparasites during 1996-1998. Myliocotyle pteromylaei gn. and sp. n. found on gills of twelve host specimens was described and illustrated. (Neifer et al., 1999). According to an investigation of metazoan parasites of elasmobranch fishes in the Gulf of Gabès, Tunisia, 2 new species of diphyllidean cestodes were discovered by Neifer et al., in 2001. Macrobothridium euterpes n. sp. is described from the spiral intestine of Rhinobatos rhinobatos, and Macrobothridium syrtensis n. sp. from the spiral intestine of Rhinobatos cemiculus. (Neifer at al., 2001). Seven Gymnura altavela (Linnaeus, 1758) (Elasmobranchii, Myliobatiformes) caught off the Tunisian coast were examined for endoparasites during a three-year period (1995-1998). Principle Fish Pathogens in Tunisian Aquaculture 45

A phyllobothriid cestode new to science was found in the spiral intestine of all host specimens. The presence of a tetrabothridiate scolex, bothridia lacking an apical sucker, laciniate strobila, and possession of post-vaginal testes are sufficient to place this species in the genus Anthobothrium. (Neifer et al., 2002). A survey of the gill parasites of Epinephelus costae (Teleostei: Serranidae) was conducted between 2001 and 2005 in the Gulf of Gabès (Tunisia). Five new species of Diplectanidae (Monogenea) were collected, all belonging to Pseudorhabdosynochus Yamaguti, 1958: P. bouaini sp. n., P. dolicocolpos sp. n., P. enitsuji sp. n., P. sinediscus sp. n., and P. sosia sp. n. These five species differ from each other and from all described species of Pseudorhabdosynochus by the morphology and size of their sclerotized vagina. These diplectanids (except P. sinediscus) were also collected from the same host off Dakar in 1981 and 1989. These five species are the first diplectanids described from E. costae. (Neifer and Euzet, 2007). Six species of the genus Myxobolus (Myxozoa) from the marine environment were collected from two species of mullet (Mugil cephalus and Liza ramada) in Ichkeul Lake, Tunisia. Four of these species were described previously (Myxobolus bizerti, Myxobolus ichkeulensis, Myxobolus spinacurvatura, and Myxobolus episquamalis) and two (Myxobolus exiguus and Myxobolus muelleri) are redescribed. The small subunit ribosomal (18S rDNA) sequences of these six myxozoans were obtained and compared to traditional criteria used in the identification and taxonomy of myxozoan species (such as spore morphology, host specificity, and tissue tropism). A distance analysis of 1,600-1,700 base pairs of the 18S rDNA of the six species indicates that they formed a monophyletic group separate from Myxobolus spp. found as parasites of freshwater fish. (Bahri et al., 2003).

CONCLUSION

One of the development goals of the Tunisian aquaculture master plan is to promote an economically and environmental reliable aquaculture activity which can contribute to the economical development of the country. About 50 coastal sites were identified for future implementation of private aquaculture farms and a national databank of aquaculture development is available in the Ministry of Agriculture (Direction Générale à la Pêche et l'Aquaculture, DGPA). Finally, the strategy of the Tunisian fisheries administration is to establish a full-fledged legal framework for the aquaculture development, covering all aspects as disease and health control, sanitary regulations, environment impacts, as well as a monitoring of pollution generated by aquaculture activities. A licensing-system for aquaculture permits is developed and managed by the DGPA, including all of the above mentioned aspects. Additional research effort has to be devoted to the pathogenesis of important etiological agents and the interactions with their hosts to assist the viability of new fish species farming in the Mediterranean region. Finally, species diversification has been extensively employed in Mediterranean mariculture industry as a tool to relief the crisis resulting from market saturation and overproduction of the two main representatives, sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata). 46 Cherif Nadia and Hammami Salah

REFERENCES

Ababouch L. (2000). Potential of Listeria hazard in African fishery products and possible control measures. Int J Food Microbiol. 62(3), 211-5. Amos K. and Thomas J. (2002). Disease interactions between wild and cultured fish: observations and lessons learned in the Pacific Northwest. Bulletin of the European Association of Fish Pathologists; 22, 95-102. Aranguren R., Tafalla C., Novoa B., Figueras A. (2002). Experimental transmission of encephalopathy and retinopathy induced by nodavirus to sea bream, Sparus aurata L., using different infection models. J Fish Dis 25,317–324. Bahri S., Andree K.B., Hedrick R.P. (2003). Morphological and phylogenetic studies of marine Myxobolus spp. from mullet in Ichkeul Lake, Tunisia. J Eukaryot Microbiol. 50(6), 463-70. Bakhrouf A., Ben ouada H., Oueslati R. (1995). Essai de traitement des vibrioses du loup Dicentrarchus labrax dans une zone de pisciculture, à Monastir, Tunisie = Sea bass Dicentrarchus labrax vibriosis treatment in a pisciculture area, in Monastir, Tunisia. Marine life 5(2), 47-53. Ben Hassine O.K., Essafi K., Raibaut A. (1978). Lernaepodidae, copepod parasites of Tunisian Sparidae. Arch Inst Pasteur Tunis. 55(4), 431-54. Boudaya L., Neifar L., Euzet L. (2006). Plectanocotyle major sp. n. (Monogenea: Plectanocotylidae), a gill parasite of Chelidonichthys obscurus (Teleostei: Triglidae) from the Mediterranean Sea. Folia Parasitol (Praha). 53(1), 53-6. Castric J., Thiéry R., Jeffroy J., de Kinkelin P. and Raymond J.C (2001). - Sea bream Sparus aurata, an asymptomatic contagious fish host for nodavirus. Dis. Aqua. Org., 47, 33-38. Chérif N., Thiéry R., Castric J., Biacchesi S., Brémont M., Thabti F., Limem L., Hammami S. (2009). Viral encephalopathy and retinopathy of Dicentrarchus labrax and Sparus aurata farmed in Tunisia. Vet Res Commun. 33(4), 345-53. Dalla Valle L., Toffolo V., Lamprecht M., Maltese C., Bovo G., Belvedere P., Colombo L.(2005). Development of a sensitive and quantitative diagnostic assay for fish nervous necrosis virus based on two-target real-time PCR, Vet. Microbiol. 110, 167–179. Derbel H., Boudaya L., Neifar L. (2007). Pseudodiplectanum syrticum n. sp. (Monogenea: Diplectanidae), a parasite of Synapturichthys kleinii (Teleostei: Soleidae) from off Tunisia. Syst Parasitol. 68(3), 225-31. Farjallah S., Ben Slimane B., Blel H., Amor N., Said K. (2006). Anisakid parasites of two forkbeards (Phycis blennoides and Phycis phycis) from the eastern Mediterranean coasts in Tunisia. Parasitol Res. 100(1), 11-17. Farjallah S., Slimane B.B., Busi M., Paggi L., Amor N., Blel H., Said K., D'Amelio S. (2008). Occurrence and molecular identification of Anisakis spp. from the North African coasts of Mediterranean Sea. Parasitol Res. 102(3), 371-9. Flegel T.W. (2006). The Special Danger of Viral Pathogens in Shrimp Translocated for Aquaculture. Science Asia 32, 215-221. Gagné N., Johnson S.C., Cook-Versloot M., MacKinnon A.M., Olivier G. (2004). Molecular detection and characterization of nodavirus in several marine fish species from the northeastern Atlantic. Dis Aquat Org 62(3),181-189. Principle Fish Pathogens in Tunisian Aquaculture 47

Gargouri Ben Abdalah L., Elbohli S., Maamouri F. (2009). Digenean diversity in labrid fish from the Bay of Bizerte in Tunisia. J Helminthol. 7, 1-7. Hastein T. and Lindstad T. (1991). Diseases in wild and cultured salmon: possible interaction. Aquaculture;98, 277-88. Kahla-Nakbi A.B., Chaieb K., Besbes A., Zmantar T., Bakhrouf A. (2006). Virulence and enterobacterial repetitive intergenic consensus PCR of Vibrio alginolyticus strains isolated from Tunisian cultured gilthead sea bream and sea bass outbreaks. Vet Microbiol. 117(2-4), 321-7. Khemiss F., Ahmadi S., Massoudi R., Ghoul-Mazgar S., Safta S., Moshtaghie A.A., Saïdane D. (2009). Effect of in vitro exposure to Vibrio vulnificus on hydroelectrolytic transport and structural changes of sea bream (Sparus aurata L.) intestine. Fish Physiol Biochem. 35(3):541-9. Mansour L., Prensier G., Jemaa S.B., Hassine O.K., Méténier G., Vivarès C.P., Cornillot E. (2005). Description of a xenoma-inducing microsporidian, Microgemma tincae n. sp., parasite of the teleost fish Symphodus tinca from Tunisian coasts. Dis Aquat Organ. 65(3), 217-26. Neifar L. and Euzet L. (2007). Five new species of Pseudorhabdosynochus (Monogenea: Diplectanidae) from the gills of Epinephelus costae (Teleostei: Serranidae). Folia Parasitol (Praha). 54(2), 117-28. Neifar L., Euzet L., Ben Hassine O.K. (1999). Myliocotyle pteromylaei gn. and sp. n. (Monogenea, Monocotylidae) gill parasite of Pteromylaeus bovinus (Euselachii, Myliobatidae) in Tunisia. Parasite 6(4), 323-7. Neifar L., Euzet L., Ben Hassine O.K. (2002). Anthobothrium altavelae sp. n. (Cestoda: Tetraphyllidea) from the spiny butterfly ray Gymnura altavela (Elasmobranchii: gymnuridae) in Tunisia. Folia Parasitol (Praha). 49(4), 295-8. Neifar L., Tyler G.A, Euzet L. (2001). Two new species of Macrobothridium (Cestoda: Diphyllidea) from rhinobatid elasmobranchs in the Gulf of Gabès, Tunisia, with notes on the status of the genus. J Parasitol. 87(3), 673-80. Olivier G. (2002) Disease interactions between wild and cultured fish-perspectives from the American Northeast (Atlantic Provinces). Bulletin of the European Association of Fish Pathologists 22,103-9. Rigos G. and Katharios P. (2009). Pathological obstacles of newly-introduced fish species in Mediterranean mariculture: a review. Rev Fish Biol Fisheries. Snoussi M., Noumi E., Cheriaa J., Usai D., Sechi L.A., Zanetti S., Bakhrouf A. (2008). Adhesive properties of environmental Vibrio alginolyticus strains to biotic and abiotic surfaces. New Microbiol. 31(4), 489-500.

Chapter 6

BREEDING THE SILVER POMFRET, PAMPUS ARGENTEUS (EUPHRASEN), FOR AQUACULTURE: ACHIEVEMENTS AND CHALLENGES

Sulaiman M. Almatar and Charles M. James Mariculture and Fisheries Department Kuwait Institute for Scientific Research, Salmiya, Kuwait

ABSTRACT

The silver pomfret, Pampus argenteus (Euphrasen), is a prime food fish that has a high market price and demand in Asian countries. Due to a declining trend in the wild stocks of this fish in recent years, research efforts are diverted towards developing a commercially viable aquaculture technology for this species. The Kuwait Institute for Scientific Research succeeded for the first time in 1998 in larval rearing and grow-out culture of silver pomfret based on the eggs collected from the wild. The egg collection trips from the wild enabled to study extensively the spawning frequency, fecundity, type of spawning and availability of gravid fish in Kuwait waters. Over the years from 1998 till to date research has focused on refinements in hatchery larval rearing and grow-out production. For larval rearing conventional live feeds such as Isochrysis, Nannochloropsis and Chlorella along with rotifers followed by Artemia nauplii were used till they were weaned to commercially available formulated feeds. The larvae were reared at 27-29oC using 1-4m3 capacity tanks. Using of mixed species of microalgae maintained at a cell density of 1x106 cells/ml in the larval rearing media with rotifers at 5/ml showed significantly higher (P<0.05) survival compared to that of using individual algal species. Performance of formulated feeds on the growth of juveniles under grow-out tank culture conditions has been evaluated. Annual growth performance of silver pomfret show that the growth is fast during the first four months compared to that of the later part of the culture period. The growth rate also depends on the water temperature showing decreased growth rate during winter. One year old silver pomfret size ranged from 69.0- 308.0g with a mean of 172.5±57.6g, n=150. Wide fluctuations in size occur in the population due to the small size of the males compared to that of females. After 20 months of grow-out period, the fish size ranged from 86.0-431.0g. During this time the male size averaged 139.5±35.9g, n=80, and the female size averaged 254.6±55.5g, n=53. 50 Sulaiman M. Almatar and Charles M. James

The results show that it is possible to obtain marketable size fish of over 250g size in 20 months of culture period under Kuwait’s environmental conditions. Spawning of the cultured brood stock of silver pomfret was elusive over the years and first breakthrough in natural spawning of two years old cultured brood stock was achieved in 2006, but the eggs were not fertilized. Studies were initiated from August 2007 onwards to induce spawning of the fish using HCG. The results show that successful ovary development and spawning of the fish is possible using HCG at 1000- 2000 IU/kg body weight. Full ovary development and spawning occurred after 8-9 hours of first HCG administration or after the second dose given the following day. Although the females naturally released the eggs in the tanks, eggs were not fertilized and in order to achieve egg fertilization the females and males were stripped. During 2008 spawning period, in addition to using HCG, succeeded in induced spawning the fish using LH-RH (a). During 2009 spawning period, fertilized eggs and hatched out larvae were observed in the natural spawning of cultured brood stock showing the possibility of obtaining fertilized eggs from the brood stock holding facility through natural spawning. Further studies are concentrating on enhancing the egg production, egg fertilization and hatching rates during the hormonal induction as well as enhancing the milt production in cultured males. Future prospects and challenges in breeding the silver pomfret for commercial ventures is discussed.

INTRODUCTION

The silver pomfret, Pampus argenteus (Plate 1), is a benthopelagic marine fish with a wide geographical distribution from East China Sea to Southeast Asia, Indian Ocean and the Arabian Gulf (Haedrich, 1967) (Plate 2). In the inshore waters it usually occurs in schools over muddy bottoms and feeds on ctenophores, scalps, medusa and other zooplankton organisms (Dadzie et. al., 2000). The northern Arabian Gulf stock of silver pomfret is exploited by fishermen in Kuwait, Iraq and Iran when it migrates to waters in the northern Arabian Gulf from March to October. During cooler months from November to March, the stock is believed to migrate to deeper waters. After winter, as the waters warm up from March to May, the silver pomfret adults return to spawn in coastal areas at the head of the Arabian Gulf including Kuwait’s waters. The nature and extent of specific nursery grounds in the northern Arabian Gulf is not fully known (Al-Hussaini, 2003). The silver pomfret is a highly valued prime food fish to the commercial fishing industry having worldwide market demand. It is also used in Chinese medicine (Tang, 1987). It is the most expensive fish in Kuwait and is considered as one of the fishes of highest quality not only by Kuwaitis but also by other nationals. Table 1 shows the total worldwide catch of silver pomfret during the period from 1990 to 2000 and percentages of contribution to the catch by different countries. During the above period, the total world catch averaged 143,197t. The major contributor is China (42.3%) followed by India (28.1%). In the northern Arabian Gulf, landings of silver pomfret from the Kuwaiti waters averaged to 715 t/yr in 1972-1979 but decreased to an average of 300 t/yr in 1982-1988 due to closing of fishing areas in the Kuwaiti and Iranian waters during the Iran-Iraq war.

Table 1. Total Catch of Zobaidy (t) Worldwide and Percentage Contributions of Different Countries from 1990 to 2000

Year Country 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 Average China* 35.4 35.0 30.1 41.4 39.8 33.1 40.1 44.7 51.5 54.3 55.6 42.3 Hong Kong 2.6 2.4 2.8 1.7 1.3 1.5 1.5 1.5 1.5 1.0 1.2 1.7 India 28.2 31.5 25.9 31.9 36.2 36.7 27.3 27.1 22.7 20.0 20.4 28.1 Indonesia 12.1 10.4 13.3 12.4 9.6 11.9 14.5 15.1 14.5 13.7 14.5 12.9 Korea 12.8 12.1 13.6 3.6 2.6 3.0 3.5 0.7 0.7 2.2 - 4.6 Kuwait 0.3 0.4 0.9 0.8 0.6 0.7 0.6 0.4 0.3 0.2 0.2 0.5 Malaysia 0.0 0.0 0.0 0.0 3.0 3.3 3.7 3.8 3.7 2.8 2.3 2.1 Pakistan 2.7 2.3 2.1 2.2 1.7 2.6 2.0 2.8 2.8 3.0 2.6 2.4 Philippines 1.8 1.6 6.2 1.7 1.2 1.5 1.7 0.7 0.9 1.0 1.0 1.7 Singapore 0.0 0.0 0.0 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.0 0.1 Taiwan 3.4 3.6 3.7 3.0 2.3 4.4 3.7 2.0 1.1 1.6 1.9 2.8 Thailand 0.8 0.8 1.4 1.2 1.5 1.2 1.2 1.2 0.3 0.2 0.3 0.9 World (Total) 117,353 135,709 121,696 140,660 173,743 158,058 137,332 135,591 147,057 155,648 152,324 143,197 *Data from China were corrected. Source: FAO Fishstat Plus Version 2.30, 2001.

52 Sulaiman M. Almatar and Charles M. James

Even though, the catches increased to an average of 1,000 t/yr in1991-1995 when the restrictions on fishing grounds were lifted in 1991, the silver pomfret landings in Kuwait declined to only around 120 t/yr in 2000 (Figure 1). Similarly, catches of silver pomfret from the adjacent Iranian waters in the northern Arabian Gulf also decreased from a peak of 1,689 t in 1997 to as low as 115 t in 2000 (Al-Hussaini, 2003). The depletion of wild silver pomfret stock in recent years was attributed to over-fishing and to environmental degradation of the northern Arabian Gulf. The silver pomfret captured from the Kuwait coastal waters is not sufficient to sustain the local consumption in Kuwait and the fish has to be imported from neighboring countries to meet with the market demand. Because of the insufficient catch and declining wild stock in the Arabian Gulf, the market price has increased from about US$8.5 in 1994 to over US$ 19.5 per kg in recent years (Al-Hussaini et. al. 2006).

Plate 1. Cultured silver pomfret Pampus argenteus (Euphrasen, 1788).

Plate 2. Distribution map of silver pomfret Pampus argenteus (Source: GBIF.ORG). Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 53

Figure 1. Declining trend in silver pomfret catches, locally know as zobaidy, from Kuwait’s fisheries and increasing market price (Source: Al-Hussaini, 2003).

In spite of the decline in the wild stocks and the increase of the worldwide market demand and price, the research relevant to developing aquaculture technologies for this species of fish was negligible before 1998. Some attempts in artificial fertilization of eggs and larval rearing were made in 1982 without achieving to the fry stage production (Oda and Namba, 1982). Limited attempt was also made to culture the fish in pond using juveniles collected from the wild (Pati 1984). The Mariculture and Fisheries Department (MFD) of Kuwait Institute for Scientific Research (KISR) had initiated and implemented a research project for the first time, during April 1998 – March 2003 (Phase-I) to assess the technical feasibility for raising the fish from the eggs to marketable size (Almatar et al., 1998). Following a breakthrough, for the first time in the world, in larval rearing of this fish in the hatchery based on eggs collected from the wild and successful raising of the fish to maturity under tank culture conditions during Phase- I research period, Phase-II research was initiated in September 2007 and succeeded in breeding cultured brood stocks of silver pomfret paving the way for possible development of technology for considering this species as a potential new candidate for commercial ventures. This chapter reviews the advances made in developing the culture technology for silver pomfret and the challenges to be resolved to bring out a reliable technology for commercial farming of silver pomfret as one of the most important and wanted candidate species for aquaculture.

SPAWNING OF WILD STOCK IN KUWAIT WATERS

Almatar et al. (2004) has described extensively the spawning pattern of silver pomfret in Kuwait waters, especially relevant to spawning frequency, fecundity, egg weight and type of spawning based on fishing conducted using gillnets during the period from May 1998 to 54 Sulaiman M. Almatar and Charles M. James

October 1999 and from May to September 2000. The results showed that the length-weight relationship differed between sexes whereby females were significantly larger than males. Females captured with gravid and running-ripe maturity stages during the period of fishing in 1998, 1999 and 2000 indicated that P. argenteus in Kuwait waters spawn from middle of May and continue until early October. Large females spawned at the beginning of the spawning season (May-June) while young females spawned during later months (August-September). Sex ratios at the spawning ground were dominated by males during the entire spawning period. Average sex ratio for males was about 70.3%. During the spawning season the water temperature ranged from 26.0 to 32.8 oC and sea water salinity 39.0 ‰. The water depth in the spawning grounds ranged between 5-12m. Spawning occurred after 13.00h, with peak spawning between 15.00 and 18.00 h during outgoing tide. Silver pomfret is a multiple batch spawner with indeterminate fecundity. Spawning frequency was always associated with the lunar cycle and spawning was concentrated during the first and third quarters of the moon period, indicating a semi-lunar reproduction cycle. The study observed that a female would spawn at least six times during the spawning season. Average relative batch fecundity was 176.3 eggs/g somatic weight (SW), corresponding to a relative total fecundity of 1058 eggs/g SW. Bigger fish produced heavier eggs and the egg weight decreased as the spawning season progressed.

Maturity Stages in Relation to Day Time

Gonad maturity stages of wild caught females silver pomfret are classified into 8 stages based on its visual appearance and size of the oocytes. For practical identification, the female gonad maturity stages are classified as Stage-1 Virgin; Stage-2 Developing -virgin or resting; Stage-3 Developing; Stage-4 Developed; Stage-5 Gravid; Stage-6 Running-ripe; Stage-7 Partially spent; Stage-8 Recovery (Table 2). Males, however are classified as spawning if milt was excreted by applying gentle pressure on the abdomen or non-spawning if no milt was observed. In the wild catch, matured gravid females with very much enlarged yellowish to red ovary, defined as ‘stage 5’, normally occur between 12:00 and 15:00h. At this stage the eggs are not released with slight pressure on the abdomen. Whereas in fully ripe gravid females with hydrated and oozing ovulated eggs, defined as ‘stage 6’ the eggs are released with slight pressure on the abdomen (Plate 4). The stage 6 females are normally caught between 15:00 - 18:00h coinciding with peak spawning activity of a day. Only spent females were observed during night hours. The Gonado Somatic Index (GSI) of males averaged 0.16±0.07% (n=42) from November to February and averaged 0.44±0.16% (n=30) in March-April. Running ripe males appeared in early May when the GSI increased and averaged 0.59±0.19% (n=42). Males were found to mature earlier than females; all males captured between June and October were running ripe and GSI averaged 0.68±0.21% (n=101). The monthly GSI of female fish was low during November through March (resting stage) averaged 0.76±0.2% (n=35), increasing in April to average 2.0±0.8% (n=36) (developing stage). The range of GSI values began to increase during the spawning season because of individual variation in the timing of gonadal development, i.e. concurrent occurrence of developed, gravid, running-ripe and partially spent stages.

Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 55

Table 2. Description of gonad maturity for female silver pomfret caught from the wild in Kuwait (Almatar et al, 2004)

Macroscopic Microscopic Virgin The gonad is thread-like. Sometime Oocytes less than 100µm difficult to sex in small size females. Developin Ovary small (creamy to pale yellow Only primary oocytes are present. Some g-virgin or colour). Small opaque eggs visible (mean sample might have a few oocytes in early Resting GSI 0.6 ± 0.2, N = 26). Maximum oocyte yolk vesicle stage. No yolky oocytes, tunica size 0.65mm. Black spots may be seen thick. scattered on the ovary in resting stage. Developin Ovaries translucent yellow to creamy Primary and secondary oocytes present. In g colour with opaque oocytes present. Few some samples a third group with true yolk ovarian blood vessels and no sign of granules (tertiary oocytes) was visible. No previous spawning (mean GSI 2.0 ± 0.9, N hyaline eggs, some atrophy can be = 36). Maximum oocyte size 0.70mm observed. Developed Ovaries large, yellowish in colour, opaque Three groups of oocytes are present. This oocytes visible. Increased ovarian blood stage resembles partially spent oocytes, and vessels (mean GSI 7.3 ± 2.1, N=75). a recruited batch for FOM can be seen. Old Maximum oocyte size 0.9-1.0mm. POF may be found, atrophy of advance oocytes present. Gravid Swelling of belly is visible externally All stages of oogenesis present. Majority of because of large ovaries filling the whole the oocytes are tertiary and are in different body cavity. Ovaries yellowish pale or stages of FOM. Hyaline oocytes still in reddish in colour. Clear hydrated oocytes follicle. Very old POF may be present. visible among opaque oocytes giving a Different stages of atrophy also present. speckled appearance. No eggs released with light pressure on abdomen (mean GSI 14.9 ± 3.7, N=96). Maximum oocyte size 1.1-1.2mm. Running – Ovaries enlarged and jelly-like, oocytes Primary, secondary, tertiary and hyaline ripe have been ovulated and freely oozed out oocytes are present. Ovulation has occurred, naturally or with light pressure on abdomen fresh POF present. Tunica very thin. as white transparent eggs. Weight and GSI range more or less similar to gravid stage. Partially Ovaries somewhat flaccid just after Three groups, primary, secondary and spent spawning, yellow or reddish due to tertiary oocytes present. POF of different increase blood vessels. Opaque eggs ages nearly always present. Tunica very visible. This stage will resemble the thin. Residual hyaline oocytes may be developed stage a few days after spawning present and undergoing atrophy. (mean GSI 4.0 ± 1.5, N = 41). Maximum oocyte 0.6-0.7mm Recovery Ovaries flaccid reddish in colour, no Primary oocytes of perinucleolar stage opaque oocytes visible (mean GSI = 4.6 ± present. A loose ovarian tissue with many 1.5, N = 15). Peak maximum size 0.5mm. spaces between ovigenous folds. Some bigger yolky oocytes can be seen undergoing atresia. Old POF can be encountered. POF, post-ovulatory follicle; FOM, final oocyte maturation; Primary oocytes, small oocytes, most advance stages are in perinucleolus stage; Secondary oocytes, oocytes with cortical alveoli; later stages show the start of true vitellogenesis; Tertiary oocytes, oocytes with true vitellogenesis and yolk granules; in later stages lipid droplets start fusion. FOM, stages of oocytes showing germinal vesicle migration or breakdown and coalescing of yolk granules and lipid droplets into homogeneous mass. 56 Sulaiman M. Almatar and Charles M. James

From May to October the GSI of developed ovaries averaged 7.3±2.1% (n=75) while gravid ovaries showed an average GSI of 14.9±3.7% (n=96). Just prior to ovulation the most advanced group of eggs take up fluid and increase in volume. These hydrated eggs greatly increase the ovarian weight. It was difficult to estimate GSI for running ripe females because eggs oozed out freely as the fish were taken out of water, but the mean values may be assumed to be between 16.0 and 17.0%. Mean GSI value for partially spent females was 4.0 + 1.5, n=41. Fish in spent stage were few and first appeared in June, while the frequency increased in October with GSI values averaged 1.7±0.2 (n=6). Recovering stages started to appear in August and peaked in September with GSI averaging 4.6±1.5% (n=15).

INITIATION OF CULTURE THROUGH COLLECTION OF EGGS FROM WILD SPAWNERS

In order to initiate culture of silver pomfret, several trials were made to collect wild brood stock from Kuwait’s coastal waters and transferred to the cultured tanks. However, the wild brood stock collected using drifting gill nets were badly injured by the nylon line which dug into its flesh. The overall survival of wild-caught breeders was very low and not encouraging. Furthermore, the wild caught fish did not survive due to difficulties in feeding them in captivity as they did not accept formulated feeds and therefore, it was almost impossible to keep the wild fish brood stock alive due to the sensitive nature of the fish. It was realized that the only alternative way to initiate the culture of silver pomfret was to strip the ripe fish to obtain fertilized eggs from the wild breeders.

Fishing Trips

Towards initiating the culture of silver pomfret, the first successful collection of fertilized eggs were made by stripping fully-ripe male and female spawners caught by gillnets in Kuwait waters during June 1997. Larvae hatched from fertilized eggs were reared until 90 days after hatching (DAH) in water temperatures of 27-30 oC. This enabled to observe and describe the larval and juvenile developmental stages of silver pomfret under laboratory rearing conditions (Almatar et al., 2000). Following the successful larval rearing of silver pomfret for the first time in the world, several fishing areas in Kuwaiti waters covering an area of 40 km2 within latitudes 29o 22’ N and 29o 24’N to longitudes 48o 00’E and 48o 06’E were surveyed from May to October in 1998, 1999 and 2000 as well as from June to August in 2001 and 2002 (Plate 3). Fishing trips were made from 10:00h to 18:00h. Collection trips were also made during the night to assess the time of spawning in the wild. During these trips matured gravid silver pomfret females with oozing eggs and matured males were caught using 14cm mesh stretch size drifting gill nets and used for stripping to obtain fertilized eggs for hatchery larval rearing. Such, fishing trips are continued till to date whenever there is a need for collection of fertilized eggs from wild spawners.

Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 57

Availability of Gravid Fish

The fishing trip surveys carried out in Kuwaiti waters show that fully mature running males outnumber the females with an average ratio of 3:1. During May to September 1998 spawning period, out of 2,743 fish caught, running-ripe females (Plate 4) with oozing eggs were maximum during June (38%) followed by July (30%) and August (23%). While it was running-ripe minimum in May (8%) and September (1%) (Al-Abdul-Elah et al., 2003). Mean size of gravid and running-ripe females in June (FL 26.6±3.0 cm, wt 630.3±221.4g) was significantly higher (P<0.01) than the females caught in July (FL 25.1±2.7 cm, wt 539.1±203.6g) or in August (FL 24.8±2.7 cm, wt 470.2±169.2g). During 1999 spawning season occurrence of gravid and running-ripe females were at the maximum in July (55%) followed by August (26%), while it was minimum in May (0.05%) and September (2%). Similar to 1998 spawning period, the mean size of spawning females was high in June (FL 26.9±2.5cm, wt 677.4±180.6g) compared to that of the fish in July (FL 26.2±2.6cm, wt 594.2±174.4g). For the collection of eggs from wild spawners, fully matured males and females are brought to the hatchery in thermo cool box with ice within an hour after catching and stripped into a plastic bowl. After stripping, the eggs and sperms are mixed gently. The fully ripe female at stage-6 provides a good flow of transparent eggs with gentle abdominal pressure (Plate 5). The males however have small testes and produce only a few drops of milt after gentle abdominal pressure. The fertilized eggs are washed thoroughly with filtered seawater to remove body fluids and other debris. The collected eggs are quantified using 1-2 liter capacity graduated cylinders. The floating viable eggs are transferred to hatching nets and the sunken non-viable eggs are discarded. The fertilized eggs are spherical, transparent and pelagic, with an average diameter of 1.08mm and having a single pale oil globule of about 0.34mm diameter and a weakly segmented yolk of 0.85mm in diameter (Plate 6).

Plate 3. Capturing of silver pomfret using 14cm mesh drifting gill net. 58 Sulaiman M. Almatar and Charles M. James

Plate 4. Running-ripe female at stage-6 caught by drifting gill net.

Plate 5. Stripping of stage-6 female caught from the wild.

The fertilized eggs are incubated in hatching nets of 29cm dia. X 42cm deep (22.5-L working volume) continuously supplied with 0.5 L/min fresh aerated ambient seawater (Plate 7). The egg incubation temperature was always maintained to the ambient seawater temperature. The eggs are incubated at a stocking density of 2000 eggs/L. At ambient seawater temperature of 29-30oC, the eggs hatch out after 15-20h of incubation. Newly hatched larva has a large, ellipsoidal yolk and an undeveloped mouth; its size averaged 2.4mm in total length. Experimental studies indicated that better egg hatching rates occur at incubating temperature of around 29.5oC and at ambient seawater salinities of 35-40 ‰. While under low salinity regimes of 10-30‰ the hatching rates were significantly low (Al-Abdul-Elah et al., 2002) compared to that of using ambient seawater salinity of about 40‰. Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 59

Plate 6. Developing stages of silver pomfret egg and newly hatched larva.

Plate 7. Egg incubating nets used in silver pomfret hatchery.

60 Sulaiman M. Almatar and Charles M. James

LARVAL REARING

For mass larval rearing and fry production 1-4m3 capacity round fiberglass tanks are used. Several experiments have been carried out over the years from 1998 onwards on the requirements for hatchery larval rearing of silver pomfret (Al-Abdul-Elah et al., 2001, 2002; Almatar et al., 2003). The results of these experiments over the years show that the optimal temperature for larval rearing is 27-29oC. The effect of stocking density on the growth and survival showed that both the growth and survival rates of larvae were not significantly different among the range of stocking densities of 20, 30 and 40 larvae/L. Better survival of larvae was achieved in the 4m3 capacity tanks than in the smaller 1m3 capacity tanks. During the larval rearing period, first peak mortality of the larvae were observed at the ages of 6-9 days after hatching (DAH) followed by second peak at 13-16 DAH and a third peak at 22-32 DAH. The second and third peak mortalities normally coincide with the tendency of larvae to swallow tiny air bubbles while they feed on live food organisms, especially at the water surface. Towards addressing the larval mortalities and enhancing the larval survival, several refinements were made over the years in the hatchery larval rearing procedures.

Effect of Microalgal Species on Larval Survival

Studies carried out on the efficiency of microalgal species such as Chlorella, Isochrysis and Nannochloropsis for feeding early larval stages indicated that using these algae alone as the initial feed for silver pomfret larvae without addition of rotifers is not conducive for the survival of early larvae (Al-Abdul-Elah et al., 2001). At 6 DAH, a maximum survival of 3% was observed with Isochrysis followed by Nannochloropsis (0.35%) and Chlorella (0.25%). All the larvae, fed with algae alone, died at 6 DAH. Further investigations using the above microalgae with rotifers and a mixture of these microalgae with rotifers showed that significantly higher survival (9.7% at 12 DAH) could be achieved in the mixture of microalgae maintained at a density of 1x106 cells/ml in the larval rearing media with rotifers at 5/ml in the culture tanks. At this feed regime, the ω-3 fatty acids in rotifers were high (36.32±0.68, n=2) and the incidence of feeding on rotifers was enhanced in larvae subjected to this feed regime (Al- Abdul-Elah et al., 2001). Studies show that the incidence of feeding on rotifers from 4 DAH was significantly high (P<0.05) in mixed species of algae (60%) and in tanks having Isochrysis (55%) compared to that of using Chlorella and Nannochloropsis. The silver pomfret larvae foraging on rotifers (Plate 8) considerably increased from 8 DAH till they were weaned to Artemia nauplii at 14 DAH onwards for a week before they were trained to accept inert feed. The hatchery larval rearing of silver pomfret lasts for about 40-45 DAH. The larval mortalities are much reduced and the survival is high from 30-35 DAH when they metamorphose to juveniles. Under experimental culture conditions, it was possible to achieve 3.6-4.2% larval survival with a mean of 3.9% using mixed species of microalgae in the larval rearing tank and rotifers fed with Isochrysis and treated with nutritional enrichment media, such as commercially available ‘Selco’, ‘Super Selco’ and ‘DHA Protein Selco’ (INVE, Belgium). Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 61

The larvae are easily weaned to commercially available inert larval feeds from 18-20 DAH onwards. The formulated feeds are offered as paste feed suspended in the water column using plastic trays. After 45-50 DAH, the juveniles are harvested and can be directly stocked in grow-out culture tanks (Plate 9).

Plate 8. Silver pomfret larvae foraging on rotifers at 10 DAH.

Plate 9. Silver pomfret juveniles produced in the hatchery.

Larval Mortality and Air Bubble

The silver pomfret larvae have a tendency to ingest air bubble occurring in the larval rearing tanks due to aeration, especially during the second week of larval rearing period. Using of surface skimmers to remove the air bubble from the culture system failed to resolve 62 Sulaiman M. Almatar and Charles M. James this problem since the larvae ingests tiny air bubble occurring at the water column and at the water surface (Plate 10). The air bubble ingestion continued till the nursery period even after terminating use of live food in the larval rearing tanks. Considerable larval mortality occurred during this period due to bloating of larval stomach with air bubble that makes the larvae to swim erratically resulting in bellying up of the individuals floating on the water surface and causing heavy mortality.

Plate 10. A) Ingestion of air bubble at water surface; B) Air bubble ingested larva in the culture tank at 28 DAH.

Several techniques were used to avoid air bubble ingestion by silver pomfret, the rearing tanks were provided with air-lift pipes (Plate 11) but still, tiny air bubbles occurred. One method to resolve this problem was using a surface skimmer to skim the water to reduce the surface tension as well as to remove the air bubble.

Plate 11. Larval rearing tank provided with surface skimmer and air-lift pipes.

Another method was addition of ω-3 enriched cod liver oil that eliminated the air bubble at the water surface as well as help in the enrichment of rotifers and Artemia nauplii present in the larval rearing tanks. The excess oil was removed from the culture system using a Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 63 surface skimmer (Plate 12). This helps in reduction of the incidence of air bubble ingestion and related mortalities.

Plate 12. Elimination of air bubble using ω-3 oil and removal of oil from water.

PERFORMANCE OF FORMULATED FEEDS ON THE GROWTH OF JUVENILES

Considerable progress has been made on the nutritional requirements for this species under grow-out culture conditions due to the research studies carried out at MFD, KISR. Preliminary studies were carried out from April 1998 to March 2003 on the growth performance and feeding behavior of juveniles under tank culture conditions using several commercially available fish feeds and locally made formulated paste feed (Cruz et al., 2000). Studies on the performance and feeding behavior of silver pomfret fingerlings with an average weight of 15.2g fed with the test diet consisting of Turbot feed, Ecostart 16 by Biomar, France offered as dry and moist pellets, carried out in six 1m3 capacity tanks, showed that the survival rate of the fish fed with wet pellets was significantly higher (P<0.03) compared to that of fish fed with dry pellets (Cruz et al., 2000). These investigations observed poor performance of commercial sea bream and turbot dry pellets compared to that of using semi-moist salmon feed and re-pelletized salmon feed mixed with shrimp meat, encapsulated larval diets, fish oil, vitamin and mineral mix (Cruz et al., 2003). All the commercial feeds tested till 2003 were not satisfactory relevant to the growth and survival of this species. The average daily growth rate observed during these early investigations, till 2003 culture period, for up to 50g size group of this fish was less than 0.34g/fish/d. Towards determining the optimum growth of silver pomfrets under tank culture conditions, experiments were carried out during 2004 and 2005 culture period using commercially available feeds as well as locally formulated feeds and feed additives. Because crustaceans such as copepods as one of the major food component in the natural diet of silver pomfret in the wild (Dadzie et al., 2000), commercially available copepods under the brand 64 Sulaiman M. Almatar and Charles M. James name “Cyclopeeze” (Argent Chemical Laboratory, Redmond, WA, USA) and fresh shrimp meat in the diet were investigated along with other commercial feeds to determine the efficiency of these feed components in the diet for the growth of the fish (Almatar and James, 2007). Experiments carried out during 2004 investigated the efficiency of using salmon feed mixed with cyclopeeze, salmon feed mixed with shrimp meat on silver pomfret juveniles of about 4.0-4.5g initial size. The second experiment evaluated salmon feed alone, and shrimp meat alone for feeding silver pomfret juveniles of about 28.0-29.0g initial size. The results showed that inclusion of shrimp meat in the diet either with salmon feed or alone give significantly high (P<0.01) weight gain and growth rate of up to 1.10±0.06 g/fish/d and significantly lower (P<0.001) feed conversion ratio compared to that of feeds without shrimp meat. The experiments carried out during 2005 investigated the use of commercially available formulated feeds with feed additives on silver pomfret juveniles of about 12.0-13.0g initial size. The results showed that feeding with ‘Gemma’ (SKRETTING) feed with 54.0% crude protein and 19.0% crude fat or salmon feed with 41.4% crude protein and 23.9% crude fat give significantly high (P<0.01) growth rates compared to that of pompano feed with 43.0% crude protein and 6.0% crude fat (Almatar and James, 2007). Since the knowledge of optimum protein requirement is essential for formulation of well balanced, low cost and environmentally friendly formulated diets, experiments were carried out to determine the dietary protein requirement of silver pomfret with an initial body weight of 12.4±0.12g (Hossain et al., 2010). Five semi-purified experimental diets were formulated to contain 35, 40, 45, 50 and 55% protein level with 12% lipid in all the diets. The results show that the growth of fish fed 45% protein diet was not significantly different (P<0.05) from that of fish fed 50 or 55% protein in the diet, but the growth was significantly higher than that of fish fed 35% or 40% protein. Significantly efficient food conversion ratio (FCR) was observed in diets containing 45, 50 and 55% protein. The FCR ranged between 1.7 and 2.5 in these diets. Fish fed 50% dietary protein showed significantly best apparent net protein utilization. The study concluded that the optimum dietary protein level for silver pomfret is 49% with a dietary lipid level of 12%. As a follow on the dietary protein requirement, studies were carried out on the dietary lipid requirement of silver pomfret. The experimental diets consisted of three treatments with 12%, 16% and 20% dietary lipid in the feed containing 49% protein. Juveniles with 33-35g initial body weight were used. After four months of culture period, the fish fed with 16% dietary lipid exhibited significantly higher growth (P<0.05) compared to that of diets containing 12% and 20% dietary lipid. Although growth is satisfactory under experimental conditions, a further refinement in feed formulation is required on the juveniles of this species.

GROW-OUT UNDER TANK CULTURE CONDITIONS

The silver pomfret juveniles used for the grow-out culture studies originated from eggs collected from the wild spawners during July 2004. After the hatchery larval rearing period, the juveniles were stocked in round fiberglass tanks of 3m3and 4m3 capacities for grow-out production. After 11 months of grow-out culture period, the fish were transferred to two 25 m3 capacity circular out-door concrete tanks and after 15 and 20 months of grow-out culture Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 65 period, potential brood stock fish were stocked in two 125 m3 capacity out-door concrete tanks. Seawater was flowed through the tanks to maintain a water exchange rate of about 8-10 times a day. Ambient seawater mixed with ground well seawater, with a temperature of 24- 26oC, were used to maintain the tank water culture below 30oC during summer and above 20oC during winter, since the ambient seawater temperature increase to over 31oC during summer and declines to less than 17oC during winter in Kuwait. All the tanks were equipped with central stand pipe and drainage. The fish were sampled once a month as well as during transferring from the tanks for growth evaluation. During sampling, all the fish were weighed individually using a digital sensitive balance (model SBC-61 from Scaltec Instruments, Germany).

Table 3. Feed Composition Used for the Grow-out Culture of Pampus argenteus

Feed ingredients % Salmon feed 93.0 Carpmin Forte* 1.0 Proburst-A** 0.2 Stabilized vitamin C 0.2 Fish oil 5.0 Binder 0.6 *Supplied by APC Nutrients Pvt. Ltd., India. Contains minerals (mg/kg diet): Calcium 1500; Phosphorus 450; Magnesium 11; Manganese 5; Zinc 11; ferrous 5; Copper 2; Cobalt 0.5; Sodium 10; Potassium 10; Sulphur 10; Iodine 1; Selenium 0.002; Molybdenum 0.001. ** Gut conditioner supplied by APC Nutrients Pvt. Ltd., India. Contains probiotics Lactobacillus and Yeast nutrilities

For handling the fish while sampling as well as during transfer from one tank to another, 3 ppm of the tranquilizer ‘Quinaldine’ (Argent Chemical Laboratories, USA) was used. Commercially available salmon feed (Dana Feed A/S, Denmark) mixed with commercially available feed additives were used. Table 3 shows the feed composition offered for feeding silver pomfret during the grow-out culture period. Feed was prepared by mixing all the ingredients along with salmon feed and re-pelletized using a meat grinder. Agar-agar was used as a binder. The fish were fed daily 3-4 times at libidum. The tank water temperature was monitored in the morning at 0800 h as well as at noon using an ordinary mercury thermometer. Dissolved oxygen concentration was monitored, using YSI-model 55, USA, three times a week. The initial size of the hatchery produced P. argenteus fingerlings ranged from 1.6-5.2 g with a mean of 3.7±0.9 g (n=150) during August 2004. Figure 3 shows the mean weight observed for the silver pomfret from August 2004 to October 2005 under tank grow-out culture conditions. The initial growth rate was fast during the first four months compared to that of the later part of the culture period. The daily fish weight gain significantly increased (P<0.01) from 0.56 g/fish/d during September (2nd month) to 1.5 g/fish/d during November (3rd month) at temperatures ranging from 28.5-29.5 oC (Figure 4). During this time the fish size ranged from 47.5-134.4 g with a mean of 81.9±12.2 g (n=150). After four months of culture, during December, the fish size ranged from 50.5-168.2 g with a mean of 91.01±22.3g (n=150). However, with the decrease of temperature from 66 Sulaiman M. Almatar and Charles M. James

28.5oC to 27.0oC, the growth rate declined to 0.69 g/fish/d. The growth rate further declined to 0.3 g/fish/d during January with the decrease of temperature to 21oC. Further decline in growth to 0.14 g/fish/d was observed during February and March culture period in which the water temperature averaged 21oC during February and increased to 23oC during March. However, no significant difference (P>0.05) in growth was observed between February (mean 115.9±25.6 g, n=150) and March (mean 120.0±19.5 g, n=150) culture period. When the water temperature increased to 26oC during May, a significant increase (P<0.05) in growth was observed (0.63 g/fish/d). During this period, the fish size ranged from 64-234 g with a mean of 150.7±33.4 g (n=150). During August 2005, one year old silver pomfret size ranged from 69-308g with a mean of 172.5±57.6g (n=150). The growth rate stabilized during the summer period from May to July and averaged to about 0.6 g/fish/d. With the onset of winter and with the declining temperature, the growth rate also declined to 0.26/fish/d during October.

Figure 3. Mean growth of Pampus argenteus during the period from August 2004 to October 2005 under tank grow-out culture conditions (males and females combined).

In general, the growth rate of fish in relation to the tank culture water temperature showed a curvilinear relation in which the fish growth rate declined with decreasing temperature and increased with the increasing temperature of up to 29.5-30.0 oC prevailed in the tanks during summer (Figure 5). After 14 months of culture period the fish size ranged from 74-315 g with a mean of 182.7±50.5 g (n=150).

Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 67

Figure 4. Mean daily weight gain of Pampus argenteus and the water temperature from August 2004 to October 2005 (males and females combined).

Figure 5. Growth rate relevant to daily weight gain observed in Pampus argenteus in relation to tank culture water temperature.

After 20 months of rearing period, the fish size ranged from 86-431 g with a mean of 184.4±64.6 g (n=150). Male and female size distribution of silver pomfret show that the males are smaller in size with reference to both individual body weight as well as forked 68 Sulaiman M. Almatar and Charles M. James length (Figures 6 and 7). The male individual body weight ranged from 86-259 g with a mean of 139.5±35.9 g (n=80) and the female weight ranged from 164-431 g with a mean of 254.6±55.5 g (n=53). The forked length for male ranged from 14.0-21.5 cm with a mean of 16.4±1.4 cm (n=80) and the female forked length ranged from 17.0-23.5 cm with a mean of 19.8±4.5 cm (n=53). The males dominated in the population and it constituted 60 %. The studies show that silver pomfret growth is fast in the initial period and it grows from 3.7 g size to an average of 81.9 g size within three months of culture period. The overall growth shows that the growth rate is significantly high (P<0.05) during summer and early part of winter when the water temperature is more than 26 oC. After 14 months of culture period fish weight reached up to 315 g with a mean of 182.76±69.4 g (n=150). The growth observed during the investigation carried out from August 2004 to October 2005 is considerably higher than the previous observations made on the same age group of silver pomfret, cultured at MFD from 1998-2003 project period, in which the mean weight per fish ranged 48.3-65.1 g (Cruz et al. 2000) and the maximum mean size obtained was 129.61 g.

70 18

72% 35% 16 60

Male 14 Female 50 26% 12

40 10 20% 17% 30 8

No of obs (Male) obs of No 6 20 obs of No (Female) 4 14% 10 6% 6% 2 2% 2% 0% 0% 0% 0% 0% 0% 0% 0 0 50 100 150 200 250 300 350 400 450 Weight (g)

Figure 6. Male and female body weight observed after 20 months of grow-out culture.

Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 69

30 14 32% 28 26% 26% 26 29% Male 12 Female 24 22 10 20 18 8 16 15% 15% 14 15% 6 12 11% 11% No of obs (Male) obs of No 10 No of obs (Female) obs of No 4 8 7% 6 4 2 2% 2% 2% 2% 2 1% 1% 1% 0% 0% 0% 0% 0% 0% 0 0 13 14 15 16 17 18 19 20 21 22 23 24 Length (cm)

Figure 7. Male and female forked length observed after 20 months of grow-out culture.

The considerable increase in the growth rate of silver pomfret in latter investigation, compared to previous years at MFD, is due to the changes made in the feed with feed additives (Almatar and James 2007) as well as feed management practices in which the feed was offered in trays instead of hand feeding as practiced during the earlier investigations. Wide size variations occur among the cultured silver pomfret, since the males are smaller in size compared to that of females. The results show that it is possible to obtain marketable size silver pomfret of over 250 g size after 20 months of culture period (about 1.8 years old). However, this depends on the sex ratio in the population. In general, the males dominated in the population constituting over 65% and their weight although reached up to 259 g, averaged at 139.47 g after 20 months culture duration. Whereas, the female size for the same age group was up to 424 g and averaged at 254.61 g showing that for commercial ventures it is important to select the females for grow-out farming. The difference in male and female size observed is similar to the data gathered on the growth of wild stocks of silver pomfret in Kuwaiti waters (Al-Hussaini et al. 2006). Furthermore, compared to the estimated age of 2.86 years for the wild silver pomfret to reach a marketable size of about 300 g in Kuwait (Al- Hussaini et al. 1998), the growth achieved under the tank culture conditions is encouraging and shows the fast growth of the fish within two years. The growth achieved in the culture tanks indicates that feed adequacy can support comparable good growth in the culture system. Temperature dependent growth of silver pomfret shows that there is a possibility to considerably increase the growth and reduce the growth period if the culture water temperature prevail 26-30oC throughout the year.

70 Sulaiman M. Almatar and Charles M. James

PATHOLOGY AND HEALTH MANAGEMENT

Pathology and health management was part of the investigations carried out over the years to maintain silver pomfret under tank culture conditions. During the early period of initiation of silver pomfret culture using 65m3 capacity outdoor tanks in 2000, serious mortalities were encountered. More than 90% of the infected fish in the culture tanks showed a distinctive swollen belly with skin hemorrhages. A few fish also exhibited slight eye haemorrhage and corneal opacity. In addition, exophthalmia was occasionally observed but only in late stages of the infection. Affected fish were lethargic and showed loss of appetite. Internal organs showed mild changes, including an enlarged liver and congestion in the kidney and spleen. The stomach and intestines contained a gelatinous or pus-like fluid. The investigations showed the presence of coccoid bacteria in the tissues. In addition, the high load of bacteria in the ascetic fluid and the acute pattern of mortality that peaked on day 4 after the initiation of symptoms further indicated an acute infection caused by Streptococcus agalactiae (Duremdez et al., 2004). The occurrence of this bacteria in cultured sea bream, Sparus auratus L., and wild mullet, Liza klunzingeri, in Kuwait has been reported previously by Evans et al. (2002). Duremdez et al., (2004) reported persistent infection of this bacterium in cultured silver pomfret. To avoid pathogenic bacterial infection of silver pomfret, from 2004 culture period onwards commercially available feed probiotics as well as water probiotics were used in the culture system. This helped to eradicate the incidence of mass mortalities of cultured silver pomfret due to pathogenic bacterial infection. Two species of ciliated protozoans, Cryptocaryon irritans and Uronema sp., were identified infesting silver pomfret. Cryptocaryon irritans infection was observed in October 1998 among the silver pomfret reared in 4m3 capacity indoor tanks. The parasite was detected in fish varying in size between 5 and 400g leading to mortalities in the range of 50-60%. The fish had mild to severe scale loss, pale foci on the skin, and excess mucus on the skin and gills. Most parasites were found on the gills but some were on the skin. Desalinated water baths (2ppt for 20 min) once a week were effective against the trophozoite stage of C. irritans, whereas baths in the combination of copper sulfate-citric acid solution (0.2mg/l) for seven days successfully controlled the theront stage. The transfer of the treated fish into clean tanks every three days greatly assisted in controlling the disease outbreak (Al-Marzouk et al., 2003). Another major disease problem encountered in the cultured silver pomfret was associated with scuticociliatosis by Uronema sp. The cultured silver pomfret juveniles and adults suffered 55-70% mortalities due to this parasitic infestation. Affected fish showed varying levels of tissue damage including severe epidermal and dermal necrotic lesions (Azad et al., 2009). The disease occurred with the raise in water temperature from 20 to 22oC during April. Loss of scales, appearance of bleached spots that coalesced to form brownish patches, haemorrhagic and severe dermal necrotic lesions were the major clinic-pathological manifestations. The parasite was found abundantly in the blood, peritoneal fluid and the cerebrospinal fluid, the skin and the gill wet mounts. Extensive fouling, necrotic degeneration of the gill epithelium and deep dermal necrosis resulted in mortality of the infected fish. The parasite was noticed in the lumen of the collecting ducts of the kidney and the alimentary canal. The parasite was also seen distributed extensively in the entire brain causing widespread nerve necrosis. Earliest separation of the clinically normal fish from the affected Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 71 fish resulted in significantly higher survival. The investigations on Uronema were of significant importance in view of the mariculture potential of this fish. One of the solution adapted to overcome this problem, was to feed the fish with formalin killed whole cell of Uronema with an objective of enhancing the immunity against this pathogen. With regular use of probiotics in the culture system and through nutritional manipulation using feed additives and tank management procedures, the occurrence of this parasitic disease was prevented in the silver pomfret grow-out culture since 2006.

DEVELOPMENT OF CULTURED BROOD STOCK

Attempts were made to develop cultured brood stock of silver pomfret from the hatchery produced juveniles from late 1990’s onwards. However, achieving cultured brood stock spawning in the tank was elusive over the years till 2006. From 1997 and 1998 hatchery production it was possible to raise 75 fish with an average body weight of 211.7g (ranged from 99 to 495g). These were kept in 65m3 capacity round fiberglass tanks. During 2000 culture period, the fish reached an average body weight of 370.5g and ranged from 156.6 to 693.5g. During the winter of 1999-2000 culture period, the brood stock were maintained in warm seawater of 24-25oC by mixing ambient seawater with ground well water. The brood stock selection and maintenance in brood stock holding tanks were continued without any spawning incidence till 2006. During these brood stock development period, studies were continued to observe the gonadal maturation of the fish under tank culture conditions as well as development of suitable diet to achieve spawning of the cultured fish.

Gonad Development in Cultured Brood Stock

In order to determine gonad development in cultured silver pomfret, histological studies were carried out on the gonad which indicated that silver pomfret is a gonochoristic species, in which the male and female sex exist in separate individuals (Al-Ablani and Lone, 2003). The studies show that the processes of sexual differentiation for the male and female are completed at the ages of 115 and 135 DAH, respectively. During these initial stages of brood stock development, gonad maturation in cultured silver pomfret was observed as it was evidenced by the occurrence of fully ripe male producing milt at a body weight of 134g and 17cm fork length on July 31, 1999 (age 2 years). However, female was found with stage 2 gonad only at the size of 222.5g in body weight and 19.5cm in fork length from the same batch of brood stock. Under the tank culture conditions, the matured males had oozing milt upon slight pressure of the abdomen (Plate 13). Except such observations in gonad development, spawning of the cultured brood stock was not achieved. Therefore, further attention was diverted toward developing brood stock diet and culture tank management practices.

72 Sulaiman M. Almatar and Charles M. James

Plate 13. Cultured silver pomfret male with oozing milt.

Brood Stock Feed Development

During the early stages of feed development for silver pomfret, from 2000 breeding season onwards, the brood stock’s diet was changed by increasing the fresh shrimp meat percentage in the diet and reducing the formulated feed percentage in addition to the inclusion of krill powder, squid meal and cod liver oil. However, no spawning was achieved till 2006 culture period. Since nutritional brood stock diet is mandatory to achieve spawning and good quality eggs in cultured silver pomfret, much attention was diverted towards developing a well balanced brood stock feed containing essential fatty acids, vitamin C and E, carotenoid pigments, micro-nutrients, probiotics and feed attractants. Table 3 shows the ingredients of brood stock diet used during 2006 spawning season. Considering the importance of essential fatty acids, especially the highly unsaturated fatty acids (HUFA) such as eicosapentaenoic acid (20:5ω3, EPA) and docosahexaenoic acid (22:6ω3, DHA) squid oil and cod liver oil in 1:1 ratio was used, as their requirements for marine fish were evidenced from 1980’s onwards (Watanabe et al., 1984; Fernandez-Palacocis et al., 1995). More recently Hossain et. al.(2010) have studied the seasonal variations of fatty acid composition of wild male and female silver pomfret for a period of one year (November 2007-October 2008). They demonstrated that the most abundant fatty acid in the whole body of both males and females was C16 followed by C18:1n-9 which account for 31-35% and 22- 24% respectively. The gonads from both sexes contained more than double the amount of EPA present in the liver but in the case of DHA it was more than three-fold higher in female gonad than male gonad indicating the importance of DHA in the development of the gonads silver pomfret. Krill was included in the diet since it enhances the feed intake and egg quality (Watanabe and Kiron, 1995). Astaxanthin was included in the silver pomfret brood stock diet since it increased the egg buoyancy and survival rate in red sea-bream, increased fertilization and survival rates of eggs and higher growth rates during the early feeding period of young salmonids (Sommer et al., 1991; Torrissen and Christiansen, 1995). By using this diet, a Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 73 breakthrough in natural spawning of two year old cultured brood stock of silver pomfret was achieved for the first time in 2006 spawning season (James and Almatar, 2007). Based on the success in spawning the silver pomfret cultured brood stocks, further improvement in the brood stock diet was made. During 2008 spawning season, in addition to commercially available salmon feed from ‘Dana’, Denmark, other feed additives were used (Table 4). Commercially available copepod under the name ‘Cyclopeeze’ from Argent Chemical Laboratories, USA was included in the feed composition, in addition to α- tocopherol (Vitamin E) and other feed ingredients. Feed was prepared by mixing all the ingredients along with formulated feed and re-pelletized using a meat grinder. Agar-agar was used as a binder.

BREEDING OF CULTURED BROOD STOCKS

The silver pomfret used for breeding originated from eggs collected from the wild spawners during July 2004. After 15 and 20 months of grow-out culture period, potential brood stock fish were selected from the grow-out tanks and stocked in two 125 m3 capacity out-door concrete tanks at a stocking rate of 3 fish/m3. Seawater was flowed through the tanks to maintain a water exchange rate of about 8-10 times a day. Ambient seawater mixed with ground well seawater, with a temperature of 24-26oC, were used to maintain the tank water culture temperature not to reach above 30oC during summer and below 20oC during winter. For handling the fish while sampling as well as during transfer from one tank to another, 3 ppm of the tranquilizer ‘Quinaldine’ (Argent Chemical Laboratories, USA) was used. The fish were fed daily 3 times at labidum. About two months before the spawning period, the potential broodstocks were measured and re-distributed in two 125m3 tanks. The sex ratio was about 1♀:6♂. More males were desired in the brood stock holding tanks, since males dominate and constitute about 65% in the natural wild stocks of silver pomfret during the spawning season (Almatar et al., 2004). The fish biomass was kept at less than 2 kg/m3 in the brood stock holding tanks. The fish were fed to satiation with brood stock diet using feed additives to enhance the gonad maturation (Table 4,5). A conical net with 400µm fine mesh was fixed at the tank water overflow channel in a submerged trough to collect the eggs in the brood stock holding tanks. Inspection for eggs was carried out between 1900-2000h as well as morning at 0730h. When eggs present, the collected eggs were washed from the suspended algae and other debris by using 1000 µm plastic mesh. The washed eggs were placed in 1liter capacity graduated measuring cylinders to quantify the floating (viable) and sunken (non-viable) eggs. The eggs were also examined under microscope to determine the egg fertilization.

74 Sulaiman M. Almatar and Charles M. James

Table 4. Feed Composition Used for the Brood Stock of Pampus argenteus During 2006 Spawning Period

Ingredients % Ingredients % Bio-Optimal 40.0 Binder 0.4 Lansy breed 30.0 Stabilized vitamin 0.2 Breed-S concentrate 10.0 Astaxanthin (Naturose) 0.2 Blood worm 10.0 Proburst-A** 0.2 Squid oil + Cod liver oil 5.0 Carpmin Forte* 1.0 Krill 3.0 *Supplied by APC Nutrients Pvt. Ltd., India. Contains minerals (mg/kg diet): Calcium 1500; Phosphorus 450; Mangnesium 11; Manganese 5; Zinc 11; ferrous 5; Copper 2; Cobalt 0.5; Sodium 10; Pottassium 10; Suphur 10; Iodine 1; Selenium 0.002; Molybdenum 0.001. ** Gut conditioner supplied by APC Nutrients Pvt. Ltd., India. Contains probiotics Lactobacillus and Yeast nutrilities.

Table 5. Brood Stock Feed Composition of P. argenteus (Spawning Period of 2008)

Ingredients % Ingredients % Dana 20.00 Proburst-A** 1.00 Gemma 25.00 Stabilized vitamin C 0.20 Lansy Breed 30.00 Cyclopeeze 0.10 Blood worm 12.00 Astaxanthin (Naturose) 0.20 Krill 5.00 Super-liv 0.30 Bio-max 0.50 Vitamin E 0.02 Carpmin Forte* 0.10 Binder 0.58 Squid oil + Cod liver oil 5.00 *Supplied by APC Nutrients Pvt. Ltd., India. Contains minerals (mg/kg diet): Calcium 1500; Phosphorus 450; Mangnesium 11; Manganese 5; Zinc 11; ferrous 5; Copper 2; Cobalt 0.5; Sodium 10; Pottassium 10; Suphur 10; Iodine 1; Selenium 0.002; Molybdenum 0.001. ** Gut conditioner supplied by APC Nutrients Pvt. Ltd., India. Contains probiotics Lactobacillus and Yeast nutrilities.

Natural Spawning of Cultured Brood Stock

The two years old brood stock size (male and female combined), stocked in two of the brood stock holding tanks, during May 2006 ranged from 128-457g with a mean of 261.7±88.55g (n=133). First natural spawning was observed on 15th June 2006, when the tank water temperature reached 26.5oC. The spawning continued till September and the peak spawning was observed during August with the increase of tank water temperature to 30oC (Figures 8, 9).

Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 75

Plate 14. Unfertilized eggs from first natural spawning of cultured brood stocks of silver pomfret in June 2006.

Figure 8. Incidence of natural spawning of the cultured broodstocks of silver pomfret during 2006 and 2007. 76 Sulaiman M. Almatar and Charles M. James

Figure 9. Total quantity of eggs collected from the natural spawning of the broodstocks from June untill October during 2006 and 2007.

During this spawning period, all the collected eggs were unfertilized (Plate 14). The spawning lasted till 15th of September. During 2007, the combined male and female brood stock size ranged from 130-675g with a mean of 294.3±139.09g (n=51). Natural spawning in the brood stock holding tanks initiated from 9 June onwards when the tank water temperature reached 27.5oC and the spawning continued till 5th of October. There was no spawning occurred during September (Figure 8). The quantity of eggs collected showed a maximum of 180.4ml eggs obtained during August 2006 and a maximum of 184ml eggs obtained during July 2007 (Figure 9).

Spawning incidence in D-1 and D-2 Tanks during 2006 80 31.0

Eggs 30.5 70 Temp 30.0 60 29.5 50 29.0

40 28.5

Eggs (ml) Eggs 28.0 30

27.5 Temperature (C) 20 27.0 10 26.5

0 26.0 Jun Jul Aug Sep Period (month)

Figure 10. Natural spawning of cultured broodstock in relation to tank water temperature during 2006. Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 77

Spawning in D-1 and D-2 in relation to temperature in 2007 90 30.5 Eggs 80 Temp 30.0 70 29.5 60

50 29.0

40 28.5 Eggs (ml) Eggs

30 Temperature (C) 28.0 20 27.5 10

0 27.0 Jun Jul Aug Sep Oct Period Figure 11. Natural spawning of cultured broodstock in relation to tank water temperature during 2007.

The quantity of eggs obtained per day varied from 3ml to 65ml during August 2006 and varied from 8ml to 78ml during July 2007 (Figure 8). During the 2006 and 2007 spawning periods the water temperature ranged from 27.5-30.5oC. Peak spawning was mostly associated with water temperatures of 29.0-30.0oC (Figure 10,11). During this natural spawning period, all the collected eggs from the brood stock holding tanks were unfertilized. The natural spawning of cultured brood stock originated from 2004 hatchery produced juveniles, continued through 2008 with no fertilized eggs. However in June 2009, some fertilized eggs with embryonic development and egg hatching was observed from the natural spawning of the cultured brood stock originated from 2005 and 2007 hatchery produced juveniles kept in a broodstock tank (Plate 15). This shows the possibility of obtaining fertilized eggs from natural spawning of cultured brood stock of silver pomfret, similar to other marine fish species.

Hormonal Induction of Cultured Brood Stock

During August 2007, induced spawning of the fish using hormones was initiated. The selection of females for hormone induction was based on the swelling of belly (Plate 16). For induced breeding of silver pomfret, lyophilized human chorionic gonadotrophin (HCG) was used at a dose of 1000-2000 IU/kg body weight of fish. The required HCG was procured under the brand name ‘Choriomon 5000 IU’ produced by IBSA Institute of Biochemique SA 6903, Lugano 3, Switzerland. Both female and males were injected in the morning between 0630-0700h (Plate 17). 78 Sulaiman M. Almatar and Charles M. James

Plate 15. Embryonic development and hatching of silver pomfret eggs obtained from natural spawning of cultured brood stock in June 2009.

Plate 16. Selection of cultured brood stock for hormonal induction. Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 79

Plate 17. Administration of HCG in cultured silver pomfret.

The injected fish were kept in two 3m3 capacity indoor hatchery tanks for observation and spawning. The tanks were provided with egg collection nets (Plate 18).

Plate 18. Egg collection tray with egg collection net fixed in the hatchery tank during hormone induction trials.

After the first injection a second dose was followed after 24h interval, if there is no egg development during the first injection. During 2008 spawning season, in addition to using HCG, the hormone LH-RH(a) procured from ‘Argent Laboratories’, USA, was used at 100 and 200µg/kg fish body weight. Two trials were carried out with 100µg/kg and one trial was carried out with 200µg/kg. Six trials were carried out using HCG. Table 6 shows the results obtained during the hormone induction trials. During the 2007 and 2008 spawning period, 24 80 Sulaiman M. Almatar and Charles M. James females administered HCG at 1 IU/g, completed egg development and the spawning percentage varied between 11.1% to 66.7%. During August 2008, administration of HCG at 1.5 IU/g in six females resulted in spawning of 50% of fish treated.

Table 6. Induced Spawning of Silver Pomfret during 2007 and 2008

Treatment Spawning Period ♀ Nos. Size (g) HCG (IU/g) LH-RH (µg/kg) No. % Aug ’07 1.0 - 3 437-537 2 66.7 Aug ’07 2.0 - 3 431-534 3 100.0 Aug ’07 2.0 - 6 386-472 2 33.3 Sep ’07 1.0 - 6 369-592 3 50.0 Jul ’08 1.0 - 9 483-749 1 11.1 Aug ’08 1.5 - 6 356-599 3 50.0 July ’08 - 100 6 466-700 2 33.3 Aug ’08 - 100 2 534-742 0 0.0 Aug ’08 - 200 1 415- 450 0 0.0

One trial using HCG at 2 IU/g August 2007 for three females each in two replicates resulted in egg development and spawning of two females after the second injection in the first tank. This was equivalent to 66% spawning. In the second tank three females were injected with HCG at 2 IU/g resulted in egg development and spawning of all the fish (100%). The results showed that 66-100% of females receiving HCG at 2 IU/g developed fully matured ovary and spawned. The ovary development and spawning was significantly low (P<0.05) in females receiving HCG at 1 IU/g, showing that administration of HCG at 2 IU/g fish body weight is effective in induced spawning of the silver pomfret. Normally the females after receiving the second injection were having fully developed ovary by 1500h and running eggs were observed before 1630h (Plate 19). During the trials, the females released the eggs naturally in the tanks between 1500-1530h without stripping. The eggs were not fertilized even though the males were present in the tanks at the time of spawning. In order to obtain fertilized eggs, females with running eggs were stripped as well as the males to obtain fertilized eggs. Stripping of these spawners during hormone induced breeding enabled to achieve fertilized eggs and hatching larvae (Plate 20). The results on the induced spawning of silver pomfret shows that it is possible to obtain fertilized eggs using HCG at 2 IU/g body weight rather than using it at 1 IU/g body weight for breeding the fish.

Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 81

Plate 19. Female with fully developed ovary after administration of HCG.

Plate 20. Hatching of larvae from hormone induced breeding.

The investigations also show that during induced spawning, females could release the eggs naturally in the holding tank however the eggs were not fertilized due to the inactive males. The results showed that stripping the males and females during induced spawning ensure fertilization of the eggs and hatching of larvae. Further investigations are required to improve the egg fertilization and hatching rates as well as in enhancing the milt production in male. The research carried out over the years till to date on the production and breeding of silver pomfret has achieved the following:

The research has paved the way in developing hatchery larval rearing techniques for this economically important new candidate species for aquaculture; Current hatchery procedures based on egg collection from wild spawners for mass production of fingerlings; Present grow-out production and growth studies for this species are based on tank culture system and it shows the possibility of achieving marketable size fish within 20 months of culture period under Kuwait’s environmental conditions; 82 Sulaiman M. Almatar and Charles M. James

Temperature dependent growth of silver pomfret shows that there is a possibility to increase the growth rate and reduce the growth period, if the culture water temperature prevail 25-30oC; The studies show the possibility to achieve natural spawning of the cultured brood stocks under tank culture conditions; and The studies show the possibility of hormone induced breeding of cultured silver pomfret that shall pave the way for mass production of fertilized eggs.

CHALLENGES TO RESOLVE

The overall objective should be refinements of techniques towards production of large quantities of fertilized eggs either through natural spawning of the cultured brood stocks or through hormonal induction that could be applicable for commercial hatchery operation. Mass production of fertilized eggs to obtain newly hatched larvae is constrained by inadequate milt production in the cultured males, availability of less number of females in the population for spawning as well as low fertilization and egg hatching rates. Attention should be diverted to resolve these issues through enhancement of brood stock feed, ensuring the availability of DHA and other essential nutrients in the feed to improve the condition factor of the cultured brood stocks. Further investigations also should focus on cryopreservation of milt for achieving egg fertilization during spawning. Studies also should focus on evaluating other commercially available hormones for induced spawning of the fish to achieve optimum egg production. The considerable improvement in the growth of cultured silver pomfret is due to the changes made in the feed with feed additives (Almatar and James 2007) as well as feed management practices in which the feed was offered in trays instead of hand feeding. Further refinements in formulated feed is required to enhance the growth rate of juveniles under grow-out culture conditions. This include application of feed probiotics, immune-stimulants and growth promoters in the feed. The grow-out production trials carried out so far was based on land-based tank culture system for this species. Current studies focus on using recirculation aquaculture systems (RAS) to overcome the winter effect in Kuwait as well as to achieve maximum production in unit space and time. Since conventional commercial aquaculture ventures use sea-cages for the production of desirable species for grow-out production, it is required to study the growth of this species under such culture conditions. Considering the high growth of females in the population, further research is required to assess the possibility of sex reversal in silver pomfret to obtain all females through genetic manipulation (Mair et al. 1997), environmental stress (Abucay et al. 1999) and hormonal induction (Nakamura et al. 2003; Bhandari et al. 2005).

Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 83

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Abucay, J.S., Hair, G.C., Skiniski, D.O.F. and Beardmore, J.A.B. (1999). Environmental sex determination: the effect of temperature and salinity on sex ratio in Oreochromis niloticus L. Aquaculture, 173, 219-234. Al-Abdul-Elah, K.M., Almatar, S., Abu-Rezq, T. and James, C.M. (2001). Development of hatchery technology for the silver pomfret Pampus argenteus (Euphrasen): effect of microalgal species on larval survival. Aquaculture Research, 32, 849-860. Al-Abdul-Elah K.M., Almatar S., Abu-Rezq, T., James,C.M. and El-Dakour, S.( 2002). Development of hatchery techniques for the silver pomfret Pampus argenteus (Euphrasen). Asian Fisheries Science, 15, 107-122. Al-Abdul-Elah, K., El-Dakour, S., Almatar, S. M., Abu-Rezq T. and Ghaffar, A.R.A.(2003). Final Report, Culture of Zobaidy, Pampus argenteus, in Kuwait, Phase I. Volume III: Preliminary Larval Rearing Studies and Development of Reared Broodstock. Aquaculture, Fisheries and Marine Environmental Department, Food Resources and Marine Sciences Division, Kuwait Institute for Scientific Research, Kuwait. KISR 6910. Al-Ablani, S. and Lone, K. P.( 2003).Final Report, Culture of Zobaidy, Pampus argenteus, in Kuwait, Phase I. Volume IV: Study of Gonadal Differentiation of Fry, the Annual Reproductive Cycle in Wild Zobaidy and Induced Spawning of Sexually Mature Fish. Aquaculture, Fisheries and Marine Environmental Department, Food Resources and Marine Sciences Division, Kuwait Institute for Scientific Research, Kuwait. KISR 6910. Al-Hussaini, M., Al-Baz, A., Al-Ayoub,S., Dasti, J. and Al-Jazzaf, S.(1998). “Establishment of a regional Fish Aging Laboratory (FAL) in Kuwait”. Kuwait Institute for Scientific Research, Report No. KISR 5276, pp.89. Al-Hussaini, M.( 2003). Fishery of shared stock of silver pomfret, Pampus argenteus, in the Northern Gulf: A case study. In: Norway-FAO Expert Consultation on the Management of Shared Fish Stocks, Bergen, Norway, 7-10 October 2002. FAO Fisheries Report No. 695, Supplement. http://www.fao.org/DOCREP/006/Y4652E/y4652e05.htm#bm05, retrieved on: 10/12/2003. Al-Hussaini, M., Marammazi, J., Al-Baz, A., Al-Ayoub, S., Chen, W., Eskandari, G., Ansari H., Safikhani, H., Al-Jazzaf S., Dashti, T., Al-Sabah, I., Taqi, A. and Murrad, H. (2006). “Stock assessment of zobaidy, Pampus argenteus in the Northern Gulf. Final Report FM039C”. Kuwait Institute for Scientific Research, Kuwait. Pp.94. Al-Marzouk, A., Fernandez, R. and Al-Gharabally, H.(2003). Final Report, Culture of Zobaidy, Pampus argenteus, in Kuwait, Phase I. Volume VII: Fish Health Management. Aquaculture, Fisheries and Marine Environmental Department, Food Resources and Marine Sciences Division, Kuwait Institute for Scientific Research, Kuwait. KISR 6910. Almatar, S., Al-Abdul-Elah, K. And Teng, S. K. (1998). Culture of Zobaidy, Pampus argenteus, in Kuwait – Phase I. Kuwait Institute for Scientific Research, Report No. KISR 5254. Almatar, S. M., Al-Abdul-Elah, K. and Abu-Rezq, T. (2000). Larval developmental stages of laboratory-reared silver pomfret, Pampus argenteus. Ichthological Research, 47, 137- 141. Almatar, S. M., Al-Abdul-Elah, K., Al-Ablani, S., Cruz, E., Abu-Rezq, T., Al-Marzouk, A., Lone, K. and Fernandez, R. (2003). Final Report, Culture of Zobaidy, Pampus argenteus, 84 Sulaiman M. Almatar and Charles M. James

in Kuwait, Phase I. Volume I: General Introduction, Executive Summary, Conclusions and Recommendations. Kuwait Institute for Scientific Research, Kuwait. KISR 6910. Almatar, S.M., Lone, K.P., Abu-Rezeq, T. and Yousef, A.A.( 2004). Spawning frequency, fecundity, egg weight and spawning type of silver pomfret, Pampus argenteus (Euphrasen) (Stomateidae), in Kuwait waters. Journal of Applied Ichthyology, 20, 176- 188. Almatar,S.M. and James, C.M.( 2007). Performance of different types of commercial feeds On the growth of juvenile silver pomfret, Pampus argenteus, under tank culture conditions. Journal of the World Aquaculture Society, 38,550-556. Azad, I.S., Al-Marzouk, A. and Khalid Abdul-Elah, M. (2009). Development and evaluation of formalin killed whole cell of Uronema sp., as a vaccine against scuticociliatosis in sobaity. Kuwait Institute for Scientific Research, Kuwait. KISR 9922. Bhandari, R.K., Alam, M.A., Higa, M., Soyano, K. and Nakamura, M. 2005. Evidence that estrogen regulates the sex change of honeycomb grouper (Epinephelus merra), a protogynous hermaphrodite fish. Journal of Experimental Zoology A. Comp. Exp. Biol., 303, 497-503. Cruz, E.M., Almatar, S., Abdul- Elah, K. and Al-Yaqout, A. (2000). Preliminary studies on the performance and feeding behavior of silver pomfret (Pampus argenteus (Euphrasen) fingerlings fed with commercial feed and reared in fiberglass tanks. Asian Fisheries Science, 13,191-199. Cruz, E. M., Almatar, S. M. and Al-Sabbah, I. (2003). Final Report, Culture of Zobaidy, Pampus argenteus, in Kuwait, Phase I. Volume V: Preliminary Study of the Growth Performance and Feeding Behavior of Zobaidy Reared in Tanks. Aquaculture, Fisheries and Marine Environmental Department, Food Resources and Marine Sciences Division, Kuwait Institute for Scientific Research, Kuwait. KISR 6910. Dadzie, S., Abou-Siedo, F. and Al-Qattan, E.(2000).The food and feeding habits of the silver pomfret, Pampus argenteus (Euphrasen), in Kuwait waters. Journal of Applied Ichthyology, 16, 61-67. Duremdez, R., Al-Marzouk, A., Quasem, J.A., Al-Harbi, A. and Gharabally, H. ( 2004). Isolation of Streptococcus agalactiae from cultured silver pomfret, Pampus argenteus (Euphrasen), in Kuwait. Journal of Fish Diseases 27,307-310. Evans J.J., Klesius, P.H., Gilbert, P.M., Shoemaker, C., Al-Sarawi, M., Landsberg, J., Durumdez, R., Al- Marzouk, A. and Al-Zenki, S. 2002. Characterization of β-haemolytic Group B Streptococcus agalactiae in cultured seabream, Sparus auratus and wild mullet, Liza klunzingeri (Day) in Kuwait. Journal of Fish Diseases 25: 505-513. Fernandez-Palacios, H., Izquierdo, M. S., Robaina, L., Valencia, A., Salhi, M. and Vergara, J. M. 1995. Effects of n – 3 HUFA level in broodstock diets on egg quality of gilthead seabream (Sparus auratus L.). Aquaculture, 132, 325-337. Haedrich, R. L. (1967). The stromateoid fishes: Systematics and classification. Bulletin of theMuseum of Comparative Zoology, 135, 31-39. Hossain, M. A., Almatar, S.M., James, C.M., Al-Yaqout, A. and Yaseen, S.B. (2010). Seaonal variation in fatty acid composition of silver pomfret, Pampus argenteus (Euphrasen) in Kuwait waters. Journal of Applied Ichthyology. DOI: 10.1111/J-1439, 1- 7. Breeding the Silver Pomfret, Pampus argenteus (Euphrasen) for Aquaculture 85

James, C.M. and Almatar,S.M. (2007). A breakthrough in the spawning of domesticated Silver pomfret. Aquaculture Asia Pacific, 3 (1), 26-28. Mair,G.C., Abucay, J.S., Skibinski, D.O.F., Abella, T.A. and Beardmore,J.A. (1997). Genetic manipulation of sex ratio for the large scale production of all male tilapia Oreochromis niloticus L. Canadian Journal of Fisheries and Aquatic Sciences, 54, 396-404. Nakamura, M., Ramji, K.B. and Higa, M. (2003). The role of estrogens play on sex ratio in Oreochromis niloticus L. Aquaculture, 173,219-234. Oda, T. and Namba, Y. (1982). Attempt to artificial fertilization and rearing of larvae of silver pomfret, Pampus argenteus. Bulletin of Fisheries Experimental Station, Okayama Prefecture, 1981, 195-197. Pati. S. (1984). Possibilities of aquaculture of silver pomfret, Pampus argenteus (Euphrasen) along the Balasore coast. Proceeding of the Symposium on Coastal Aquaculture, India, 782-786. Sommer T.R., Potts, W.T. and Morrissy, N.M. (1991). Utilization of microalgal astaxanthin by rainbow trout (Oncorhyncus mykiss). Aquaculture, 94,79-88. Tang, W.C. (1987). Chinese medicinal materials from the sea. Abstracts of Chinese Medicine1(4), 571-600. Torrissen, O.J. and Christiansen, R. (1995). Requirements of carotenoids in fish diets. Journal of Applied Ichthyology, 11,225-230. Watanabe T., Arakawa T., Kitajima C. and Fujita S. (1984). Effect of nutritional quality of broodstock diets on reproduction of red sea bream. Bulletin of Japanese Society of Scientific Fisheries 50, 495-501. Watanabe, T. And V. Kiron. (1995). Broodstock management and nutritional approaches for quality offsprings in the Red Sea Bream. In: Bromage, N.R., Roberts R.J., (Eds.), Broodstock Management and Egg and Larval Quality. Cambridge University Press,

Chapter 7

SOME METOCEAN ASPECTS FOR THE SELECTION OF SUITABLE MARICULTURE SITES IN THE ARABIAN GULF

S. Neelamani∗ Coastal and Air Pollution Department, Environment and Urban Development Division Kuwait Institute for Scientific Research Safat, Kuwait

ABSTRACT

Selection of suitable sites for marine aquaculture activity is very important. The site selection is based on many aspects like the wave climate, current intensity, tidal variation, quality of marine water, possibility for better flushing of the ambiant water, water temperature and salinity, influence of the discharges from power , desalination and municipal wastes, ease of accessibility of the aquaculture cage, ease of availability of suitable manpower, machines, materials, electric power etc. The catch of different types of wild fishes from the Arabian Gulf water is not sufficient to meet the requirements of the populations living around the Gulf. Hence, most of the Arabian Gulf countries import significant percentage of the fish requirements. Developments of Mariculture in the Arabian Gulf may reduce the dependency of the import of fish varieties. The mariculture must be economical, efficient and pollution free. It is hence essential to select suitable sites from different influencing environmental aspects. This paper describes the main environmental parameters of the Arabian Gulf, the ways to use the marine power for aeration and other purposes of the aquaculture activities, techniques for reducing the wave and current induced forces on the cages and mooring lines which will help in reducing the cost of installation of aquaculture systems.

∗ Phone : +965 2498 9770, Fax : +965 2498 9759, Email : [email protected] 88 S. Neelamani

INTRODUCTION

Aquaculture is nothing but the raising and harvesting of fresh and saltwater plants and animals. The most economically important form of aquaculture is fish farming, an industry that accounts for an ever increasing share of world fisheries production. Formerly a business for small farms, it is now also pursued by large agribusinesses, and by the early 2000s it had become almost as significant a source of fish as the wild fisheries (Columbia Encyclopedia, 2008). Successful aquaculture takes into consideration the biology of the aquatic species (feeding, water flow and temperature needs, disease prevention) and engineering design (water source and water quality study, pond and tank containment systems, water filtration and aeration) as well as issues pertinent to any business. Common products of aquaculture are catfish, tilapia (St. Peter's fish), trout, crawfish, oysters, shrimp, and salmon, and tropical fish for aquariums. Some are raised in huge freshwater tanks or ponds; others require the running water of rivers or streams. Saltwater species are often raised in saltwater ponds, in enclosed bays, or in pens placed in coastal or deeper sea waters. There are potential environmental problems associated with aquaculture. Most of the fish that are raised are genetically altered or hybridized for quick growth. If they escape into the wild, they compete against and can crowd out smaller or less voracious native fish. Confined fish can become a breeding ground for diseases or pests, which can be transmitted in some cases to wild fish. In addition, the large amounts of water that are used in aquaculture become laden with fish feces and unconsumed food that, if not removed through treatment or used as agricultural fertilizer, can add injurious amounts of nitrogen and phosphorus to a river or stream when the water is returned to it. Development of improved recirculating-tank technologies, however, may lead to a reduction in such pollution threats, as well as the spread of aquaculture to areas where large volumes of water are not available in the environment. The practice of aquaculture dates back to 1000 BC in China. It is growing worldwide, in part in response to overfishing and the deterioration of the world's fisheries and concerns about the effects of pollution on seafood. In the United States, aquaculture is also a response to the increased demand for fish and shellfish as a result of changes in the nation's eating habits. Cattle require 8-10 pounds (3.6- 4.5 kg) of feed per pound of live weight. Poultry require 3 pounds (1.4 kg) of feed per pound of live weight. Fish, because they are poikilothermic ("cold-blooded"), only require 2 pounds (0.9 kg) or less of feed per pound of live weight. No energy is required to maintain body temperature. This is one of the motivations for increase in aquaculture activity worldwide. The design and development of effective aquacultural systems for marine and freshwater facilities is one of the scientific requirements for successful aquacultural activities. A basis understanding of marine environments is necessary for selection of suitable sites and cost effective design of aquaculture facilities. Presence of ranges of magnitudes of waves, currents, winds etc are beneficial as well as problem for the aquacultural activities. The design of cages in the open sea is mainly governed by extreme wave activities Neelamani et al. (2007). Many different types of cages are used for growing fish in the sea but within a control volume (Figures 1 to 3). Most of the cages have the frame works made out of load bearing members like steel members covered by porous skins, which are made out of polyethylene or nylon wires woven with suitable pores to suit the size of the fish planned to be raised inside the cage. Some Metocean Aspects for the Selection of Suitable Mariculture Sites … 89

Figure 1. Dome type cage.

Figure 2. Submerged cone type cage.

The cage themselves experience loads due to the action of waves and currents and handling loads. The cages are relatively retained in position using systematic mooring arrangements. Single point mooring (Figure 4) is widely used. However, multipoint moorings may be required when the size of the cages is becoming larger and the environmental loads due to waves and currents are higher. This paper highlights the marine environmental conditions of Arabian Gulf like waves and currents which influence the aquaculture activities. Also ideas to protect the aquaculture systems from marine environmental forces and the ways of converting the wave energy into aeration of aquaculture ponds are provided.

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Figure 3. Exposed circular shaped cage.

Figure 4. Typical single point mooring arrangement of a cage. Some Metocean Aspects for the Selection of Suitable Mariculture Sites … 91

MARINE ENVIRONMENTAL CONDITION OF ARABIAN GULF

The Arabian Gulf (Figure 5), a marginal sea in a typical arid zone, is an arm of the Indian Ocean. It lies between the latitude of 24o -30o N. The gulf covers an area of 226,000 square km. It is 990 km long and its width ranges from 56 to 338 km. It has a total volume of 7000 to 8400 km3 of seawater (Emergy (1956), Pursar and Seibold (1973), El-Gindy and Hegazi (1996)).

Figure 5. Arabian Gulf (Source: Google Earth).

The entire basin lies upon the continental shelf. The average water depth of the Arabian Gulf is about 35.0 m. But depths more than 107 m occur in some places. The gulf's water depth increases in the south east direction. The Gulf is connected to the Gulf of Oman and the Arabian Sea through the Strait of Hormuz, which is 56 km wide and with an average water depth of 107 m and allows water exchange between the Arabian Gulf and Arabian Sea. Further details of the Oceanographic Atlas of Arabian Gulf can be obtained from Al- Yamani et al. (2004). In the Arabian Gulf, in general the dominant wind direction is northwesterly (Elshorbagy et al. (2006)).

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Figure 6. Locations in the Arabian Gulf waters for extreme wave analysis.

Design, Significant Wave Height and Mean Wave Period for Aquaculture Cages in the Arabian Gulf

Safe and optimal design of the structure components of aquaculture cages in the Arabian Gulf need the extreme wave information like extreme significant wave height and the corresponding mean wave period. The extreme wave analysis is carried out for a total of 38 different locations in the Arabian Gulf as shown in Figure 6. The longitude, latitude and the water depth of each location is given in Table 1. Detailed extreme wave analysis is carried out for all these locations (Neelamani et al. (2007)). The probable extreme significant wave height for different return periods are shown in Figure7. Also, a plot showing the predicted extreme significant wave height for 100 year return period in the Arabian Gulf at different locations is given in Figure 8 for quick reference.

Some Metocean Aspects for the Selection of Suitable Mariculture Sites … 93

Table 1. Longitude, Latitude and local water depth at 38 different locations in the Arabian Gulf waters

Location Longitude Latitude Water depth Remarks/Nearest Country

(oE) (oN) (m) 1 49.2 29.9 15 Iran 2 49.1 28.1 15 Saudi Arabia 3 49.6 27.5 15 Saudi Arabia 4 53.4 26.7 61 Iran 5 54.9 26.5 11 Iran 6 55.9 26.6 31 Iran 7 54.0 26.4 55 Iran 8 48.7 28.2 9 Saudi Arabia 9 49.9 26.9 16 Saudi Arabia 10 50.8 26.4 12 Bahrain 11 51.8 25.7 19 Qatar 12 51.9 24.4 10 UAE 13 52.9 25.2 16 UAE 14 54.4 24.7 10 UAE 15 55.2 25.3 16 UAE 16 55.9 25.9 20 UAE 17 50.9 26.2 9 North west of Qatar 18 50.6 25.4 17 South west of Qatar 19 50.3 25.9 20 In between Saudi Arabia and Bahrain 20 49.3 27.6 9 Saudi Arabia 21 48.8 29.8 10 In between Kuwait-Iran 22 49.2 29.2 33 In between Saudi Arabia-Iran 23 49.7 28.6 45 In between Saudi Arabia-Iran 24 50.2 27.9 48 In between Saudi Arabia-Iran 25 50.8 27.3 62 In between Bahrain-Iran 26 51.5 26.7 39 In between Qatar-Iran 27 52.2 26.2 44 In between Qatar-Iran 28 53.2 25.8 54 In between UAE-Iran 29 54.4 25.8 59 In between UAE-Iran 30 55.5 26.3 57 In between UAE-Iran 31 52.4 27.2 79 Iran 32 51.6 27.6 22 Iran 33 50.9 28.4 42 Iran 34 50.4 28.9 44 Iran 35 49.9 29.7 24 Iran 36 48.7 29.1 19 Kuwait 37 52.0 25.3 15 East of Qatar 38 53.4 24.9 20 UAE

94 S. Neelamani

Figure 7. Predicted extreme significant wave heights in the Arabian Gulf waters for different return periods based on Weibull distribution.

Figure 8. Predicted extreme significant wave heights for 100 year return periods in the Arabian Gulf waters. Some Metocean Aspects for the Selection of Suitable Mariculture Sites … 95

In general the extreme waves on the territorial waters of Kuwait, Saudi Arabia, Bahrain, Qatar and UAE are smaller compared to the Iran's territorial waters and in the Arabian Gulf midway between the longitudinal boundaries of both the sides. If we consider the whole Arabian Gulf, then the predicted 100 year significant wave varies from 2.2 m (in the Saudi Arabian territorial waters) to 7.0 m (midway between UAE and Iran). Even on the longitudinal direction of the Arabian Gulf along its midway, the 100 year return period ways are of the order of 5 m in the Northern part of the Gulf and is about 6.0 to 7.0 m in the southern part of the Gulf. This could be due to the higher water depths and longer fetch length available for the southern part of the gulf for the North West winds. Design of aquaculture cages around these locations need to consider these points for safe and economic designs. The territorial waters off UAE coast, the 100 year return period significant waves are of the order of 5.0 to 5.5 m. The complete picture of the predicted extreme waves for different return periods in the Arabian Gulf can be used for economic and safe design of the cages. The wave periods are also very essential for the design. This is because, the dynamic response of the cages depends on the wave periods. It is advisable to design the cages so that they do not encounter resonance, especially during extreme wave actions. The mean wave period and the significant wave heights are correlated. A typical plot showing the relationship between the significant wave height and mean wave period for location 23 is provided in Figure 9. The best fit polynomial equation and the coefficient of regression is given in the plot. For all the 38 locations in the Arabian Gulf, similar exercise is carried out to obtain the mean wave periods for different return periods, viz. 12, 25, 50, 100 and 200 years and the mean wave period obtained is provided in Figure 10. It can be seen that the mean wave period range from 4.5 s to 8.1 sec when all the locations and all the return period range of 12 to 200 years are considered together.

Figure 9. Relationship between the mean wave period and significant wave height for location 23 in the Arabian Gulf. 96 S. Neelamani

Figure 10. The predicted mean wave period for significant wave height obtained based on Weibull for 12, 25, 50, 100 and 200 year return periods.

In fact, one can see that for a selected location, the difference between the mean wave period for 12 year return period and 200 year return period is only of the order of 0.5 sec, where as the location has very significant effect on change of Mean wave period. For example, for location 8 (Saudi Arabian territorial waters), the mean wave period is in between 4.5 and 5 sec for return periods in the range of 12 to 200 years, whereas for location 28 (Offshore in between UAE and Iran), the mean wave period is in between 7.5 and 8 sec for return periods in the range of 12 to 200 years. This aspect is very important in the design of ocean structures which are very sensitive for wave periods (Like the wave transmission characteristics of floating breakwater, which is very sensitive for wave period). For clarity and quick reference, Figure 11 is provided, which shows the mean wave period at different locations in the Arabian Gulf for 100 year return period event.

Tide Induced Currents in the Arabian Gulf

The magnitude of currents induced by the tidal variations at any location in the Arabian Gulf is needed in the selection of location for installing the aquaculture cage. High currents are beneficial for removing the wastes generated by the aquaculture activities like drifting the residual feeds and excreta of fish and for self cleaning of cage surroundings. However, high current causes significant forces on the cage and mooring lines. A detailed study by Rakha et al. (2006) shows the maximum tidal current at different locations in the Arabian Gulf. The northern part of the Arabian Gulf in Kuwaiti territorial water, north-western part of Qatar, and the entrance of Arabian Gulf have currents of the magnitude 0.7 m/s and more (Figure 12). Mooring systems and the porous nets covering the steel members of the cages need to be designed for such current velocities in these locations. Some Metocean Aspects for the Selection of Suitable Mariculture Sites … 97

Figure 11. Mean Wave Period in the Arabian Gulf for 100 Year Return Period.

Figure 12. Maximum Tidal Currents for the Arabian Gulf (Rakha et al., 2006). 98 S. Neelamani

Tidal Fluctuations in the Arabian Gulf

Rakha et al. (2006) has carried out a detailed study on the tidal variation in the Arabian Gulf. The highest tidal variation in the Arabian Gulf occurs at the northern part of the Gulf (Figure 13). This means that the cage has to move up and down by 3.0 to 4.0 m. Though this is not an issue in the design of cage itself, but it is necessary for the design of the mooring arrangements. Enough slack in the mooring line must be provided to take care of the vertical excursions.

Figure 13. Maximum Range in Water Level for the Arabian Gulf (Rakha et al. 2006).

Protection of Aquaculture Cages against Severe Wave Forces and Aeration using the Marine Wave Energy Cages installed at locations, where the design significant wave height is less than say 3.0 m needs no additional protection against wave induced forces. However, locations offshore of UAE, where the 100 year return period significant wave can exceed 6 to 7 m, it is advisable to go for structural protection of the cages. These are all floating breakwaters and they have systems to convert wave energy into pneumatic power. This concept, called mighty whale is already tried in countries like Japan (Figure 14) and the results are encouraging. The locally available wave energy is used to aerate the fish ponds and fish cages to increase the oxygen level in the water and hence creating a healthy environment for the fish growth. There are many merits in this proposal. Wave power can be used to compress air in chambers and use them for aeration of fish ponds (Figure 15). Waves of 1.0 m height and 8.0 Sec periods have about 4.4 kW of power per m width of the coast and hence, the power can be generated and used for various activities of the cage culture. Some Metocean Aspects for the Selection of Suitable Mariculture Sites … 99

Figure 14. The concept of aeration of fish ponds using array of floating wave power structure, called Might Whale, the Japanese Concept.

Figure 15. Schematic sectional view of the Floating OWC wave barrier for supply of air for aeration of fish cage and also for reducing the waves around the cage area.

The floating wave energy caisson also protects the aquaculture cages against severe wave attacks (Figure 16). The wave transmission of less than 20% can be achieved by proper design of the floating wave power caisson (See Figure 17). 100 S. Neelamani

Figure 17. Transmission coefft. as a function of relative width of caisson.

In Figure 17, 'B' is the width of the floating breakwater, 'L' is wave length and Kt is the wave transmission coefficient, which is defined as the ratio of transmitted wave height to the incident wave height. In the Arabian Gulf most of the waves occur with wave length of 30 to

40 m. For Kt of 0.2, the B/L value is about 0.2, and hence width ‘B’ of about 6 to 8 m of the floating breakwater will do. Hence for a design wave of 5.0 m, the transmitted wave will be about 1.0 m and hence significant amount of investments can be saved in the design of the fish cage and the mooring arrangements.

CONCLUSION

Appropriate selection of locations for installing the cages for marine aquaculture is one of the important criteria for the success in this business. The extreme wave activity governs the strength and size of components of the cages and mooring systems. The design physical marine environmental conditions like extreme waves, high currents and tidal variations in the Arabian Gulf are revealed in this article. The offshore waters of UAE experience waves more than 6.0 m for 100 year return period. Hence cages at these locations must be stronger than that in the Kuwaiti territorial waters, where 100 year return period waves are in the range of 3 to 4 m only. High tidal variations, with tidal fluctuations of up to 4.0 m and above occur in the northern part of Arabian Gulf and hence mooring arrangements should have enough slacking in order to take care of the vertical excursions of the cages without causing undue tensions in the mooring lines. High currents of the order of more than 0.7 m/s are at locations around the northern part of the Arabian Gulf in Kuwaiti territorial water, northwestern part of Qatar, and the entrance of Arabian Gulf. Mooring systems and the porous nets covering the steel members of the cages need to be designed for such current velocities in these locations. The merits of these high currents for Some Metocean Aspects for the Selection of Suitable Mariculture Sites … 101

natural drifting the disintegrating residual feeds and excreta of fish and for self cleaning of cage need to be appreciated though high current causes significant forces on the cages and mooring lines. The natural wave energy available at different locations can be used for aeration purposes at the expense of placing floating wave energy breakwaters and the merits of force and stress reduction on the cage structures need to be recognized. The factual physical oceanographic information provided in this manuscript will be of use for selection of suitable locations in the Arabian Gulf for cage culture installations.

ACKNOWLEDGMENTS

The author thanks Kuwait Foundation for Advancement of Science for sponsoring the projects, from where the results of some of the figures are used. The author is thankful for Kuwait Institute for Scientific Research, Kuwait for providing all the infrastructure facilities to carry out this work. The author is grateful o his college Dr. Karim Rakha for permitting to use the results of his studies on tides and currents.

REFERENCES

Al-Yamani, F.Y., Bishop, J., Ramadhan, E., Al-Husaini, M. and Al-Ghadban, A. (2004). Oceanographic Atlas of Kuwait's Waters, Kuwait Institute for Scientific Research, Kuwait, 203 pp. Columbia Encyclopedia, Sixth edition, 2008. El-Gindy, A. and Hegazi, M. (1996). Atlas on Hydrographic Conditions in the Arabian Gulf and the Upper Layer of the Gulf of Oman, University of Qatar, 170 pp. Elshorbagy, W., Azam, M.H. and Taguchi, K. (2006). "Hydrodynamic Characterization and Modeling of the Arabian Gulf", Journal of Waterway, Port, Coastal and Ocean Engineering, ASCE, 132 (1), 47-56. Emery, K.O. (1956). Sediments and Water of the Persian Gulf, Bull. Amer. Ass. Petrol. Geol., 40 (10), 2354-2383. Neelamani, S., Al-Salem, K. and Rakha, K. (2006). Extreme Waves for Kuwaiti Territorial Waters, Ocean Engineering, Pergaman Press, UK, 34 (10), 1496-1504. Purser, B.H., and Seibold, E. (1973). The Principal Environmental Factors Influencing Holocene Sedimentation and Diagenesis in the Persian Gulf. In: "Persian Gulf", Purser, B.H. (ed), Berlin, pp.1-9. Rakha, K., Al-Salem, K., Neelamani, S., Al-Banaa, K. Al-Nassar, W., Al-Ragum, A., Al- Gamily, H., and Al-Othman, A. (2006). Interactive coastal information system for Kuwait’s territorial waters, Phase I: Hindcasting of waves, water levels, and currents. Kuwait Institute for Scientific Research, EC026C. Final Report KISR 8568.

Chapter 8

INDUSTRY PERSPECTIVE OF AQUACULTURE IN THE MIDDLE EAST - STATUS AND ISSUES

C. Regunathan∗ Project Manager, Al-Oula Marine Consulting Company, Kuwait

ABSTRACT

Aquaculture in the Middle East and North Africa is picking up momentum with many Government initiatives. Several countries have a subsidy scheme for different investments in the field of aquaculture. Middle East countries such as Bahrain, Oman, Saudi Arabia, UAE and Yemen have gained momentum. Iran too has been vigorously working towards achieving growth in this food sector. Though being a pioneer in the field of aquaculture research (Kuwait Institute for Scientific Research), Kuwait has lagged behind in the process of commercialization of the aquaculture production sector, mostly due to the lack of interest among the private investors. This chapter is aimed at giving an overview of the aquaculture activity in the Middle East and the industry perspective of the sector.

INTRODUCTION

Increasing World population has raised the demand for food, including aquatic ones. Meanwhile, the capture fisheries production, which was the major supplier, has leveled off globally for some years, now at about 90-100 million metric tons (mmt) and recorded 92 mmt in 2006 (FAO, 2009). Sustainability issues do not allow further intensification of fishing in these areas. The problem is further exacerbated by both anthropogenic (overfishing, bycatch, pollutants, habitat destruction, damming, poaching, piracy) and natural influences (harmful algal blooms, global warming). Presently, aquaculture has been found the best alternative to fill the gap between supply and demand for both food (fishes, crustaceans, molluscs, seaweed) and non-food (ornamental

∗ E-mail: [email protected] 104 C. Regunathan fish, pearl oyster) aquatic products. In this background, World aquaculture has grown tremendously during the last fifty years from a production of less than a million metric tons (mmt) in the early 1950s to 51.7 mmt by 2006. World aquaculture has grown at an average annual rate of 8.8 % from 1970 to 2004 against 2.8 % of livestock production during the same period (FAO, 2009). In 2006, globally, aquaculture contributed 47 % (51.65 mmt) to the total foodfish production of 110.4 mmt. (FAO, 2009). Aquaculture now accounts for 76 % of global freshwater finfish production and 65 % of mollusc and diadromous fish production, 42 % of crustaceans and 70% of shrimps and prawns. It has been predicted that, in order to maintain the current level of per caput consumption at the minimum, global annual aquaculture production should touch 65 mmt by 2030, considering the fact that 2 billion people will be added to world population (FAO, 2009). In this report, present aquaculture status and needs for future growth of nine Middle East countries is dealt with. The countries include Bahrain, Iran, Iraq, Kuwait, Oman, Qatar, Saudi Arabia, United Arab Emirates (UAE) and Yemen. Except for Yemen all other countries are members of RECOFI (Regional Commission for Fisheries) of FAO. Bahrain, Kuwait, Oman, Qatar, Saudi and UAE are members of Gulf Cooperative Council (GCC). As the case with many of the fishing regions, Middle East too is facing the fish short supply crisis attributed to declining marine landings. For example, Kuwait fishery has declined from 7,752 t in 1994 to 4,373 t in 2008. Similarly, UAE fish landings dropped from 108,600 t to about 74,075 t in the same period. Yemen produced 228,116 t of fish in 2003, but fell down in 2008 to only 127,132 t of fish (FAO FishStat Plus, 2009). In Iraq, combinations of factors have led to considerable reduction in marshland fish catch. The factors include upstream dams in Turkey and Syria, the Iran-Iraq war in the mid- 1980s and the building of the drainage system in the 1990s that diminished the flow of water and nutrients into the marshlands (Woiwode, 2005). The countries that have reported increase or consistency in fish landings over recent years too report one or many of the following problems either as existing or anticipated. This includes fluctuation in annual landings, low CPUE (catch per unit effort), touching or crossing maximum sustainable level, plummeting landings of commercially important species, destruction of fish breeding grounds and potential future landing reduction etc. Over 60 % reduction in landings of orange-spotted grouper, Epinephelus coioides in Bahrain over the last two decades (in 1166 t in 1986 vs 307 t in 2008) and reported Caspian Sturgeons stock decline (legal catch drop from 22,800 tons in 1984 to 760 tons in 2004) (Pourkazemi, 2006) and extinction threat to their stocks by 2021 (http://www.sturgeon.de/ News/news_index.html) are enough examples to explain the exigency. The higher demand outstripping supply, skyrocketing fish prices, dwindling landings of commercial marine species, export earnings, health benefits associated with seafood consumption, employment opportunities, food security, poverty alleviation etc. in part or cohesively has made the countries realize significance of aquaculture and pushed them to devote attention to the sector.

Industry Perspective of Aquaculture in the Middle East 105

CHARACTERISTICS, BRIEF HISTORY AND DEVELOPMENT LANDMARKS

Aquaculture development has been relatively a recent event in the Middle East that began earnest in 1980s and is still in its infancy in most of the countries. Aquatic foods (fishes, crustaceans and molluscs) are not a staple diet in these countries. However, per capita fish consumption has been increasing due to increasing population, fish being cheaper protein than other animal protein sources (poultry, red meat) and awareness of health benefits related to fishfood consumption etc.

a. Characteristics of the Region

The Middle East region is characterized by extremes of climatic conditions with an air temperature ranging from about 48°C in summer to even 0 °C in winter. Seawater temperature ranges from 35 °C in summer to 16 °C in winter. Seawater salinity ranges from 39 to 43 ppt. Average annual rainfall is less than 15 cm and with virtually no runoff flow except in the northern part of Arabian (=Persian) Gulf. The coastal length in these countries ranges from just 58 kms with Iraq to 2,440 kms with Iran. These countries also record varying per capita fish consumption with UAE recording the maximum of 33 kgs and Iraq the least of 1 kg. Seafood is exported and imported by all these countries with the exception of Iraq where the export quantity was nil in 2007. Self- sufficiency with fisheries sector also differs between countries, for example while it is 100 % with UAE, it is only 43% in the case of Saudi Arabia in 2005 (Saudi MOA Report, 2006). The countries together represent a total population of more than 148 million, with Iran, Saudi and Iraq accounting the maximum with over 65, 28 and 25 million respectively. Another characteristic of Middle East is the high percentage of expatriate population (except Iran and Iraq). The expat population is quite high in countries like UAE, Qatar (both > 80 %), Kuwait (about 50 %), Bahrain (about 32.5 %), Saudi Arabia (about 20%) and Oman (about 17.5 %). The expat population influences fish preferences among population, so market demand and value. This again influences the economic feasibility of culturing particular species. Tilapia culture in Kuwait is targeted at meeting local Egyptian consumer demand. Except for Iran, Iraq, Oman and Saudi Arabia, where freshwater aquaculture is prevalent, in rest of the countries aquaculture is limited to brackishwater or seawater (mariculture). In almost all countries the local population has limited fish preferences and so aquaculture is more focused on these species. However, in some cases it is either to feed the expatriate population or the export scope that dictates the industry. Both these factors have served as the major reason for introduction of non-native species also.

b. Brief Aquaculture History

In all of these countries, government took the initiative to investigate the aquaculture potential by setting up aquaculture research centers and hatcheries, funding research programs etc. Once the culture potentiality is proven, commercial aquaculture sector started to take 106 C. Regunathan shape with investments flowing in from private sector. Even at that juncture, the support to sector continued in one or many forms and included easy site leasing, tax relaxation, soft loans, juvenile supply from own hatcheries, export incentive etc. b.1. Bahrain In Bahrain, applied scientific research in mariculture started in 1979 with the establishment of National Mariculture Center (NMC) by Directorate of Marine Resources with cooperation of FAO. The center is located at Ras Hayan on the South-Eastern coast and has been working on the seed production of various finfishes and shrimp in its hatchery facility. This led to successful mass production of fingerlings of rabbit fish (Siganus canaliculatus), sobaity seabream (Sparidentex hasta), gilthead seabream (Sparus aurata), mangrove red snapper (Lutjanus argentimaculatus), grouper (E. coioides), streaked rabbit fish (Siganus javus) and shrimp (Penaeus semisulcatus). Cage culture trials in 1999 in the shallow waters (9 m depth at the marine terminal of Bahrain Aluminum Factory) with six, 40 m circumference cages was stopped after couple of years due to severe fouling, predator problems and site related issues (Shams, 2009). b.2. Iran The first documented report on inland fish breeding in Iran dates back to 1922 (Mehrabi, 2002) at an Ichthyological center near the Caspian Sea. Serious efforts started with attempt to culture rainbow trout (Oncorhynchus mykiss) at Karaj, near Tehran in 1959 and with establishment of carp culture research station in Guilan province in 1970. The Karaj unit produced 3 million trout fingerlings using eggs imported from Denmark during 1965-1967. Caspian Sea Salmon (Salmo trutta caspius) fingerlings were first produced in the same unit in 1967. The formation of Iranian Fisheries Research and Training Organization (IFRO) in 1971, bolstered aquaculture research on finfishes (warm and cold water) and shellfishes. Between 1979 and 1989, several aquaculture centers capable of breeding trout were built. Commercial trout farms came into existence only in 1981. Though first commercial carp culture facility was established in 1969 with the support of Romanian experts (Salehi, 2004), only since 1985 culture of carps (common carp Cyprinus carpio, silver carp, Hypothalmichthys molitrix, grass carp Ctenopharyngodon idella and Big head carp, Hypothalmichthys nobilis) has developed to commercial levels. Fingerlings of Labeo rohita, an Indian carp, were imported to Guilan in 2004 to enrich the diversity of cultured fish (http://www.briancoad.com/ Species%20 Accounts/cyprinidae.htm). Attempts to culture of marketable size sturgeon (3-5 kg) in a pilot facility using freshwater was initiated in 1990 and cage culture trials in 1992 (IFTRO, 1995). In 2001, a private company in the north part of Iran started the first culture attempt with beluga sturgeon (Huso huso) culture using brackish water. Cultivation of this species in earthen ponds in the central Iranian desert at Bafqh near Yazd has been carried out. After six months at 16ºC and 11‰ salinity, the fish weighed 1100 g with a survival rate of 96% (IFRO, 2003). Commercial sturgeon farming started only post 2005. Iran has been seriously involved in hatchery production and ranching of number of fish species either in the Oman Sea or Gulf or Caspian Sea. The candidates included sturgeons (H. huso, Acipenser persicus, A. gueldenstaedtii, A. nudiventris, A. stellatus), yellowfin seabream (Acanthopagrus latus), barbel (Barbus sharpeyi), pike-perch (Sander (=Stizostedion) lucioperca), Caspian salmon (S. trutta caspius), shrimps (Fenneropenaeus indicus and P. Industry Perspective of Aquaculture in the Middle East 107

semisulcatus) etc. Artificial breeding and restocking programs for five sturgeon species had been ongoing in the southern part of the Caspian Sea since 1970s. According to Rajaby (2008) over 3 billion of fish juveniles (including 219.8 m of sturgeons) and 130 million shrimp juveniles have been searanched between 1993 and 2006. The initial steps to set up shrimp culture in Iran emerged in Bushehr Province in 1976 with site selection activities by France Research Co. However only in 1987, the first shrimp farm was established in Hormuzgan province. Preliminary studies were conducted on banana shrimp (F. merguiensis), the green tiger prawn (P. semisulcatus) and the Indian white shrimp (F. indicus) at Kolahi Fisheries Station and later in National Shrimp Culture Development Center in south of Iran (Faizbakhsh and Arnason, 2004).Commercial shrimp (F. indicus) culture activity has a short history only since 1991. Disease issues with native species culture led to issuance of license to import exotic whiteleg shrimp (Litopenaeus vannamei) broodstock since mid 2006. Giant freshwater prawn (Macrobrachium rosenbergii) has been farmed in Iran for years. Prawn larvae were caught from the Anzali Wetland and the Aras Dam reservoir and were grown in nurseries before being transferred into grow-out ponds. The Sefid-Rud Fisheries Research Site in Astaneh Ashrafiyeh near Rasht, as a pioneer of the industry, has set a 1,825 kilograms per hectare production record in 2006 (http://www.thefishsite.com/ fishnews/3216/freshwater-prawn-farming-gains-ground-in-northern-iran). Pilot scale pearl oyster farming was initiated in Berkeh Khalaf Village, Qeshm Island in August 2001 (http://sgp.undp.org/web/projects/6643/aquaculture_of_pearl_by_the_local_community_of_b erkeh_khalaf_village_qeshm_ island_ pearls_of_persian_.html). Early research with marine cage culture was done in 1990 by Iranian Fisheries Research and Training Organisation (IFRTO) with some small experimental cages for rearing wild caught fish juveniles. Understanding between the Iran Fisheries Organization (IFO) and a Norwegian company (Refa Holding AS) led to establishment of a pilot cage farm in Qeshm island in 2005 (Shakouri, 2009). They consisted of six circular, 16 m diameter polyethylene floating cages each with 1600 m3 volume. The farm has a production capacity of 180 t per annum. The farm was used to rear local marine species like Sobaity seabream (S. hasta) and exotic gilthead seabream (S. aurata). A second pilot farm was planned to be established in Bushehr province. b.3. Iraq Iraq’s Fisheries Department started pilot-scale fish farms in 1965 to test culture systems and suitable species (White, 1988). Commercial activities started only in late70s and early 80s, recording 3800 t of production in 1983. Common carp (C. carpio) dominated the production, others being grass carp (C. idella) and silver carp (H. molitrix). In the 80’s both State Board of Fisheries (Ministry of Agriculture and Irrigation), and the Iskandaria Agricultural Company, promoted development of small-scale fish farming in the farms located within the Tigris and Euphrates river basins. Fish farming was encouraged by leasing of suitable culture area by the government. By 1997, 1727 farms were operational covering a total area of 3200 ha, and produced 3400 t of carps. The farms ranged in size from 0.25 ha to 2.5 ha in area. Productivity per unit area was low in most fish farms, ranging from 1.4 to 2 tons/ha. This low productivity was attributed mainly to the shortage of adequate fish feeds. The mean annual production for 1986-1997 was 4000 t. 108 C. Regunathan

Other than commercial purpose, hatcheries produced fish fingerlings for restocking, which contributed greatly to the inland fisheries catch. Since late 1980s the country's fish farming industry has been in decline due to conflicts, reduced purchasing power, quality issues, juveniles and feed shortage and less investment from the government in aquaculture sector. The economic sanctions (1990-2003) further hampered development. The cumulative effect is clear from the fact that production in 2001 was only 2000 t, compared to 3400 t in 1997. Similarly, out of the total 2000 farms operational before 2003, only 500 were operational in 2008. b.4. Kuwait Aquaculture research started in 1970s by Kuwait Institute for Scientific Research (KISR) with feasibility of culturing introduced Nile tilapia (Oreochromis niloticus). The other initial research projects were on determination of spawning season and reproductive potential of different tilapia species like seawater tilapia (O. spilurus), blue tilapia (O. aureus) and Nile tilapia. KISR’s efforts on hatchery propagation of orange spotted grouper (E. coioides, earlier misidentified as E. tauvina) began in 1975. Natural spawning in captivity achieved with this species accelerated research on larval rearing methods (Hussain et al. 1975; Hussain and Higuchi, 1980) and led to future success with broodstock management and larval rearing techniques. Farming related research work also was carried out (Ahmed et al. 1999, 2000). Research on Sobaity seabream (S. hasta) culture started in early 1979 when captive broodstock spawned spontaneously in concrete tanks (Hussain et al. 1981). This led to successful larval rearing studies (Teng et al. 1984, 1999) and four-year research project (1982-1986) to develop viable commercial culture technology (Teng, 1987). KISR succeeded first in 1997 with larval rearing and fry production of Silver pomfret (Pampus argenteus) under hatchery conditions using wild-stripped eggs leading to a five-year project on larval rearing was initiated in April 1998. Studies also covered larval development (Almatar et al. 2000), feeding (Cruz et al. 2000, Almatar and James, 2007), overwintering (Cruz et al. 2003) and grow-out aspects (James and Al Matar, 2008). In 2006, a breakthrough was achieved by spawning of two year old Pomfret from domesticated broodstock developed from hatchery reared juvenile (James and Al Matar, 2007). Commercial aquaculture activities gained importance in late 1980 through the concerted efforts of the Public Authority for Agriculture Affairs and Fish Resources (PAAFR). Tilapia farming was first reported at private farms in the Al-Wafra and Al-Abdali agriculture areas in 1986. In 1992, the Bubiyan Fisheries Company began commercial production of gilthead seabream (S. aurata) and sobaity (S. hasta) in floating cages located in Kuwait Bay. Shrimp culture of P. semisulcatus has been widely researched in Kuwait since 1979 (Farmer, 1981; Al Hajj et al. 1983, Kneale et al. 1985, Al-Ameeri et al. 2006), but is still in experimental stage. b.5. Oman Oman’s aquaculture research started with the establishment of Marine Sciences and Fisheries Center (MSFC, under Ministry of Agriculture and Fisheries, MAF) in 1986 and hastened further by Aquaculture lab under it in 1992. The research unit carried out studies on site availability for aquaculture and on the culture potential of local shrimp (F. indicus), oyster (Saccostrea cucullata), abalone (Haliotis mariae) and fishes (sobaity seabream). Industry Perspective of Aquaculture in the Middle East 109

Viability of culturing gilthead seabream and sobaity in cages was carried out by MSFC in 1997 at Bandar Khyran area in Muscat Governorate. Four small cages (14 m diameter) were used in the project with juveniles imported from Greece and Bahrain. Research with abalone larval rearing started with the help of JICA in 1993 and production of juveniles was achieved in 1996. The aquaculture center under the MFW was established in September 2006. The first commercial cage farms were established in Quriat (capacity 2000 t / annum) and Bander Khyran (200 t/year) with Greek technology (Nireus Chios Aquaculture) in 2001 culturing variety of species viz., gilthead seabream (S. aurata), European seabass (Dicentrarchus labrax), thinlip mullet (Liza ramada), grouper (E. coioides), sobaity (S. hasta) and yellowfin seabream (Acanthopagrus latus). The cages used included both of 40m and 60 m perimeter and were imported from Norway (Polarcirkel). Yellowfin tuna (Thunnus albacares) fattening project was initiated in 2003 by the same company in Bandar Khiran using 50 m diameter cages targeting Japan’s sashimi market. Research studies on trial culture of tilapia (O. niloticus) including a recently imported Thai strain in agricultural fields along the crop fields were carried out in 2004, using ground water (0 to 20 ppt). Encouraging results have been reported with Thai strain reaching 300-400 g in five months (Goddard et al. 2004). The first commercial shrimp project was established in Sur in 1984 for farming Penaeus monodon. However the project was closed down later. The Oman International Shrimp Co was established in 2001 at Al Duqm, 600 km south of Muscat in the Al-Wusta region. The planned large-scale shrimp farm after pilot crops had to be shutdown in October 2003 as government took back the land for establishing port. Commercial shrimp farming is active again from 2007 with startup of a shrimp farm (Bentoot Shrimp farm) located close to Duqm. b.6. Qatar Qatar’s aquaculture research began with establishment of Doha Aquaculture Center in 1988 in cooperation with JICA. Research studies were carried out in this center, mainly on hatchery production and farming potential of economically important rabbitfish (S. canaliculatus), yellowfin seabream (A. latus), sobaity (S. hasta), grouper (E. tauvina), mullet (Velamugil seheli), golden travelly (Gnathanodon speciosus), tilapia (O. niloticus) and shrimp (P. semisulcatus). University of Qatar too is involved in research related to culture potential of commercial species like grouper and rabbitfish. b.7. Saudi Arabia In Saudi Arabia, the Fish farming center (FFC) established in 1982 at North Obhur, near Jeddah with the cooperation of FAO, experimented on establishing the captive breeding and culture technique for farming marine finfishes and shrimps. The finfishes included seawater tilapia (O. spilurus), rabbit fish (S. rivulatus), groupers (E. tauvina, E. coioides, E. malabaricus, E. polyphekedion, and E. fuscoguttatus), Asian seabass (Lates calcarifer), snapper (L. argentimaculatus) and flat head mullet (Mugil cephalus). The shrimps included the indigenous shrimps F. indicus, P. monodon and P. semisulcatus. Through its marine fish program the centre has succeeded in domesticating several species of commercially important fish species and maintains healthy broodstock of several grouper species, rabbit fish, mullet, seabream and seabass. The current research focuses on mass fish larval/fingerling production and reduction of hatchery operation costs. The Centre also succeeded in culturing the Sabaki tilapia (O. spilurus) in full strength seawater. Other research programs focus on live feed organisms, feed formulation and fish diseases. 110 C. Regunathan

Once the technical and economic viability of commercial farming was proven for tilapia and shrimp (F. indicus), commercial projects started to come up. The first commercial Tilapia farm was established in 1983 at Qassim and for shrimp on the Southern Red Sea coast of Saudi Arabia (Huraidha-Assir) 160 kilometer north of Jazan (Saudi Fisheries Co., SFC). SFC with an annual capacity of 1500 tons started operations in 1997 with F. indicus as primary culture candidate. P. monodon was produced initially but discontinued due to acute wild broodstock shortage. The success story with SFC lured more investors to enter the shrimp culture field. For freshwater aquaculture, research projects were started in 1980 by The King Abdulaziz City for Science and Technology (KACST, earlier Saudi Arabian National Center for Science and Technology), Riyadh, at their research centers in Dirab and Qassim. The R&D project was executed with the support of Taiwan Fisheries Research Institute (TFRI) and covered various aspects of culturing the freshwater fishes viz., Nile tilapia, common carp, grass carp, silver carp, bighead carp (H. nobilis), African walking catfish, (Clarius gariepinus) and giant freshwater prawn, M. rosenbergii. Later, TFRI team with other aquaculture experts from Taiwan in cooperation with Saudi personnel conducted research, evaluated more than 50 locations and 60,000 hectares for aquaculture development, and developed a national aquaculture plan. Sturgeon farming attempt was started in 2003 by a Dammam based private firm (Growfish, 2003) b.8. UAE In UAE, Marine Resources Research Center (MRRC), Umm Al Qaiwain established in 1978 with the technical co-operation from Japan (JICA) spearheaded research works since 1984 on potential aquaculture species. This started with fingerling production of marine fish species viz. rabbit fish (S. canaliculatus, S. javus), grouper (E. coioides) from 1985 to 1996. Gold-lined Sea bream (Rhabdosargus sarba), yellowfin bream (A. latus), sobaity (S. hasta) and mullet (Liza macrolepis) were produced during 1997-2003. MRRC also produced postlarvae of shrimps P. semisulcatus and F. indicus since 1985 and weaned them to adult size. The shrimp culture studies were temporarily halted in 2001. Major share of fish fingerlings produced were released into sea as a part of restocking program. First commercial aquaculture project was the cage culture project started in 1999 by the International Fish Farming Company (ASMAK) in technical partnership with Greece based Nireus group. The farm with 20 circular cages was located in the coastal waters off the coast of Ras Al- Khaimah was then moved to Dibba on the east coast in 2001. Finfish species cultured were the sobaity bream (S. hasta), the gilthead seabream (S.aurata), European seabass (D. labrax), grouper (E. coioides). Eventually, local fishermen also started to keep in locally made cages located in the lagoon area of Umm Al Quiwain to stock commercially important juvenile bycatch fish. Freshwater aquaculture of Tilapia (O. niloticus) in UAE is confined to a few irrigation channels, ponds and tanks adjacent to agriculture farms. The private fish and shrimp farming project based in Abu Al Abyad island (situated 125 km west of Abu Dhabi city) has been carrying out aquaculture research and has conducted farming experiments with tilapia (O. niloticus), shrimp (F. indicus) and rabbit fish (S. canaliculatus) (Yousif et al. 2003a, Yousif, 2004, Yousif et al. 2005). The project also reported successful breeding and fingerling Industry Perspective of Aquaculture in the Middle East 111

production of Sobaity (Yousif et al. 2003b) and experimental farming of native Cobia (Rachycentron canadum) (Yousif et al. 2009). b.9. Yemen The Yemeni government in 1977 requested the Japanese company Nichiro Gyogyo Ltd. to investigate the feasibility of shrimp culture (P. semisulcatus) in the country. Later the Aquaculture Research Center was established in Al-Buraika district, Aden, which began operations in April 1988. The center has been involved in research activities related to production of shrimps (F. indicus and P. semisulcatus) and a finfish (goldlined seabream Rhabdosargus sarba). The first commercial shrimp hatchery and pilot-scale farm for F. indicus was established only in 1997 in Al Sheher village (near Mukalla, Hadramout province) with investment from Saudi. The farm and hatchery had to be closed down after couple of crops due to administrative issues. The first full-scale commercial shrimp farm was set up by Hodeidah based Musallam group, in Lohayya along the Red sea and started production in 2005.

PRESENT STATUS OF AQUACULTURE AND DEVELOPMENT

a. Regional Overview

In general, aquaculture in these countries has registered remarkable growth in the recent times, increasing production from just 2,235 tons in 1994 to 198,562 tons in 2008. The aquaculture contribution to total fisheries increased markedly from 4.5 % in 1994 to 18.2 % in 2008. Development of commercial aquaculture involved number of foreign consultants and agencies either for technical transfer or for funding. It is worth mentioning here that Yemen joined the group of commercial producers only in 2005 and Bahrain and Qatar are yet to have a large-scale commercial aquaculture activity. All these countries are putting their best efforts to augment commercial aquaculture production. Individually, while some of them like Iran and Saudi have achieved substantial increase in aquaculture production, others are either in their infancy or at research trial levels (Bahrain, Qatar). Target to achieve reduction in imports by increasing domestic fisheries production, higher export earnings, employment opportunity, food security, poverty alleviation etc. acted as fillip to the growth of aquaculture sector. Commercially aquacultured species in these countries do not include aquatic plants and mollusks and is restricted to fishes and crustaceans. Aquaculture production of non-food aquatic species is only a minor sector of aquaculture in the region, and principally includes ornamental fishes. While production quantity is dominated by finfish species in most of the countries with Saudi and Yemen, it was by shrimp. The recent production figures show that few fishes like tilapia, carps, rainbow trout, European seabream, sobaity seabream and rabbit fish dominate finfish production (FAO FishStat Plus, 2009). Sea ranching of both shrimps and finfish juveniles has been practiced regularly in countries like Bahrain, Iran, Kuwait and UAE mostly by the government institutions. 112 C. Regunathan

The fish species cultured include both domestic and exotic ones, and the latter include both freshwater and marine shrimp (whiteleg shrimp) and fishes (carps, trout, sturgeon, European seabream, tilapia etc). Though inland aquaculture contributes to 99% of total production, all have identified the enormous potential for mariculture. Iran, Kuwait, Oman, Saudi and UAE already have marine cage farms in operation. The industry has been striving towards attaining international standards related to food safety and environmental protection.

Table 1. Fisheries production trend (1998-2008) and increased contribution of aquaculture in total fish production

Aquaculture share (%) in total Country Aquaculture (t) Capture (t) fish production 1998 2007 1998 2007 1998 2007 Bahrain 1 1 9849 15012 0.01 0.01 Iran 33237 158789 367212 403635 8.30 28.23 Iraq 7500 15810 22574 57779 24.94 21.48 Kuwait 220 348 7798 4373 2.74 7.37 Oman 13 175 106171 151744 0.01 0.12 Qatar < 0.5 36 5279 15190 0.01 0.24 Saudi 7099 20453 51291 70000 12.16 22.61 Arabia UAE < 2.0 570 114739 87000 0.00 0.65 Yemen 0 300 127620 179916 0.00 0.17

b. Countrywise Status and Production Overview b.1.Bahrain Aquaculture is still in its incipient stage in the Kingdom of Bahrain and there is no major commercial farming activity. With limited freshwater resources, growth potential is mainly in mariculture. The National Mariculture Center is currently the leading producer of juveniles in the region for a wide range of commercially important fishes like European seabream, grouper, sobaity and rabbit fish. Other than exporting to cage farms in UAE, Oman and Iran, juveniles are released into sea, as part of its stock enhancement programs. In 2008, a total hatchery production of 4,956,470 juveniles of three species of fish was recorded. This included 507,035 juveniles of Sobaity (S. hasta), 193,659 of the brown spotted grouper (E. coioides) and 4,255,776 of sea bream (S. aurata). Rabbit fish (S. canaliculatus) is the other species bred. The 2008 production from farming comprised of around 1.0 t of sobaity and 1.0 ton of grouper (FAO, 2010). Awal Fishing Company (associate of ASMAK, Dubai) is the only private aquaculture company that has a technical cooperation with Directorate of Marine Resources and is involved in marine finfish juvenile production. Center’s restocking program releases fishes like rabbit fish, sobaity and grouper in to sea and protected areas. Many scattered small farms presently produce Tilapia in small scale for Industry Perspective of Aquaculture in the Middle East 113

local consumption. The aquaculture production in the country since 1998 is presented Table 2 depicting a decreasing production trend since 2005. b.2. Iran Iran, with 2700 km of coastal area in the southern (1850 kms along Oman Sea and Gulf) and northern Iran (900 km along Caspian Sea), 1,900 natural, seminatural and artificial waterbodies and 150 earth dams, 235 barrage dams and 1,500 irrigation reservoirs holds huge potential for aquaculture and culture based fisheries activities. Total aquaculture production has gone up from 4935 t in 1978 to 154,979 t in 2008 (FAO Fishstat plus, 2010) constituting 27.5 % of total fish production (562,821t).

Table 2. Annual aquaculture production (1998-2008) in tons (FAO Fishstat plus, 2010

Country 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007

Bahrain <0.5 1 3 12 0.3 3 4 8 3 2.3 1.3

Iran 30279 33237 31800 40550 62550 76817 91714 104330 112001 129708 158789

Iraq 3,400 7,500 2,183 1,745 2,000 2,000 2,000 13,947 17,941 14,867 15,810

Kuwait 204 220 264 376 195 195 366 375 327 568 348

Oman 0 13 <0.5 <0.5 <0.5 <0.5 352 503 173 89 90

Qatar 2 0.3 0.3 0.3 1.3 0.6 0.6 0.6 11.6 36.6 36

Saudi 2696.6 3835.6 4690.6 5101 5620 6004 8218 6744 11824 11172 14375

UAE 1.2 1.2 1.5 1.5 1.5 1.5 2301.5 570 570 570 570

Ye-men ------380 350 350

Aquaculture in this country could be classified as 1) Warm water fish culture 2) Warm water shrimp culture, 3) Cold water fish culture and 4) Culture based fisheries and juvenile production for restocking programs. Warm water fish culture includes the culture of carps namely the common carp and Chinese carps (silver, grass and big head). In small scale, the fishes are reared in ponds and open waters following semi-intensive and extensive type of technology respectively. The provinces of Khuzestan, Guilan, Mazandaran and Golestan are the main geographical areas where warmwater fish farms are located. Extensive farming is carried out mainly in lakes, dams and reservoirs. Aras Dam in Azerbaijan province, Hamun lake in Sistan-Baluchistan province, reservoirs viz. Hoor-al-Shadegan and Howr-al-Hovizah in Khuzestan province are the major waterbodies where stocking is done to facilitate subsequent harvest by inland fishermen. In the ponds, carp fingerlings are stocked in March-April at a density of 2000-6000 per hectare and harvested between November and February and the production averages 3.5 tons/ha. Capital-intensive and professionally-engineered and constructed farms managed on a full time basis also exist. Supplementary diets include a variety of grains (100-6000 kg/ha/yr) 114 C. Regunathan or, for intensive monoculture of common carp, high protein pellets (30-40%). Polyculture of common carp with Chinese carps is also practiced. The general combination is 15-20% of common carp, 5-10% of grass carp, 60-70% of silver carp and 5-10% of bighead carp. Polyculture using species like carp bream Abramis brama has also been reported (IFTRO, 1995). Farming of giant river prawn (M. rosenbergii), freshwater bream (A.brama), milkfish (Chanos chanos), barbel (B. sharpeyi) and pike-perch (S. lucioperca) are being promoted to farmers as a way of diversifying production, increasing income and providing increased marketing flexibility. Barbel is grown with carps especially in Khuzestan province. The total area of warm water fishponds in Iran is estimated at approximately 29,836 ha, producing some 77,463 tons of fish in 2006 or 52 % of total aquaculture production. Both government and private sector are involved in hatchery production of fingerlings. Integrated farming systems are not common and involve a combination of duck, rice and fish and contribute only 2 % of total production. Coldwater fish culture mainly means culture of Rainbow trout in tanks, reservoir dams and raceway farms located in mountainous areas characterized by cool summers and cold winters (central, north-west and western parts of the country). Though majority of farming system is simple raceway made of concrete, production is also carried out in cages, pens, earthen ponds and agricultural reservoirs. The trout production has increased from 440 tons in 1989 to more than 58,761 tons in 2007. At present there are 60 private sector hatcheries including both licensed and unlicensed facilities, working in 13 provinces. Although the market demand for trout weighing more than 500 grams is good, the average market weight of fish is around 250 grams, and fish need at least 15 months to reach this size. Production of gilthead and sobaity sebream in Qeshm seacages (in 2007) has been reported (Maygoli, Pers. Commun.). Presently, the cages have been rented to a private company, however the cages have not been stocked yet. The Commercial marine shrimp culture industry grew quite faster with the government assistance, recording a production of 8,903 t from 310 farms in 2004 against 5 t per year production from 2 farms in 1992. However, disease problems since early 2000 crippled the industry growth and production. In 2008, only 219 farms (2481 ha) were operational producing 4,372 t of shrimp (IFO, 2009). Shrimp culture mostly at modified extensive to semi-intensive level is practiced in coastal provinces viz. Khuzestan, Bushehr, Hormozgan and Sistan-Baluchistan. Till 2003, more than 97% of production was of the endemic F. indicus, rest consisted of P. semisulcatus (Bushehr and Khuzestan provinces) and F. merguiensis (Hormozgan province). In 2006 L. vannamei broodstock import from Hawaii was allowed as an alternative to F. indicus which was faced with whitespot viral disease problems. In 2009 out of the four provinces only two cultured shrimp, while Hormozgan province (which has not faced disease problem yet) farmed F. indicus, Bushehr farmed L. vannamei. Commercial freshwater prawn production has gained interest recently registering hike in production from 23 tons in 2001 to 278 tons in 2008 (FAO FishStat Plus, 2010). Other than juvenile production for restocking purposes, recent interest has been on culture of Surgeon towards production of meat and caviar. The aquaculture candidates are Persian (A. persicus), stellate (A. stellatus) and great (H. huso) ones. Commercial Sturgeon farms have been set up in the northern provinces (Golestan, Mazandran and Guilan). In 2005- 2006, there were 11 sturgeon farms operational (private and 5 governmental) mainly for sturgeon meat production (20 tons per annum) and 10 more were about to start (Bronzi, Industry Perspective of Aquaculture in the Middle East 115

2007). At present there are 15 commercial sturgeon farms operational and several under construction (Pourkazemi, Pers. Communication, Dec. 2009). The total annual aquaculture production (warm water and cold water fishes and shrimps, excluding capture based) in Iran since 1998 is shown in Table 1, indicating a continuous upward production trend. b.3. Iraq The Tigris and Euphrates rivers and their branches are the main sources of inland freshwater in Iraq. The inland freshwater bodies cover between 600, 000 and 700, 000 ha, made up of natural lakes (39%), dams and reservoirs (13.3%), rivers and their branches (3.7%) and marshes (44%). Despite diverse water resources, both aquaculture and capture fishery productions from inland water resources drastically declined from 1994 to 2003 owing to various political and economic reasons. Economic sanctions imposed on Iraq since 1991 have restricted the availability of imported feed, medications, machinery and other supplies and equipment for aquaculture, thereby restricting the potential for expansion of the sector. Now, apparently, there are only around 500 operational farms (against 2000 before the war in year 2003), using earthen ponds, and averaging around 8000 m2 of water surface. Central Iraq boasts 70% of the country's fish farms. The fish farms raise freshwater carps like grass carp, silver carp, common carp, mullets and barbel sp. in small quantities. As in 90s the fish farmers still adopt an extensive type culture technology with limited feed supplementation, no artificial aeration etc. The farmers also lack proper facilities and operate much below their capacity. Even with the produce the facilities for storage and transportation are not of any quality standard. Currently, only four hatcheries are operating in Iraq, three of them privately owned. Fish feed production do not meet even minimal international standards and feed is common to all the species, with unknown formulations and quality. The quality and nutrients vary, as they are prepared using imported ingredients available in the country at the time of manufacture. There is also serious lack of trained biologists, specialists and consultants for project conception, design and operation. In 2008, with 19,246 t, aquaculture contributed 35.8 % to total fisheries production (FAO FishStat Plus, 2010). Kurdistan region produces annually 6700 tons of fish per annum with 247 farms (http://www.aknews.com/en/aknews/2/64426/). The production figures (Table 2) show sharp increase in production from 2004. This is mainly due to efforts by various international organisations like FAO, USAID and Nature Iraq along with Iraq’s Ministry of Agriculture. The projects implemented by these agencies aim at reactivating non-operational aquaculture facilities and even developing new ones. The construction of pumping station of nation’s largest fish farm, Euphrates Fish Farm Hatchery project in Babil province at a cost of $600,000 is one such project. The project executed by Soldiers from the 4th Brigade Combat Team, 3rd Inf. Div., with USAID’s Inma Agribusiness will support hundreds of local fish farms and will create employment to the level of 5000 people (http://www.blackanthem.com/News/iraqi-freedom/Fish-farming- rebounds-in-MND-C16591.shtml). In 2008, Nature Iraq had set up its pilot floating fish cage farm near the town of Abu Subat on the banks of Euphrates river (http://www.natureiraq.org/ Eng/proj_current.html).

116 C. Regunathan b.4. Kuwait Kuwait’s aquaculture activity includes culture of tilapia in concrete tanks using low saline underground water and marine cage farming. As such there is no commercial shrimp farming activity despite a pre-feasibility study by Stirling aquaculture, U.K. in 1998. Tilapia farms are based on limited low salinity underground water (2 -10 ppt) from 15 to 20 m deep wells with a temperature of 26 ºC round the year. The farms are located in AI- Wafra, AI-Abdaly and AI-Sulaibiya areas. The main species cultured include Nile tilapia (O. niloticus) and salt-tolerant Sabaki tilapia (O. spilurus). Concrete tanks with 1-2 m depth are used for culture with fingerling stocking rates of 10 and 50 /m2. Fish attain a marketable size of 350-400 g within six to eight months. Based on stocking density, the farms record a production of 10 to 15 kg/m3. Semi-recycling integrated system is adopted in agriculture areas where the discharge water is used to grow plants like alfalfa, tomato, onion etc. in the morning and in the night effluent water is recycled. Tilapia farms have increased in numbers from 3 in 1986 to 65 in 2006 producing 557 t (Ministry of Interior Report, 2007). However, the production came down to 300 t in 2008 (FAO FishStat Plus, 2010). Tilapia farms get an annual feed subsidy from the government to encourage productivity. Subsidized feed meets 50% of the farmers' needs. The PAAFR has established a new hatchery at AI-Wafra, which supplies tilapia fingerlings to the farmers. The fish culture cage farm is located in the Ras Kathmoh Marine Area near Doha Port in Kuwait Bay, where the water depth is approximately 11 m. Culture candidates include native sobaity seabream (S. hasta,) and gilthead seabream (S. aurata). The company owns 73 floating cages (15 m diameter each, total volume of 116340 m3), however only five of them were in operation in 2007. The feeds are imported from KSA, Netherland or from France. Juveniles are imported from France or Greece or from local hatchery using eggs imported from these countries. Commercial finfish hatchery production was started by Gulf International Aquaculture Company (GIAC) in 2000 by renting the facility of KISR. Till 2008, the hatchery had produced nearly 6 million juveniles, which included gilthead seabream, European seabass, yellowfin seabream, sobaity and grouper. The juveniles produced were consumed locally or exported to UAE or Oman. The commercial hatchery is no more operational. Kuwait’s aquaculture production (Table 2) over the years shows fluctuation in quantity produced. b.5. Oman Commercial aquaculture activities in Oman currently include cage culture of finfishes, pond culture of tilapia and shrimp farming. Cage culture of finfishes was started by the Quriat Aquaculture Co. in 2001, at two different sites viz. Bandar Khiran and Quriat. At present there is only one farm active (in Quriat) as the private company shifted the cages from Bander Khyran area. The farm mainly produces gilthead seabream with eight cages in operation. In 2004, fattening of yellowfin tuna (T. albacares) caught from Gulf of Oman was carried out in a 50 meter diameter cage in Bander Khiran. Presently, these cages also have been relocated in Quriyat. In 2004, 460 tons of European seabream, 27 tons of European seabass, 13 tons of yellowfin seabream and 14 tons of yellowfin tuna were produced. Since 2004, production of marine fishes has come down recording only 173 and 89 t in 2005 and 2006 respectively. In 2008 only 34 tons of gilthead seabream was produced. (RAIS, 2009). Industry Perspective of Aquaculture in the Middle East 117

Tilapia, which is an exotic species in Oman has been experimented as culture species in 2004 (Goddard et al. 2004). Initial farming research with Nile tilapia in selected farms carried out showed promising results. Each farm operates on pumped groundwater (salinity range 0- 20 ppt). Presently research is under way to examine the integration of tilapia production with traditional crops and trials have demonstrated excellent growth of the Thai strain. The best- performing fish averaged 300-400 g after five months at water temperatures ranging 25-33°C. In 2004 and 2005, 1.4 and 5 tons of tilapia was produced respectively, after this no production has been recorded (FAO, 2009, RAIS, 2009). After the shutdown of Oman International Shrimp Co in 2003, shrimp culture has again picked up in Oman recently with the establishment of a shrimp farm by private sector. The shrimp farm (Bentoot Shrimp farm) is located 500 km south of Muscat and is 100 Km away from Mahoot town. While 16 hectare area has been developed another 70 hectare area is under construction. Future plan includes expansion to 700 ha producing 3000 tons per annum. In 2007 and 2008 around 85 tons each of shrimps (F. indicus) were produced by the farm (RAIS, 2009). Another species of aquaculture interest is the Omani abalone (Haliotis mariae) and is a high value species with a great potential for culture. Studies at Mirbat Aquaculture Facility, Fisheries Research Center in Salalah showed some significant findings on the feasibility of propagating Omani abalone H. mariae under captivity. The MAF has also launched a project in association with a Japanese company to undertake aquaculture of culture candidates like sea urchin, octopus and abalone (Kamoonpuri, 2007). Ongoing research include developing breeding techniques for grouper E. areolatus and Red seabream Cheimerius nufar at Al Hail and Marbat facilities. Other species of interest is sea cucumber (Holothuria scabra) for which breeding and seed production will be tried and the seeds searanched. Research is also being carried out with breeding of clown fish. Oman’s production figures (Table 2) indicate an increment from 2003 due to the contribution from marine finfishes, however the increase was short timed one as production came down in 2005. Less than 0.5 t production in table indicate production of white shrimp by pilot scale farm. b.6. Qatar Aquaculture in Qatar is in its embryonic stages. Though significant efforts to develop the sector have been made since 1988, commercial culture activity is yet to be undertaken. The aquaculture center started working with the rabbitfish (S. canaliculatus), a popular fish in Qatar. The wild fingerlings collected from the sea were reared in an open system for 6-8 months until they reached marketable size of 200 g. Imported artificial feed was used during the rearing period. The Department of Fisheries is planning new experimental projects for the growth of the aquaculture industries as a profitable venture. Research studies have also covered mullet (L. macrolepis) and freshwater prawn (El Sayed, 1994, Kardousha, 2003). Since 2004, small scale semi-intensive culture of Nile tilapia is practiced by the private sector in earthen ponds (10 x 20 x 1 m) and in concrete tanks (3 x 10 x 1 m). In 2008, 36 tons each of tilapia fish were produced (Table 2). The Qatar Company for meat and livestock trading company (Mawashi) announced its plans to diversify into foodstuffs and fish and shrimp farming in 2008. In cooperation with the Ministry of Municipal Affairs and Agriculture, Mawashi has entered into a contract with a global consultancy company to assess initial feasibility of a mega project, which 118 C. Regunathan might be located near Al Areesh, a fishing village in northwest Qatar (http://www. thepeninsulaqatar.com/Display_news.asp?section=Local_Newsandsubsection=Qatar+Newsan dmonth=April2008 andfile=Local_News20080410293.xml). b.7. Saudi Arabia Proven culture feasibility of candidates by Fish Farming Center, near Jeddah and by The King Abdulaziz City for Science and Technology (KACST), Riyadh attracted private investments and paved the way for establishing an indigenous aquaculture industry. Currently, Saudi aquaculture production includes both freshwater and marine based farming. While the freshwater aquaculture is concentrated on the regions around Riyadh, marine fish and shrimp farming activity is along the Red Sea. The freshwater aquaculture production includes Tilapia (O. niloticus, O. aureus, O. niloticus x O. aureus hybrids, and Taiwanese red tilapia O. mosambicus x O. niloticus), carp (C. carpio), African catfish (C. gariepinus) and ornamental fishes. Mariculture includes commercial or pilot-scale production of grouper (E. coioides), sea bream (S. aurata), Asian seabass (L. calcarifer), rabbit fish (S. canaliculatus) and mullet (L. macrolepis). Tilapia farming is mostly intensive practiced in concrete and fiberglass tanks with 100% artificial feed input and usually with a target production of 10-15 kg fish.m3. Under these intensive conditions, the tanks are aerated, and 20 to 100% of water is exchanged daily, depending on the stocking density of the fish (Siddiqui and Al Najada, 1992). Recently, many of the tilapia farms (8 out of 12) in Saudi’s Eastern Province are closed down owing to number of technical and economic issues. Major reason being influx of cheaper frozen tilapia from South East Asian countries (http://www.zawya.com/story.cfm/sidZAWYA 20040809135424/Fish%20Farming%20in%20Easter%20Province:%20New%20Investment% 20Possibilities) Commercial shrimp mariculture at present is restricted to native F. indicus. Number of commercial shrimp farms are now operational along the Red Sea, mega ones being Saudi Fisheries Co, Arabian Shrimp Co., Jazan Agricultural Development Company (Jazadco) etc. However, the biggest is that of National Prawn Co. (NPC) located 15 km south of Al Leith township, and around 180 km south of Jeddah. Project’s phase 1 completed in 2004, includes more than 2500 ha waterspread area farm, over one billion postlarvae per annum hatchery capacity, 50,000 t per year feed mill and a processing plant capable of handling 80 tons per day of head-on shrimp. The project is targeted to produce more than 15,000 t of shrimp per year. Phase 2 of this project will add another 3600 hectare area and would take total production to more than 30,000 t per year (NPC web site - www.robian.com.sa). Once completed this will be the largest integrated desert shrimp farm in the World. Saudi Fisheries Company produces annually 1600 tons of shrimp. Aquaculture production is growing rapidly with shrimp (F. indicus) production that increasing from just 20 t in 1995 to 17,912 t in 2008. Total aquaculture production has jumped from 2,235 t in 1996 to 22,253 t in 2008 representing around 25% of total fish production in the Kingdom (Table 2). Tilapia production has been nearly constant over the recent years (2006-2008) averaging about 3800 t per annum. Only Cage farm was started by Jazadco’s Tabuk Fisheries company with the support of Greek company (Selonda aquaculture SA). The farm is located in Northern Red Sea near Tabuk area and cultures gilthead seabream (RECOFI, 2009). Industry Perspective of Aquaculture in the Middle East 119

NPC has initiated efforts on culturing indigenous Greater Amberjack (Seriola dumerili) on land as pilot scale, using a recirculation technology hatchery facility imported from Norway (www.akvasmart.com). Based on success with initial 5000 t target the future expansion will aim production of 35,000 to 50,000 tons per annum. NPC is also involved presently in hatchery production of sea cucumber (H. scabra) juveniles and plans to grow them in ponds. The first caviar-producing project in the entire region, was started by Dammam based Abdallah Al Faris Group. This project started with ambitious plan to produce sturgeon (A.gueldenstaedtii, A. baerii) meat and caviar. The company website (www.caviarcourt.com) advertises the availability of various grade Osetra caviar and sturgeon meat products. Initial production target is 5 tons per annum Osetra caviar and 200 tons of sturgeon meat. b.8. UAE The focal point of aquaculture in the UAE is the Marine Resources Research Center (MRRC) of the Ministry of Agriculture and Fisheries based in Umm Al Qaiwain. In MRRC’s facility larvae are produced either through natural spawning or by induced spawning, as the case is and reared to fmgerling size in 100 m3 tanks and later transferred to grow-out ponds. As a routine practice of implementing government policy, fingerlings or juvenile stage fishes are released to the sea also every year and includes fishes like sobaity (S. hasta), rabbit fish (S. canaliculatus and mullet (L. macrolepis). MRRC produced Sobaity juveniles are supplied to cages farms too. During the recent period, only commercial cage farm was of International Fish Farming Co (Asmak, located in Fujairah. The juveniles were imported from Greece, France, Kuwait or Bahrain and feeds from Greece, France and Saudi Arabia. The Fujairah site (1.5 km off Dibba) with 60 circular cages (19 m dia x 12 m depth each) produced 815 metric ton fish of gilthead, and 80 tons of sobaity in 2007. The red tide phenomenon in 2008 August - September wiped out the entire fish stock in the cages and led to the closure of farm leading to lower production record (Table 2). The harmful algae associated with fishkill were identified as dinoflagellate Cochlodinium polykrikoides. The traditional cages used by fishermen measure 2.5x2.5x2 m in size and are constructed locally and there is no official record of number of cages. Tilapia (O. aureus and O. spilurus) and grass carp culture is carried out in small scale, recording a yearly production of 6 tons (from 2001 – 2006). Al Jaraf Fisheries LLC based in Abu Dhabi is also involved in Tilapia farming. The company commenced its fish breeding operations in Al Ajban by 2006, A fishing company (Mubarak Fisheries) has recently signed an agreement with Ministry of Environment and Water and will venture into hatchery production of fingerlings (European seabream, Sobaity) and cage farming and has already taken up part of the MRRC hatchery facility (http://worldfishing.net/ new_horizons / new_ horizon.ehtml?o=2672). Currently commercial shrimp farming is carried out only by Abu Dhabi based Al Jaraf Fisheries (AJF), farming both F. indicus and P. monodon. The farm with lined ponds located in Barmid island started production in 2006. The shrimp feeds are imported from India and Saudi Arabia and final products are sold in the local market. AJF is planning cage farming of groupers also (www.palgroup.com). Recent aquaculture research activity in Abu Al-abyad Island includes breeding and fingerlings production of Cobia. The juveniles are released to sea as a part of restocking program. 120 C. Regunathan

Aquaculture production reached its peak in 2003 with peak production from offshore cage farm facilities (Table 1). Since then production stabilized at 570 tons till 2007 which included seabass, seabream and sobaity. In 2008 the production shot up to 1206 t (Table 2). Bin Salem GTE and United Food Technologies, its German partner, have already initiated construction of 38 million Euros investment project for Sturgeon culture in Abu Dhabi. This land based project (AquaOrbis UAE) plans producing 32 tons of caviar and 693 tons of sturgeon meat per annum (www.uftag.de). The plant is presently under construction in Abu Dhabi over a plot of around 60,000 m2, and will start operations in second half of 2010. The Siberian sturgeon (A. baerii) will be the species cultured (www.caviarist.com). This Ossetra sturgeon is smaller than the famous Beluga (H. huso) and it is said to produce a more intense, nuttier-tasting roe. Recently, UAE’s Ministry of Water and Environment signed a MOU with Japan’s Kinki University to farm Pacific bluefin tuna (Thunnus orientalis) in the country (http://www.thefishsite.com/ fishnews/9779/uae-japan-unite-on-bluefin-farming). b.9. Yemen The Aquaculture research center in Aden produces about a ton of shrimp on experimental basis. The shrimp farm (Musallam aquatic farms) located in Lohayya, near Hodeidah (Musallam aquatic farms) on the Red Sea coast is the only commercial facility presently operating in Yemen. The farm mainly cultures native F. indicus and P. monodon with the latter on trial basis. For P. monodon, wild juveniles of 30 to 50 gram size are pond-reared to 100 grams later to be used as broodstock for hatchery larval production. The farm with 500 tons per annum capacity produces about 350 tons per annum since 2005. The feeds are imported from Malaysia, Taiwan and China. The hatchery has a designed production capacity of 50 million postlarvae per annum. Many new shrimp farms are coming up along the Yemeni red coast including foreign investment ventures. Table 3 provides the details on various culture species presently cultured or in experimental stage with hatchery or farm level. When total aquaculture production in 2008 from all these countries is considered, finfish dominated in quantity contributing 88.4 % of total, remaining 11.6 % being shrimp. The major finfish species produced in terms of quantity included carps (102,042 t), rainbow trout (62,630 t), mullet (4893 t), tilapias (4,114 t) and gilthead seabream (1560 t). The fishes like catfish, rabbit fish, grouper, Asian seabass and sturgeon were produced in minimal quantities. The Indian white prawn (F. indicus) was the major crustacean species cultured, other shrimps being P. monodon , P. semisulcatus and exotic L. vannamei. Total shrimp production from the four countries (Iran, Oman, Saudi and Yemen) in 2008 was 23,008 t. In Iran, where exotic L. vannamei has been introduced has overtaken native F. indicus in terms of production quantity, with former contributing to 59 % of brackishwater shrimp produced. The production of carps and rainbow trout in 2008 represented 93.8 % of the total finfish production from these countries. Interestingly, major share of carps (86%) and total trout production came from Iran. Major share of shrimps came from Saudi Arabia (78 %) and Iran (20 %). At present all species farmed in the region is conventional; there are no Genetically Modified Organisms (GMO). SPF (specific pathogen free) status programs have been restricted only to shrimps, namely F. indicus and L. vannamei.

Industry Perspective of Aquaculture in the Middle East 121 c. Culture Species, Production Quantity

Species cultured and other details are presented in table 3.

Table 3. Countrywise list of aquacultured fishes

Country Fish Common name Scientific name Status of production

Bahrain Sobaity bream Sparidentex hasta H,PF Whitespotted Rabbit fish Siganus canaliculatus H,PF Streaked Rabbitfish Siganus javus H Mangrove snapper Lutjanus argentimaculatus H Gilthead seabream Orangespotted Sparus aurata H,PF Grouper Epinephelus coioides H Iran Giant river prawn Macrobrachium rosenbergii E Rainbow trout Oncorynchus mykiss C Common carp Cyprinus carpio, C Silver carp Hypothalmichthys molitrix C Grass carp Ctenopharyngodon idella C Big head carp Hypothalmichthys nobilis C Rohu carp Labeo rohita C Freshwater bream Milkfish Abramis brama E Barbel Chanos chanos E Pike-perch Barbus sharpeyi H Great (beluga) sturgeon Sander lucioperca H Persian sturgeon Huso huso C Stellate sturgeon Acipenser persicus C Russian sturgeon A. stellatus H Fringebarbel sturgeon A. gueldenstaedtii H Caspian Salmon A, nudiventris H Kutum Salmo trutta caspius H Caspian roach Rutilus frisii kutum H Yellowfin seabream Rutilus rutilus H Grouper Acanthopargus latus PF Gilthead seabream Epinephelus coioides PF Sobaity seabream Sparus aurata C Silver pomfret Sparidentex hasta C Indian white shrimp Pampus argenteus E Banana shrimp Fenneropenaeus indicus C Green tiger shrimp Fenneropenaeus merguiensis E Giant freshwater prawn Penaeus semisulcatus E Pearl oyster Macrobrachium rosenbergii E Seaweeds Pinctada margaritifera E Gracillaria sp. E Iraq Common carp Cyprinus carpio C Silver carp, Hypothalmichthys molitrix C Grass carp Ctenopharyngodon idella C Mullets Liza sp. C Barbs Barbus sp. C Kuwait Nile tilapia Oreochromis niloticus C Sabaki tilapia Oreochromis spilurus C Sobaity seabream Sapridentex hasta C Grouper Epinephelus coioides E Gilthead seabream Sparus aurata C European seabass Dicentrarchus labrax C Picnic seabream Acanthopagrus berda C Yellowfin seabream Acanthopagrus latus C Silver pomfret Pampus argenteus E Green tiger prawn Penaeus semisulcatus E

122 C. Regunathan

Table 3. (Continued)

Country Fish Common name Scientific name Status of production Oman Tilapia Oreochromis niloticus E Areolated Grouper Epinephelus areolatus E Gilthead seabream Sparus aurata C European seabass Dicentrarchus labrax C Yellowfin seabream Acanthopagrus latus C Yellowfin tuna Thunnus albacares CF Thinlip mullet Liza ramada C Indian white shrimp Fenneroenaeus indicus C Abalone Haliotis mariae E Sea cucumber Holothuria scabra E Oyster Saccostrea cucullata E Red seabream Cheimerius nufar E Qatar Nile tilapia Oreochromis niloticus C Rabbit fish Siganus canaliculatus E Largescale Mullet Liza macrolepis E Saudi Nile Tilapia Oreochromis niloticus, C Arabia Blue tilapia Oreochromis aureus, C Taiwanese red tilapia O. mosambicus x O. niloticus C Common Carp Cyprinus carpio C African catfish Clarius gariepinus C Brownspotted grouper Epinephelus coioides C Gilthead seabream Sparus aurata C Gold-lined Sea bream Rhabdosargus sarba E Asian seabass Lates calcarifer C Rabbit fish Siganus canaliculatus C Largescale Mullet Liza macrolepis C Greater amberjack Seriola dumerili PF Russian sturgeon Acipenser gueldenstaedtii C Siberian sturgeon Acipenser baerii C Indian white shrimp Fenneropenaeus indicus C Giant tiger prawn Penaeus monodon C Sea cucumber (sand fish) Holothuria scabra PF UAE Rabbit fish Siganus canaliculatus C Streaked rabbit fish Siganus javus C Brown spotted grouper Epinephelus coioides C Gold-lined Sea bream Rhabdosargus sarba E Yellowfin bream Acanthopagrus latus C Sobaity Sapridentex hasta C Gilthead seabream Sparus aurata C European seabass Dicentrarchus labrax C Largescale Mullet Liza macrolepis C Cobia Rachycentron canadum E Nile tilapia Oreochromis niloticus C Green tiger shrimp Penaeus semisulcatus E Indian white shimp Fenneropenaeus indicus C Giant tiger prawn Penaeus monodon C Yemen Gold-lined Sea bream Rhabdosargus sarba E Green tiger shrimp Penaeus semisulcatus E Indian white shimp Fenneropenaeus indicus C C- Commercial farming, E- Experimental stage, H – Hatchery production stage, PF – Pilot scale farming.

Table 4. Countrywise Production of fishes during the year 2000-2007 (FAO, 2010)

Country 2000 2001 2002 2003 2004 2005 2006 2007 ssb (12) ssb (<0.5) ssb (3) ssb (3) ------mrs (1) - - - Bahrain - - - rf (1) rf (1) rf (1) rf (1) ------gsb (<0.5) gsb (<0.5) - - - - ssb (6) ssb (2) ssb (1) ssb (1) bhc (1500) bhc (2415) bhc (3288) bhc (3665) bhc (3270) bhc (3670) bhc (3873) bhc (4863) cc (7000) cc (9915) cc (13700) cc (15271) cc (16350) cc (18349) cc (19366) cc (24316) Iran gc (2000) gc (4135) gc (3836) gc (4276) gc (9810) gc (11009) gc (11619) gc (14589) sc (17000) sc (26285) sc (33977) sc (37872) sc (35970) sc (40368) sc (42605) sc (53494) rbt (9000) rbt (12170) rbt (16026) rbt (23138) rbt (30000) rbt (34760) rbt (46275) rbt (58761) - fwp (23) fwp (30) fwp (30) fwp (27) fwp (268) fwp (270) fwp (258) iws 4050)- iws (7607) iws (5960) iws (7462) iws (8903) iws (3577) iws (5700) iws (2508) cc (1745) cc (2000) cc (2000) cc (2000) cc (8712) cc (8350) cc (11176) cc (12000) - - - - gc (1306) gc (1760) gc (1010) gc (1010) Iraq - - - - sc (2178) sc (2760) sc (1010) sc (1100) - - - - mlt (1751) mlt (5071) mlt (1671) mlt (1700) gsb (83) gsb (43) gsb (43) - - gsb (142) gsb (11) gsb (55) gss (150) gss (78) gss (78) - - - - - Kuwait ta (30) ta (16) ta (16) ta (202) ta (275) ta 185) ta (557) ta (293) gr (6) gr (3) gr (3) - - - - - ssb (107) ssb (55) ssb (55) ssb (164) ssb (100) ------esb (40) esb (142) esb (11.21) esb (12.73) - - - gsb (331) gsb (460) gsb (135) gsb (82) gsb (80) - - - esb (13) esb (27) esb (28) - - Oman - - - mlt (8) ------yfs (13) ------gr (0.222) - - -

Table 4. (Continued)

Country 2000 2001 2002 2003 2004 2005 2006 2007 - - - - yft (3) yft (5) yft (7) yft (10) - - - - - ta (5) ------iws (85) - - - - - ta (11) ta (36) ta (36) Qatar rf (<0.5) rf (1) rf (<0.5) rf (<0.5) rf (<0.5) rf (<0.5) rf (<0.5) - yfs (<0.5) yfs (<0.5) yfs (<0.5) yfs (<0.5) yfs (<0.5) yfs (<0.5) - mlt (35) mlt (20) mlt (22) mlt (18) mlt (10) mlt (30) mlt (12) - - - - - cr (27) cr (35) cr (5) Saudi ta (3968) ta (3981) ta (2019) ta (2580) ta (2396) ta (2987) ta (3781) ta (3804) Arabia cf (33) cf (25) cf (30) cf (35) cf (30) cf (32) cf (25) cf (46) rf (42) rf (27) rf (25) rf (27) rf (23) rf (10) rf (45) rf (15) - - - - - gr (50) gr (55) gr (<0.5) iws (1961) iws (4150) iws (4650) iws (9160) iws (8705) iws 11259) iws 11615) iws 14528) - - - gsb (750) gsb (190) gsb (190) gsb (190) gsb (190) - - - esb (750) esb (190) esb (190) esb (190) esb (190) gls (<0.5) gls (<0.5) gls (<0.5) gls (<0.5) - - - - UAE gr (<0.5) gr (<0.5) gr (<0.5) gr (<0.5) ------ssb (800) ssb (190) ssb (190) ssb (190) ssb (190) rf (<0.5) rf (<0.5) rf (<0.5) rf (<0.5) - - - - bts (<0.5) bts (<0.5) bts (<0.5) bts (<0.5) - - - - iws (<0.5) iws (<0.5) iws (<0.5) iws (<0.5) - - - - Yemen - - - - - iws (380) iws (350) iws (350) Bhc: Bighead carp; bts: Black tiger shrimp; cc: Common carp; cf: Catfish; cr: Croaker / Drums; esb: European seabass; fwp: Freshwater prawn; gc: Grass carp; gls: Goldlined seabream; gr: Grouper; gsb: Gilthead seabream; gss: Golksilk seabream; iws: Indian white shrimp; mlt: Mullets; rbt: Rainbow trout; rf: Rabbit fish; ssb: Sobaity seabream ; ta:Tilapia; yft: Yellowfin tuna; yfs: Yellowfin seabream. Industry Perspective of Aquaculture in the Middle East 125

III.d. Non-Food Aquatic Species Non-food aquatic species are a minor part of aquaculture production in these countries and includes ornamental fishes, seaweeds and pearl oyster. With ornamental fishes, there is an increased interest in domestic production in order to trim down the reliance on imports. Iran and Saudi, both present importers of ornamental fishes are the major producers of ornamental fish. Iran’s ornamental fish industry involves over 800 people and the turnover is to the tune of US$ 15 million with 85 species of them locally bred (www.iranexportsmagazine.com). The major production cities are Kashan, Tehran, Arak and Guilan. The target is to double employment and turn over by 2010. In Saudi Arabia, freshwater ornamental fishes are bred and exported by a private entrepreneur (Rashied Al Balla Est. www.maram.com) and claims to be the only breeder and exporters of live aquarium fishes in Saudi Arabia.. Currently, small-scale ornamental fish production is destined for development. Middle East ornament fish industry is valued at $11.4 million with the UAE as the largest importer of exotic fishes. UAE’s ornamental fish imports in 2008 crossed USD 1.14 million and have a substantial potential to emerge as regions hub of export and re-export. The demand for exotic fishes in UAE is expected to grow by 5 to 7 % annually (http:// www. ameinfo. com/ 185005.html). Iran’s pilot projects have demonstrated the feasibility of farming seaweed (Gracilaria spp.), pearl oyster (Pinctada radiate and P. margaritifera) and Artemia. The pilot project (2003-2007) in Qeshm has achieved culturing the oysters and developed bank of broodstock for both species (http://sgp.undp.org/web/projects/6643/aquaculture_of_pearl_by_the_local_ community_of_berkeh_khalaf_village_qeshm_island_pearls_of_persian_.html). Biotechnology center in Qeshm is presently involved with research on culture of seaweeds and pearl oyster.

e. The Non-Indigenous Species Introduction

Except Yemen, all the countries have introduced exotic culture candidates. The list of commercially bred or cultured exotic species in each of the countries is given below (Table 5). Table 5 shows the details of exotic species introduced for aquaculture purposes in the middle east.

f. Culture Environments

Among three culture environments (fresh, brackish and marine), nearly 87% was contributed by freshwater. Marine and brackishwater sector contributing only 10% and 3% of aquaculture production in 2008. Freshwater production was dominated by carp and trout from Iran, carp and mullet from Iraq and tilapia from Saudi Arabia. Marine water production comprised of shrimp from Saudi Arabia and fishes from cage farm. Brackishwater share came from Tilapia (Saudi and Kuwait) and shrimp from Iran and Oman.

126 C. Regunathan

Table 5. List of foreign species introduced for aquaculture purpose

Name of Introduced Species introduced Common name Introduced from Country Year Bahrain Sparus aurata, Gilthead seabream France 2005 Lates calcarifer, Asian seabass Malaysia 1990-99 Ctenopharyngodon idella Grass carp USSR, 1966 Romania,China 1968 Cyprinus carpio Common carp China 1968 Hypolthalmichthys molitrix Silver carp Romania, 1968 Hypothalmichthys nobilis Bighead carp China 1994 Iran Unknown 1966 Oncorynchus mykiss Rainbow trout Italy, Norway, U.K. Unknown Sparus aurata Gilthead seabream Bahrain 2007/8 Macrobrachium rosenbergii Freshwater prawn Bengladesh, Thailand 1994 Litopenaeus vannamei Pacific shrimp USA (Hawaii) 2006 Penaeus monodon Black tiger shrimp Unknown 1992 - 93 Cyprinus carpio Common carp Unknown 1955 Ctenopharyngodon idella Grass carp Japan 1968,85 Iraq Hypolthalmichthys molitrix Silver carp Unknown 1966-69 Hypothalmichthys nobilis Bighead carp Unknown 1966-69 Cyprinus carpio Common carp Hungary 2009 Oreochromis niloticus Nile Tilapia Taiwan Unknown Oreochromis aureus Blue Tilapia USA (Florida) 1979 Kuwait Oreochromis spilurus Sabaki Tilapia Kenya 1990-95 Sparus aurata Gilthead seabream France, Greece 1998 Dicentrarchus labrax European seabass France, Greece 1999/2000 Penaeus monodon Black tiger shrimp Singapore, Thailand 1987/88 Oreochromis niloticus Nile Tilapia Egypt, Thailand Unknown Oreochromis aureus Blue Tilapia UAE 1985 Oman Sparus aurata Gilthead seabream France, Greece 2001 Dicentrarchus labrax European seabass France, Greece 2001 Liza ramada Thinlip grey mullet Greece 2001 Qatar Oreochromis niloticus Nile Tilapia Unknown Unknown Oreochromis spilurus Sabaki Tilapia Kenya 1977,82 Oreochromis mosambicus Mozambique Tilapia Taiwan 1980 Oreochromiurolepis Rufigi Tilapia Unknown Unknown Oreochromis niloticus Nile Tilapia Unknown Unknown Tilapia zillii Redbelly Tilapia Unknown Unknown Lates calcarifer Asian seabass Singapore 1998 Clarius gariepinus African catfish Egypt Late 90’s Cyprinus carpio Common carp Taiwan Unknown Saudi Ctenopharyngodon idella Grass carp Unknown Unknown Arabia Hypolthalmichthys molitrix Silver carp Unknown Unknown Labeo rohita Rohu India Unknown Macrobrachium rosenbergii Freshwater prawn Taiwan Unknown

Hawaii 1992 Barbus apoensis Barb fish Unknown Unknown Sparus aurata Gilthead seabream Unknown 2007/08 Acipenser gueldenstaedtii Persian sturgeon Unknown 2002/03 Acipenser baerii Siberian sturgeon Russia 2002/03

Oreochromis spilurus Sabaki Tilapia Kuwait 1985 Oreochromis aureus Blue tilapia Kuwait 1985 UAE Ctenopharyngodon idella Grass carp Hong kong 1968 Sparus aurata Gilthead seabream Greece 1999 Dicentrarchus labrax European seabass Greece, France 2002-2004

Industry Perspective of Aquaculture in the Middle East 127

AQUACULTURE – MARKET, TRADE AND LAWS

a. Aquaculture Sales, Export, Impact on the Economy

Except for the shrimps and European fishes cultured, the aquaculture products are mostly sold in the domestic market. While shrimp produced by these countries is exported mostly to EU, USA, Japan, Egypt, and UAE, European origin exotic finfishes are exported to target EU market. However, Kuwait sold all exotic fishes produced in cages in the local market, unlike Oman and UAE. Major quantity of other cultured finfishes (tilapia, rainbowtrout, carps) is sold in the local market. In all of these countries aquaculture generally makes minimal contribution to national economies, when assessed by percentage of Gross Domestic Product (GDP). Differentiation of aquaculture product in their trade statistics has been initiated by few very recently, and thus for most countries the specific contribution of the aquaculture sector to GDP and Gross National Product (GNP) cannot be assessed. According to FAO statistics, the percentage contribution of fisheries (capture fishery and aquaculture combined) to GDP is 0.1–1 % for Bahrain and Iran, and <0.1 %, Kuwait, Oman, Qatar, UAE and Yemen. a.1.Bahrain Bahrain's aquaculture industry is still in its infancy; currently the fish harvested from the National mariculture center is sold in the local market. The center also exports European seabream and sobaity fry to nearby fish farming countries like Iran, Kuwait, Saudi and UAE. a.2.Iran Fish is not a popular part of the Iranian diet, especially in its central cities, which possess main proportion of the population. Per capita consumption was 1 kg/year in 1980 and reached 7.35 kg by 2007. This figure is quite low compared to some 23.1 kg of beef and lamb and 11.8 kg of poultry consumed by them each year. Marketing campaigns by the IFO and MOH has also helped to enhance fish consumption in the country especially for trout. IFO now targets a consumption of 10 kg/person in 2009, contributing 4.5 g /day of animal protein consumed. While the aquaculture produced trout and carps are sold to domestic market, shrimp exported to Europe is the major export earner. The role of fisheries (culture and capture) as a contributor to the Iranian economy (only 0.23 % in 2002) and its share of the agricultural sector are very low (2.2 %). But with potential for increased aquaculture production, contribution to the country's economy is poised to shoot up. a.3.Iraq With Iraq, there is a clear demand for fish that outstrips supply; fish is often unavailable in the markets. Current per capita fish consumption in Iraq is only 1.4 kg per year against 2.5 kg in 1990 (before the economic embargo). It is estimated that an additional market demand for farmed fish is around 25,000 to 50,000 tons. Actual fish demand seems currently inhibited by excessive retail price for fish - 3.500 IQD/kg ($2.33/kg) – often the same level as poultry. Preliminary studies indicate the possibility to produce farmed fish at a competitive price - 128 C. Regunathan perhaps at a retail price 15% lower than poultry and 70% below red meat. Estmates say, Iraq if returns to its pre-embargo per capita fish consumption level, then the fish import requirement will be above 58,000 tons, worth 104 million USD considering the domestic production of 12,000 tons. a.4.Kuwait Tilapia farmers in Kuwait sell their fish on-site or to small shops. Fish from cage farm is also sold locally. Farm-produced high quality fresh tilapia is sold for a price ranging from $4.5 to 6.0 (Ridha. 2006). Fish fry produced by the GIAC is exported to the UAE and Oman cage farms. But since 2008, the hatchery is not operational. When compared to the oil industry in Kuwait, the economic contribution of the fishery industry is very limited. However, as a traditional sector, Kuwait offers investment opportunities for private sector. The PAAFR has been encouraging aquaculture activities as a matter of priority and production is expected to meet future local demand for fish. a.5.Oman Although half of the Omani population depends on agricultural farming and fishing, agriculture contribution to GDP is very minimal. The majority of aquaculture production is exported as whole fish products to the UAE with only very minor quantities being sold locally. The reasons being, relatively high price of aquaculture products and less consumer- preference for them compared to wild marine fish. Recent data from FAO showed that fish consumption in Oman is about 27.2 Kg/year/capita. The 2004 price of exported gilthead seabream was 4.5 US$/kg, and for European seabass was 5 US$/kg. Tuna from the tuna-fattening project was exported directly to Japan. The shrimps produced (about 80 tons each in 2007 and 2008) are sold locally. Exported tuna fetched a price of around 20 US$/kg, while tilapia fetches about 2.57 US$/kg on the domestic market. a.6.Qatar Qatar's aquaculture production is very meager and its income is not contributing to the national economy. At present, there is no export of aquaculture products from Qatar. a.7.Saudi Arabia The shrimps produced along the Red sea is the prime export commodity. Shrimps are exported to Japan, Australia, USA, Egypt and EU. Saudi is also major producer of ornamental fishes mostly supplying the local market. The private ornamental fish breeding company (Rashied Al Balla Est.) exports freshwater ornamental fishes to Germany, Belgium, Italy, France, U.K., Qatar, UAE, Jordan, Kuwait and Bahrain. All the tilapia produced is sold in local markets. a.8.UAE In UAE fish harvested from the cages in Dibba coast are mainly exported to the EU, Canada and USA. The exported products are whole fish (fresh/frozen), gutted fish Industry Perspective of Aquaculture in the Middle East 129

(fresh/frozen) and fillets. The shrimps produced in commercial farm, fishes produced in the traditional cage farm and from land based tilapia farms are sold in domestic market. a.9. Yemen Yemen’s fish export revenues have been falling since recent years, increasing contribution of aquaculture to fisheries exports. Fisheries revenue fell during the first quarter of 2009 in Yemen by 13 % from $56.5 million in the same period last year to $49.5 million. The shrimps produced in Hodeidah region are exported to EU and is the only aquaculture product exported at present.

b. Laws, Permits, Certification and Agreements

Laws related to aquaculture activities, regulations, permits, certification, aquacultured fish export, export and import of fish eggs, juveniles and broodstock are in place in most of the countries. However, countries like Bahrain, Iraq, Qatar, UAE and Yemen have less comprehensive regulations in place. Regulations related to shellfish are found in fewer countries than those affecting finfish. However, within the shellfish producing countries, there are regulations in place for export of market size product and seed. b.1. Bahrain In Bahrain, rules and regulations relating to aquaculture are set by the Government viz. The Royal Decree on Exploitation and Utilization of the Marine Resources, issued in 2002. This law has provisions for controlling the culture of organisms such as licensing and quality issues. According to the law, a company may not undertake any aquaculture activity without permission from the authorized government body (General Directorate for the protection of Marine Resources). It also controls the collection of seed from the wild. There are no other specific laws or regulations related to fish farming. b.2.Iran The Iranian Fisheries Organization (IFO, Shilat in Persian) affiliated to the Ministry of Jihad Agriculture is responsible for the provision of related regulations and codes of practice for aquaculture management and development. The legal framework for fisheries and aquaculture activities in Iran is based on the provisions of the Law of Protection and Exploitation of Fisheries Resources of the Islamic Republic of Iran (1995 Law). The General Guidelines for Aquaculture and Fisheries (adopted in 1999 and amended in 2007), provides the legal framework for aquaculture activities. The guidelines include activities of following related organizations:

a) Iranian Fisheries Research Organisation (IFRO) and Iran Fisheries Organization (IFO) are responsible for technical issues such as the location of production units, breeding, nutrition, harvesting, handling and distribution, and refinement of rules and regulations for aquaculture b) the Environment Conservation Organization (ECO) of Iran has introduced some regulations to prevent certain activities having a negative impact on the environment 130 C. Regunathan

c) Iranian Veterinary Organization (IVO) contributes to this program by preparing sanitary and welfare rules and regulations. Animal diseases, hormones and drugs are dealt by them. d) Organisations such as the ECO and related research centers are involved in drafting rules pertaining to pollution and the environment and environment-friendly organic farming activities e) the Forestry Organization is involved because destruction of forests for pond construction is prohibited

The duties of each agency in the licensing procedure are clearly defined by the parliament and Council of Ministers. According to guidelines, a formal licence is required for activities such as fish farming in water bodies where aquaculture is not the major activity, for example irrigation canals and reservoirs, but they do not need to follow all the formal procedures, farmers usually obtain a letter of approval from the nearest Fisheries Department. Feed industry regulation is done by IFO, IVO, and the Ministry of Industries. b.3. Iraq Iraq’s law no. 48 for 1976 regulates the whole activities of fisheries. The Ministry of Agriculture issues regulations under this Law, according to the need and includes licensing for aquaculture firms too. Resolution No. 995 of 1985 linked to the establishment of pisciculture farms also details leasing of land by the Ministry of Agriculture and Agrarian Reform for the purpose of establishing pisciculture farms. However, enforcement of regulations is weak, particularly after the change of Government in 2003. b.4.Kuwait In Kuwait, PAAFR administers the basic national legislation in Kuwait, which is contained in law No. 46 of 1980. Aquaculture activities are administered and promoted by the Aquaculture division of PAAFR’s Fisheries Department. PAAFR also regulates aquaculture activities and adopts rules and regulations for aquaculture development. In 2005, government adopted resolution no.293 regarding issuance of aquaculture licences especially for the land- based farms. The resolution specifies farming area, source of water to be used, introduction of exotic species, drug use and disease control. b.5.Oman There is specific regulation for aquaculture in Oman namely the law on Aquaculture and Quality Control of cultured fish regulation (Ministerial decision No.36/2004). This executive bylaw encompasses various aspects of aquaculture like licensing requirements, quarantine requirement, related procedures, exotic species introduction and quality issues. The bylaw also states the role of the aquaculture committee and the follow up of applications from private sector. For environment protection, Ministry of Regional Municipalities and Water Resources (member of aquaculture committee) requires a study of Environmental Impact Assessments (EIA) for any aquaculture project before issuing its approval for the project. The law also deals with the quality of the product and the hygiene issues of the farms.

Industry Perspective of Aquaculture in the Middle East 131 b.6. Qatar The government body responsible for aquaculture development and control is the Ministry of Municipal Affairs and Agriculture, Qatar. At present, there are no specific laws or regulations for aquaculture in Qatar. b.7. Saudi Arabia In Saudi, the Deputy Ministry for Fisheries Affairs, was established under the Saudi Ministry of Agriculture and Water in 1992 to oversee national fisheries development policy. Simultaneously, a Department of Aquaculture (DoA) was established by the Ministry to execute and facilitate the activities related to aquaculture development. The activity includes, evaluation and enhancement of aquaculture activities, supervision of aquaculture farms, following up research activities, conducting feasibility studies, extending technical and extension services to farmers etc. The department also facilitates area allotment to farmers, loan sanctioning from banks and speedy approval from the aquaculture authorities to fish farmers for their short and long-term aquaculture projects. The law regulating fishing, investment and protection of living aquatic fisheries resources in the Kingdom was issued as the Royal Decree No. M/9 in 27/3/1408, entrusting the Ministry of Agriculture with the responsibility of supervising and developing this economic sector. The Ministry supervises this industry through the Deputy Ministry of Fisheries Affairs by establishing general policies, planning and designing short- and long-term developmental programs. The Deputy Ministry issues resolutions and regulating by-laws, and supervises three separate departments: 1) the Department of Aquaculture, 2) the Department of Fisheries and 3) the Department of Aquatic Environment. It also supervises the activities of a number of research canters and the regional fishery offices located on both coasts. b.8. UAE In UAE, the Ministry of Agriculture and Fisheries introduced Federal Law No.23 in 1999, regarding the exploitation, protection and development of the living aquatic resources in the waters of UAE. This is a comprehensive regulation governing many areas concerning fisheries, fishing activities, coastal zone management, marine resource and environmental protection, conservation of endangered marine species and coral reef areas etc. Aquaculture activities also come under the purview of the law (Articles 33 to 38 under chapter Protection and Development). The articles deal with issues like licence for establishment, introduction of exotic species and environmental protection. b.9. Yemen Yemen’s Ministry of Fish Wealth (MFW) is responsible for the aquaculture activities. Part 3 of Law No. 2 of 2006, in articles 32 to 35 speaks on control and development of aquaculture. The MFW is responsible to control, supervise and develop aquaculture activities, establishment of farms and encouragement of investment in the sector. It also manages a) import, culture and production of new aquaculture species, including aquarium fish species, b) stock enhancement programs, c) leasing of land or coastal area for aquaculture purpose and c) conducting aquaculture research and training.

132 C. Regunathan c. Aquatic Animal Health, Food Safety and Transboundary Issues

All these nine countries are members of the World Organization for Animal Health (Office international des epizooties, OIE), while six of the nine countries are members of the WTO (the exceptions being the Iran, Iraq and Yemen which have observer status). All the nine countries reviewed are members of Codex Alimentarius, ISO (Yemen correspondent member) and AIDMO (Arab Industrial Development and Mining Organization) etc. The membership of countries in OIE and WTO provides them with a common, agreed-upon formal methodology and structure (as outlined in the OIE Code and Manual) for conducting trade in live aquatic animals and which can be used in developing national and regional aquatic animal health programs. In addition to other monthly and annual reporting responsibilities to the OIE, the National Veterinary Services of OIE member countries are obligated to immediately (within 24 hours) report disease outbreak. Among countries, relevant aquatic animal health legislation varies from nonexistent (Qatar), through to numerous laws and regulations scattered in various legal documents (Bahrain, Oman, Saudi Arabia), to some which are specific to veterinary or aquaculture law (Iran, Oman, Saudi Arabia, UAE, Yemen). Regard to food safety, GCC countries does have regulatory harmonization with number of GCC standardization Organization (GSO) draft standards; however discrepancies do exist between countries. The Gulf Standards Organization (GSO) is comprised of senior standards officials from the six GCC member countries and is responsible for developing food and other standards in the GCC. Presently GCC member countries do have a joint panel called Food Safety Committee, which discusses the issues. Currently these countries are close to adopting a common food safety law. The uniform law once implemented will make food import and safety rules uniform in all member countries. GSO established under the umbrella of GCC and based in Riyadh, Saudi Arabia is working towards the same. c.1. Bahrain In Bahrain, the Public Health Directorate’s Food and Water Control Section (FWC), Ministry of Health is responsible for enforcing food safety regulations. The Food Safety Committee (FSC), an interagency committee composed of representatives from MOH, the Directorate of Standards and Metrology, Ministry of Commerce, Directorate of Agriculture, Ministry of Municipal Affairs and Agriculture (MMAA), decides all food safety and control issues, including ban imposition. c.2. Iran Iranian Veterinary Organization (IVO) and Ministry of Health and Medical Education cooperate closely in monitoring the supply of fish and fish products to the markets. IVO controls the safety of fish and fish products from production in the aquaculture facilities to the markets. The Office for Aquatic Health and Disease of the IVO, together with IFO, is responsible for aquatic animal health and diseases. The responsibility for establishing an aquatic animal disease surveillance system lies with the IVO as state-run body. Codes of conduct for food safety have been adopted.

Industry Perspective of Aquaculture in the Middle East 133 c.3.Iraq Iraq’s health Ministry with Food Control Laboratory under Nutrition Research Institute (NRI) shoulders the responsibilities of food control. The 2003 war disrupted food inspection services, however a risk-based food safety system was implemented in 2004. The present food safety system is a multi agency system and efforts are on by various International agencies to improve the Food Safety situation and even to develop a Food Safety Authority. At present though food laws and regulations exist they are not updated and not enforced. The Laboratories need to be modernized and staff trained on performing advanced tests. c.4. Kuwait Number of departments in Kuwait is involved in food safety monitoring and regulation. This includes the Municipal Services Systems Department, Imported Foods Department and Food inspection Department. Services system department sets systems, regulations, studies and laws for all procedures related to Food health and safety. While imported foods department deals with monitoring imported goods and Food Inspection Department carries out evaluation of food quality. PAAFR and Public Authority for Industries also play a vital role in food safety regulations. c.5. Oman Oman’s Law of Fishing and Protection of living aquatic resources (issued in 1982 and amended in 1993) states that the Directorate General of Fisheries is the competent authority responsible for managing the aquaculture sector. Within the framework of this law there are various executive bylaws which include bylaw on fish quality control (Ministerial decision No.136/1998) and bylaw on aquaculture and quality control of cultured organisms (Ministerial decision No.36/2004). c.6. Qatar Qatar’s Public Health Affairs Department under Ministry of Municipal Affairs and Urban Planning is responsible for food safety. c.7. Saudi Arabia Food safety is ensured by Ministry of Municipal and Rural Affairs. The Saudi Food and Drug Authority (SFDA) established under the Council of Ministers resolution no (1) dated 07/01/1424 H (10 March 2003), as an independent body includes food safety also in its objectives. Recent reports suggest that SFDA is giving the final touches to a food safety draft law. If passed by the Cabinet, the law will help to ensure that all imported and indigenous foodstuff are in conformity with local specifications and internationally recognized standards. (http://www.saudigazette.com.sa/index.cfm?method=home.regconandcontentID=2008072512 649) c.8. UAE The UAE General Secretariat of Municipalities (GSM) establishes food safety regulations based on recommendations made by the National Food Safety Committee (NFSC) on food related matters. The Emirates Authority for Standardization and Metrology (ESMA) is responsible for developing or adopting all standards. Emirate of Abu Dhabi has Abu Dhabi 134 C. Regunathan

Food Control Authority (www.adfca.ae) to take care of food safety issues and is a member of official committees in UAE. In Dubai and Sharjah, food control department of Municipality is the supervising body. Presently a committee comprising members from the Ministry of Health, municipalities and the economic departments has been set up to working towards forming an independent federal body to determine and administer safety standards for Food and pharmaceutical products. Once setup, UAE will be second country after Saudi (its SFDA) to form an independent body for food safety control (http://www.khaleejtimes. com/DisplayArticle08.asp?xfile=data/theuae/2009/November/theuae_November421.xmlands ection=theuae.). c.9. Yemen The Law No (2) of 2006 authorizes Yemen’s Ministry of Fish Wealth to be responsible for fish quality issues. The Quality Control division of the Ministry is involved in quality conformation of exported and domestic fish products. European Commission is involved in project related to various aspects of fish quality assurance including HACCP implementation. The Standards and Trade Development Facility (STDF, http://www.standardsfacility.org/) is currently providing assistance to Yemeni Seafood Exporters Association (YSEA) established in 2005 to improve quality and safety of Yemeni seafood products. The project was developed from an STDF project preparations grant and is to be completed by end of 2009.

d. Markets for Aquaculture Produce and Challenges to Farmers

The aquaculture produce varies from country to country and also the domestic demand. In some cases the aquaculture industry is export based, for e.g. shrimps, European fishes. Better prices from foreign buyers also dictate the industry. Presently major quantities of cultured finfishes are meant for local consumption. Diseases, increased production costs, decreased profitability due to lesser market prices or low productivity etc are the common challenges faced by the farmers. In Iran, shrimp production has been hit seriously by the disease problem especially the F. indicus farmers. The present shift to L. vannamei has brought down the intensity of the predicament in some of the areas. However, majority of them are not operational now. As the domestic demand is limited due to low per capita shrimp consumption, major quantity of production needs to be exported. Iran exports small quantity of carps to Middle East countries like Qatar, Iraq and Bahrain and trout to its neighbours like Iraq. According to Poursaeed and Falahatkar (2007) the increasing demand for quality fish will ensure trout culture to be economically feasible for the near future. However, lack of broodstock management programs, genetic problems are emerging among hatchery-produced fry, which is likely to result in a decline in production rate and productivity. This is against the backdrop of increasing demand for fry. To date, different lines of broodstock have been imported as eyed eggs have been cross-bred, resulting in a loss of genetic diversity, reduced production rate and increased food conversion ratio in farms. Other issues that affect the future of the industry include shortage as well as varying quality of fish feed, widespread diseases and lack of technical training. Carp farming has also been profitable, but the cost-benefit ratio and profitability varied between regions (Salehi, 2004). The carp farmers earn less profit due to low productivity which is again blamed on Industry Perspective of Aquaculture in the Middle East 135

lack of knowledge and equipments. Improving farming and hatchery techniques and training are the major issues facing the carp industry. In Iraq, shortage for juveniles and feeds are the major issues and is being dealt by International Agencies to augment production. Moreover, market linkages are insufficient, leading to disruptions in supply and occasional periods of general or localized oversupply. Fish storage and transportation facilities are not sufficient and even existing ones are not of International standard resulting in quality problems. Unpredictability of supply has a deleterious effect on potential demand for the product. Currently, Kuwait’s tilapia from land farms and fishes from cage farm are sold in domestic market. Tilapia industry is struggling with low production and profitability. High production cost, slow growth rate, high FCR, high feed cost, lack of trained manpower, impaired coordination among the farmers in marketing exist and competition from imported and frozen tilapia are the major constraints to farmers (Ridha, 2006). Oman the finfishes produced in cages and shrimp produced in ponds are the major aquaculture products and belongs to private companies. The need to import fish juveniles (as Oman does not have a commercial hatchery) and feed for both fish and shrimp are the major constraints. The Ministry has insisted on moving towards cage farming of indigenous species and such move needs a through economic analysis. In Saudi, major quantity of farm produced shrimp is exported. With tilapia industry, since the beginning of this decade, has been beset with various issues. All farms operated at less than profit-maximising scale and most operate at less than minimum efficient scale. The reasons attributed included low quality fry, low levels of management expertise in culturing tilapia and the secondary nature of tilapia farming. Added to these issues, imported frozen tilapia was cheaper than locally produced costly fresh tilapia, and dominated the market. While the local production cost Tilapia is about 9 Saudi Rials (1 SR=0.26 US$), the imported products are sold with a price tag of 5 SR. This has resulted even in closure of some of the farms. Other issues faced include shortage fish feed mills and limited technical guidance from Ministry. Offering of land by government in very remote areas with poor infrastructure, for future projects has further brought down the interest in new investment. Lack of water is likely to limit future expansion of tilapia farming in Saudi (Elhendy and Alzoom, 2001). Importing of fish juveniles (done till recently), feed and equipments are the major factors affecting UAE’s cage finfish farm and shrimp culture industry. In Yemen, importation of feed, machineries and low domestic demand are the issues facing the farmer.

e. Market Price of Wild Fish Compared to Culture Produce

Comparing the market price for wild and cultured it varies from country to country. While in Iran there are no clear price differentials between wild and cultured fish species, cultured ones are slightly costlier in Iraq, Kuwait, Oman, Saudi and UAE.

136 C. Regunathan

FOOD SECURITY AND AQUACULTURE

a. Food Security

Aquaculture contributes to food security (especially to the food insecure rural populations), rural employment and income generation. According to FAO (2009), 32 % of Yemen’s population was undernourished (2004-2006). Similarly, Iran’s 4 % population is under nourished (WFP, 2009). In 2005, the World Food Programme (WFP) estimated that more than four million Iraqi families were food insecure, with a further eight million at risk. Aquaculture projects implementation in viable areas could help to tackle the nutrition deficiency issue and would be an income generator to the vulnerable population.

b. Per Capita Fish Consumption

The per capita fish consumption varies from country to country reflecting different eating habits and traditions, availability of fish and other foods, prices, socio-economic levels, and seasons. The annual per capita fish consumption is high (>20 kg/person/year) in Oman, UAE and Yemen (27, 33 and 30 kg, respectively), moderate (10-20 kgs) in Bahrain (17 kgs), and Qatar (14.2 kgs), and low (<10 kg/person/year) in Iran (7.35 kgs), Kuwait (6 kgs), and Saudi Arabia (8 kgs). Iraq records the lowest value of 1.4 kg /person/year. The contribution of aquaculture to fisheries production also varies between countries.

c. Fish v/s Other Protein Sources

In relative terms, consumption of fish is lower than that of red meat and poultry across these countries. The relative contribution of fish to the total animal protein varies greatly from country to country; it is 15–25 % of total protein in Oman and Yemen, between 5–15 % in Bahrain, Iran, Iraq, Kuwait, Qatar, Saudi Arabia and the United Arab Emirates. In Iraq per capita consumption of fish has dropped down due to the long periods of unrest and sanctions and also to the decrease in the purchasing power and lack of initiatives to increase national fish production.

Industry Perspective of Aquaculture in the Middle East 137

Table 6. Per capita Fish vs Poultry and Total Meat Consumption in the countries

Poultry Meat Fish consumption Fish consumption Country consumption consumption 2003 2007 2005* 2002^

Bahrain 16.7 17.0 35.0 70.7 Iran 6.1 7.4 15.2 23.1 Iraq 1.0 1.4 8.5 - Kuwait 5.5 6.0 57.1 60.2 Oman 25.8 27.0 15.4 49.8 Qatar 12.0 14.2 28.7 90.5 Saudi Arabia 7.9 8.0 38.5 44.6 UAE 33.0 33.0 42.1 74.4 Yemen 30.0 30.0 9.2 14.7

RESOURCE USE AND THE ENVIRONMENT a. Water and Land Use in Aquaculture

In Bahrain, aquaculture activities are carried out only by the National Mariculture Center, occupying an area of 24 ha. Shrimp farms in Iran are both brackishwater and direct seawater based. In 2007, while 208 shrimp farms covered a total area of 1207 ha, the coldwater and warm water fish farms covered more than 22,000 ha. Marine shrimp culture in Oman is carried out in 16 ha waterspread area. About 4.6 ha of irrigation ponds are used as for extensive farming of tilapia in Qatar. In the UAE, Marine Resources Research Canter (MRRC), occupying an area of about 12.7 ha on the western side of the Entrance channel of Umm AI Qaiwain lagoon, carries out mariculture activities. In Kuwait , all 65 farms culturing Tilapia are located in Wafra agricultural area located about 100 km south of Kuwait City and in the Al–Abdali area north of Kuwait City. UAE’s Al Jaraf fisheries operates with 55 ha area for shrimp and 10 ha area for fish farming. In Yemen the marine shrimp farm near Hodeidah covers an area of 100 ha.

b. Feed and Seed Resources

There are no commercial fish / shrimp feed mills in Bahrain, Iraq, Oman and Qatar. Saudi Arabia has few commercial fish feed mills and is the largest regional producer of fish feeds (more than 20,000 tonnes / year) in the GCC region. Saudi Arabia exports annually to the United Arab Emirates about 500 tonnes of fish feed and an additional 200 tonnes to other GCC countries. National Prawn Company of Saudi Arabia itself has the capacity to produce 50,000 tons of shrimp feed per year. In Iraq, feedstuff producers do not meet even minimal 138 C. Regunathan international standards: Feed composition is standardized rather than modified for the needs of individual species. Often the feed employed was originally developed for poultry and then adapted to fish farming. The exact formulations are often unknown, and may vary depending on the availability of imported raw materials in the country at any given moment. Usual proximate composition includes 30 % protein and costs 0.2$/kg and with carps yields a feed conversion ratio of 2.3 (USAID, 2006). In Iran, six feed producers with a capacity of more than 20,000 tons produced 10,000 tons of feed in 2003 and more than 1,000 tons were also imported from Taiwan. In 2004, feed production increased to almost 11,000 tons, but 3,000 tons were also imported from Taiwan and China. Since 2009, Iran exports shrimp feed to Oman. In Kuwait fish feeds are mostly imported from France (Biomar) and Saudi Arabia (ARASCO). More recently, fish feeds are manufactured on a small-scale by two Kuwaiti-based companies (Sultan Feed Company and Kuwait Animal Feed Factory) from which Bubiyan Fishing Company is getting fish feed in limited scale. There is one partially operating fish feed mill in the UAE. However, the requirement is met by importing feeds from Saudi Arabia and Europe (for marine fishes) and from Saudi and India (for shrimps). Yemen shrimp farm imports feed from Malaysia, China, Taiwan and Saudi Arabia. Related to seed production, all the countries do have hatchery facility for shrimp seed production. However, purely commercial finfish hatcheries exist only in Iran, Iraq, Kuwait, Saudi Arabia and UAE. In the case of Kuwait the marine fish hatchery which belongs to Kuwait Institute for Scientific Research was rented out to a private company earlier and at present the hatchery is not operational. The marine cage farms need to import juveniles from Bahrain or from European countries like France or Greece. Bahrain hatchery which belongs to the Ministry produces fish juveniles (Table) and supplies GCC countries or releases them into sea as a part of restocking program. In Iran, hatcheries do exist for freshwater fishes (both cold and warm water) and for freshwater ornamental fishes. In 2004, more than 95 % of the juveniles were produced by private sector. However for marine fishes only modified shrimp hatcheries are used mainly to execute the larval rearing and nursery part of juvenile production. Currently in Iraq, only a few carp hatcheries are operational, four in the Baghdad region, none in the north apparently, where fish consumption is the lowest in the Iraq, and one is reported to be operating in Basrah. The renovated Euphrates Fish Farm Hatchery project produced 12 million fingerlings in 2008 against just 2 million in 2007 (https://www.inma-iraq.com/?pname=openandf= doc100242_010_activity_ 250px. jpgandid=242andtype=htmland). In Saudi, Fish Farming Center supplies farms along the Red Sea coast with juveniles of grouper, Asian seabass, rabbit fish etc. Commercial hatchery for tilapia, catfish and ornamental fishes exist along the Eastern province. With UAE, the government hatchery sells the juveniles or uses it for research purposes or for restocking programs. Production of juveniles for exotic species like gilthead seabream or European seabass is usually associated with import of eggs or just- hatched larvae from France or Greece. Commercial-scale marine shrimp hatcheries exist in all the countries that farm shrimps (Iran, Oman, Saudi Arabia, UAE and Yemen). In the case of Iran, broodstock of L. vannamei has been imported from Hawaii and with UAE, the broodstock of P. monodon from Tanzania. National Prawn Company of Saudi Arabia boasts of the shrimp hatchery with an annual capacity to produce over one billion postlarvae. Use of domesticated broodstock for hatchery Industry Perspective of Aquaculture in the Middle East 139

production has been reported with F. indicus in Saudi Arabia, Yemen and Iran. In other cases the domestication program is either in the initial stages or entirely dependent on wild broodstock. In the case of marine fishes, Kuwait reports the use of domesticated grouper (E. coioides) and sobaity (S. hasta) for juvenile production.

c. Environmental Management Issues

The General Directorate for the protection of Marine Resources in Bahrain issues licences for mariculture activities, operational regulations, export licenses for marine products and permits for any fish catch and processing business. However, there are no other specific laws or regulations for fish farming; there are no guidelines for EIA studies or for any environmental monitoring programs for mariculture. The Environment Conservation Organization of Iran has introduced some regulations to prevent certain activities having a negative impact on the environment (recommends recirculation of waste waters, filtration of waste, environmental impact assessment, etc.). Organisations such as the Environment Organization (EO) and related research centres are involved in drafting rules pertaining to pollution, environment and organic farming activities. The EO and the Energy (Water) Organization are involved in issues surrounding water supply for marine and inland aquaculture, respectively. In Oman, the Ministry of Environment and Climate Affairs (MECA) was established (Royal Decree No.90/2007) as the governmental authority responsible for the protection of environment. The law on Conservation of the Environment and Prevention of Pollution is the main one and provides the framework for environmental protection in Oman. The law was issued by the government in 1982, and subsequently amended by the Royal Decree No. 114/2001 on 14/11/2001. The Ministerial decision 187/2001 details the necessary requirements and the approval system for EIA studies. Aquaculture projects require an EIA study. However, it is opined that the guidelines of MECA are general and there is a need to develop specific requirements and guidelines for aquaculture EIA studies. The bylaw for aquaculture and quality control of aquaculture products issued in 2004 by the Ministry of Fisheries specifies that farm sites should not conflict with the activities of local fishermen and be located away from environmentally-sensitive areas such as mangrove swamps, coral reef and turtles nesting sites. The selection process is overseen by a specific aquaculture committee headed by the Ministry of Fisheries and includes members of other relevant governmental authorities. Presently, there are no specific laws or regulations for aquaculture in Qatar. With Saudi Arabia, the General Environmental Law and Rules for Implementation (Royal degree M/34 dated 16 Oct, 2001), details the environmental protection standards to be followed including EIA and disaster management requirements. The same assigned general responsibility of environment protection to MEPA, now called Presidency of Meteorology and Environment Protection (PME). In UAE, Federal Law No. 23 (1999) of Ministry of Agriculture and Fisheries is a comprehensive regulation governing many areas concerning fisheries, coastal zone management, marine resource and environmental protection, conservation of endangered marine species etc. Aquaculture activities including pollution control and regulation on introduction of alien species also come under the purview of the law (Articles 34 to 38). 140 C. Regunathan

LEGAL, INSTITUTIONAL AND MANAGEMENT ASPECTS a. Aquaculture Sector Management, National Support and Policy a.1. Bahrain In Bahrain, the Directorate of Marine Resources (DMR) within the General Directorate for the Protection of Marine Resources is the leading government agency responsible for management and development of aquaculture sector in the Kingdom. DMR also liaises with other government bodies on issues relating to aquaculture development and quality control. The DMR in Bahrain is working on a master that will comprise strategy for the aquaculture sector development and will deal with related issues like legislation, environmental monitoring, aquatic health, sustainability etc. The plan will also specify the role of different government authorities as well as the private sector in the management process of this sector. a.2. Iran In Iran, the Government through IFO and IFRO has been involved in various levels to support the industry. This support includes running of hatcheries, technical assistance to feed companies, financial assistance to new projects, research studies subsidies etc. Numerous schemes are on place to increase both brackish and marine aquaculture and fish production from cages as well as in ponds, lakes, reservoirs and rivers. The private sector has emerged as the major player in aquaculture investment, particularly in shrimp and warm water farming. Seafood exports are now recognised as a major source of export earnings. The processing facilities have to comply with EU standards. The Iranian Fisheries Organisation, in line with the government has already developed its fourth 5-year plan for fisheries (2005-2010). The plan deals with objectives like increased food security through increased domestic production, aquaculture productivity improvement, increasing fish consumption, increasing exports etc. Recently, Shilat has decided to involve in sturgeon farming with the support of German Company UTE (Iran Daily, June 16, 2009). It is estimated that 50 tons of caviar and 1000 t of sturgeon meat could be produced by aquaculture in Iran by 2011-2016 (Bronzi, 2007). a.3. Iraq In Iraq, various projects have been implemented post-2003 by International bodies like FAO, UNESCO, UNEP, USAID and locally General Board of Fish Research and Development (GBFRD) of Ministry of Agriculture to revive the industry. These projects aim to increase national fish production and enhance food security and livelihoods of fishermen, farmers and associated rural communities by utilizing unutilised inland saline water bodies in a sustainable manner with community participation. USAID’s Inma plans importing top quality fish broodstock from Hungary this year, which, upon passing Ministry of Agriculture quarantine, will be cross bred with heat resistant Iraqi stock to significantly improve the growth rate. From April to June 2010, the crossbred offspring will be distributed to hatcheries and fish farms throughout Iraq, estimated at 25 million fingerlings (USAID, 2009).

Industry Perspective of Aquaculture in the Middle East 141 a.4. Kuwait Both establishment of tilapia hatchery unit at Al-Wafra and support to cage farming industry in finding an alternate site, stand as proof to government’s interest. New site has been identified at the southern coast of Kuwait whereby the Bubiyan Fishing Company and other companies are likely to establish the cages for marine fish production in large scale. The aquaculture industry is presently getting supported by government in the form of feed subsidies for the tilapia farms and financial subsidy for the cage farm. The aquaculture production is expected to flourish with the concerted support of Government and fulfill the future demand for fish supply in Kuwait. a.5. Oman With Oman, establishment of Mariculture Center by Ministry of Fisheries Wealth with its advanced facilities will enable the country to cope with an expected expansion in the aquaculture sector. A Master Plan has also been prepared by the Aquaculture Laboratory for the future development of the aquaculture sector. The Plan covers areas such as legislation, environmental and disease monitoring, exotic species introduction, guidelines related to role of government and private sector in management of sector and best management practices towards sustainable management and development. The country currently concentrates on standardizing culture techniques for highly viable species like grouper (E. areolatus) and abalone (H. mariae). a.6. Qatar The construction of new hatchery in 2001 at the Doha Aquaculture Center helped to initiate series of research programs on finfish culture. The Government of Qatar is establishing a marine aquaculture center in Ras Matbakh which will be the keystone for the development of aquaculture in the country. Furthermore, the Agricultural Development Department has signed an agreement with the Industrial Bank by which long-term loans (25 years at 1.5 percent interest rate) are given to encourage farmer to establish fish farm. The aim of this policy is for the country to become self-sufficient with regards to its domestic demand for fish and particularly freshwater fish. a.7. Saudi Arabia Government’s Fish farming Center is currently involved in egg and juvenile production of fishes like rabbit fish (Siganus rivulatus), mullet (Velamugil seheli), seabass (L. calcarifer) and tilapia (O. niloticus). Other than researching on the aquaculture potential and standardizing culture protocol, the centre also supplies juveniles to private farmers and thus promotes the industry. The Department of Aquaculture, under Deputy Minister for Fisheries Affairs extends support with regards to the identification suitable sites where aquaculture operations can be established. The Department also conducts market analysis for aquaculture products which are made available to the private sector. a.8. UAE In UAE, government has been attracting investors in to aquaculture. The recent success with commercial cage farm and shrimp farming will pave the way for more such ventures. 142 C. Regunathan

Freshwater aquaculture is limited to a few irrigation channels, ponds and tanks adjacent to agriculture farms. Expansion is likely in the future as people are becoming aware of the dual benefits of rearing fish such as tilapia in such facilities which will not only produce fish but also fertilize the irrigation water. Marine Resources Research Centre has been contributing its share to aquaculture growth by providing fingerlings and imparting technical information to interested citizens. Government’s interest to farm bluefin tuna and other fish species is also an encouraging sign. a.9. Yemen Government is seriously involved with the projects dealing with quality and safety of Yemeni seafood products. As the project also involves application of latest standards in fish handling and processing would also be applicable to aquaculture products. Yemen Fish Company with government backing is planning to enter Tuna aquaculture sector (www.sabanews. net/ en/ word178162.htm).

b. Private Sector Participation

Commercial aquaculture in all the above countries is carried out by private sector. The private sector is supported by government in various forms and includes tax holidays, reduced taxes and land rentals, low-interest loans, supply of subsidized electricity, feed, juveniles, equipments, purchase of end product from farmers when problems are faced with exporting, purchase of juveniles from hatcheries for ranching purposes etc.

c. Education, Research and Training – Present Status

University courses in aquaculture, at the undergraduate and/or graduate levels, are currently offered by universities in Iran, Kuwait, Oman and Saudi Arabia. Courses are offered in general topics as aquatic science, fisheries science, hydrobiology, marine biology, and oceanography, and specific topics such as aquaculture, aquaculture hygiene, disease, feeding, fish husbandry, food hygiene, genetics, and production. In countries other than Iran, more limited aquaculture related training is available. Several institutes, universities and organizations have been involved in applied aquaculture research (Table 7). Iran, Oman and Saudi Arabia provide comprehensive government-supported research, extension and support services, such as pilot farms, hatcheries, and laboratories, and these services may be offered free or for a nominal fee. A key role of such centers is the provision of field and basic training in all aspects of aquaculture operation, and extension services such as regular meetings, and dissemination of information. Qatar is setting up an Aquatic and FisheriesResearch Center at Ras Matbakh in Al-Khor that will include a fishfarminglaboratory (http://www.ashghal.gov.qa/English/PublishingImages /Magazine Area/ Ashghal Plan_E.pdf). In Iraq, USAID’s aquaculture training program will establish training centers in the Babil area, propagating techniques that distinctly increase the production, quality and growth rate of Industry Perspective of Aquaculture in the Middle East 143 commercially bred fish. Two grants for aquaculture training centers have been announced, one each in North and South Babil (USAID, 2009).

Table 7. List of main research institutions involved in aquaculture research in different countries

Country Main Research Institutions National Mariculture Centre, Ras Hayan

Bahrain Centre for Studies and Research Bahrain University of Bahrain, Manama Iranian Fisheries Research and Training Organization Includes, a) Shrimp research centre, Bushehr b) Cold water Fishes Research Cenre, Mazandran c) Artemia Research Centre, Urmia d) International Sturgeon Research Institute, Rasht Iran The Scientific and Industrial Research Organisation Persian Gulf Biotechnology Research Centre, Qeshm Universities : Islamic Azad University (Tonekabon); Tarbiat Modarres Univ. (Tehran); Tehran Univ. (Tehran); Islamic Azad Univ (Tehran), University of Marine Science and Technology (Khorramshahr); Shahid Chamran Univ. (Ahwaz); Urmia Univ. (Urmia), Isfahan Univ of Tech (Isfahan) Fish Research Center (Zeafaraniyah, Baghdad); Marine Science Center (Basra); Agriculture Research Center; Iraq Central Hatchery at Swairah; Fisheries and Marine Resources Department in College of Agriculture (Basra) Kuwait Institute for Scientific Research, Ras Salmiya; Public Authority of Agriculture Affairs and Fish Kuwait Resources; University of Kuwait, Shuwaikh. Aquaculture Centre, Ministry of Fisheries Wealth, Muscat; Sultan Qaboos Oman University , Al Khod; Fishermen Training Institute, Al-khaboura. Qatar Aquaculture Centre, Doha; University of Qatar, Doha Fish Farming Centre , Jeddah; King Abdul Aziz City for Saudi Science and Technology, Riyadh; Eastern province fisheries Arabia research centre ; Red sea Fisheries Research Cnetre Marine Resources Research Centre, Umm al Qaiwain; UAE United Arab Emirates University, Al Ain Yemen Aquaculture Research Centre, Aden.

d. Aquafarmers’ associations, cooperatives

There are currently no aquaculture associations / cooperatives in Bahrain, Oman, Qatar, UAE and Yemen. In Iran, there are three cooperative unions, one each for coldwater, warm water, and shrimp production; the unions have been formed to lead aquaculture development, to collaborate in decision making and to support farmers. In Iraq fish farmers association is being formed by the efforts of USAID’s programmes. 144 C. Regunathan

In Saudi Arabia, currently no producers’ associations exist, however, the General Directorate of Aquaculture, Ministry of Agriculture has undertaken a study to establish an aquaculture society that would work as National Information Center.

SOCIAL IMPACTS, EMPLOYMENT AND POVERTY REDUCTION

The data on aquaculture employment for 2005 FAO’s National Aquaculture Sector Overview indicate maximum employment by Iran with more than 17,000 were involved in aquaculture either in private or government facilities. A recent report from IFO puts the figure at around 24,000 (Shariab, Shilat website). This is followed by Saudi Arabia and Kuwait with nearly 3,500 and 162 people respectively. Rest of the countries report a figure of less than hundred people with Qatar recording the lowest of 10. However recent report by USAID says more than 100 farms and local fish associations in Babil alone received fish juveniles from Euphrates fish hatchery (USAID, 2009). This means the manpower associated with aquaculture will be very well more than 162 thus taking Iraq to third position. In future with an estimated potential of 50,000 tons, the fish farming industry in Iraq could probably create at least 5,000 direct jobs, plus a considerable amount of related jobs (USAID,2006). Because of being an industry still in the technology and knowledge-intensive start-up phase aquaculture industry employs more technically trained people. However in many cases the employment includes illiterate labourers to the level of 80% workforce. Involvement of women in aquaculture has been reported with Iran, Saudi and Yemen. A study in the west of Iran (5 provinces ; Hamedan , Kerman shah, Lorestan, Eilam) shows that women and children are involved in 36 % of 298 fish units , including fish farm , double purpose fish ponds and raceways (Royan Engineering Consultancy, 2002). Women were also involved in non – production activities such as research, extension, consulting and support services in government or non – government aquaculture sectors and had higher education. Aquaculture has been recognized to be industry that can support poor families by providing employment, income and nutritionally-healthy, cheap protein. In countries like Iran, Iraq and Yemen, aquaculture produce is a vital source of food security in areas with poor infrastructure. For the rest of the countries, aquaculture industry would help to reduce the unemployment problem and earn foreign exchange.

RECENT TRENDS AND PRIORITY ISSUES

The recent trend has been towards diversification of species, intensification, integration and importation of foreign species. Research institutes have been working with potential new species for culture (silver pomfret, grouper, cobia, abalone). Intensification is done considering the economic viability and limited availability for land and water. Number of non-native species has been introduced in countries (European bream and bass, sturgeon, Pacific white shrimp) targeting the export market. The recent interest by International Sturgeon Research Institute (www.sturgeon .ir) to import paddlefish Polyodon spathula confirms that the trend is there to go on. Integration of agriculture and aquaculture has been practiced in Iran, Kuwait, Oman, Saudi and UAE and is strongly recommended and supported. Industry Perspective of Aquaculture in the Middle East 145

Culture of non-food species also has received greater interest recently in countries like Iran, Oman and Saudi Arabia and includes ornamental fishes, pearl oyster and seaweeds. Efforts to venture into organic aquaculture are yet to take place in these countries. Similarly, commercial SPF broodstock facilities and recirculation aquaculture systems do not exist in these countries. Inland culture of fishes like grouper and European seabass have also been planned by companies (Innovation Norway, 2009) The priority issues in Middle East aquaculture sector include the following: 1) Limited availability of suitable sites for culture. Limited availability of sites affects growth of the industry and also influence the technology adopted. In country like Kuwait, land-based mariculture activity is not feasible due to highly limited site availability close to sea. So, inshore or offshore culture is the only option available. In all the countries, even if suitable sites exist, they face conflict with concomitant users like tourism, conservation, fishermen, human settlement etc. Even the operating inshore, offshore sites face potential pollution problems. 2) Culture technology. Absence of local hatchery facility or inadequate production from existing ones compels farmers to import juveniles and an erratic supply affects farm’s production planning and economics. The long transportation hours also results in quality compromise of imported eggs / larvae / juveniles. Much research has to go into culture of endemic species, their domestication, larval rearing techniques, nutrition, farming technology, disease control protocol etc. Absence of local feed industry (except Iran and Saudi) leads to importation of feed resulting in high feed costs and so unit production cost. Present culture technology also needs to be modified to make it more environment-friendly and its products safe to consumers. 3) Marketing of products. In all these countries, per capita consumption of red meat and poultry meat is considerably higher than fish as the latter is not a traditional diet. Even with fish eating population the demand is for limited number of species. Countries have realized the potential of domestic market and country like Iran has taken steps to popularize seafood among its population quoting its health benefits. Increased domestic demand would help the farmers to escape out of fluctuating international demand and prices. This again requires comprehensive production and marketing strategies such that the products of required size and presentation are produced at a competitive price and are available at the time of peak demand and include variety of items to meet the demand of various segments of population. 4) Diseases, aquatic animal health monitoring, drug usage. Diseases have been a major issue leading to severe economic loss. Many of these countries (except Bahrain and Qatar) do have a policy effective enough to prevent entry and spread of pathogens. Yet, all the related issues are not covered except in Iran, Kuwait and Saudi Arabia. The inadequate disease monitoring program is a pressing issue in these countries. Such programs have been reported to be adequate only with Iran and Iraq. Disease monitoring programmes are currently planned for countries of Bahrain, Kuwait, Oman and Qatar; but not yet for UAE or Yemen (RECOFI, 2008). Other key regional deficiencies in disease awareness and management are difficulties in accessing information, an absence of specialists, and a scarcity of suitably qualified diagnostic laboratories, quarantine procedures and inadequate facilities in some instances. In a number of countries there is no regulation or legislation pertaining to chemicals and drugs approved for use in aquaculture. Much needs to be done in the form of regulations to ensure food safety. 146 C. Regunathan

5) Government support, Complex administrative procedures. Although all the countries have realized the significance of aquaculture, there is a lack of broader aquaculture development strategy. There is also lack of legal framework and even with prevailing laws they are not strictly enforced in some cases. Action discontinuity due to change of department heads also been a problem. Across the region there are circumstances where policies were or are absent, obscure, or complicated, thus hindering aquaculture growth? Obstacles include numerous agencies needing to be consulted for addressing single or limited issues, time consuming bureaucratic procedures, contradictory laws, rigid policies, lack of co-ordination among agencies and a lag between the speed of development of the administrative framework and the faster speed of development of the aquaculture industry itself. 6) Scarce financial assistance from banks or government. Repeated disease, product contamination, drug residue detection related shipment rejection and environment related issues have led to banks being too cautious to support for aquaculture. In many of the countries the governments have been playing a more proactive role in aquaculture development in the form of subsidies, low rentals, writing off bad debt from affected farmers, supply of juveniles etc. 7) Inadequate manpower, training and research. Shortage of trained personnel has been an obstacle to aquaculture development in many of the countries. Extension planning and lab- to-land programs are still lacking in all these countries. Lack of funding has been a major reason behind poor aquaculture related RandD work. RandD studies related to culture of local species, genetic improvement, environment-friendly management, integration of aquaculture with agriculture, polyculture, organic farming, low-cost feed formulation etc are need of the hour. Issues like harmful Algal blooms, biotoxins, episodic pollutants, global warming related issues etc also deserve much attention.

BAHRAIN

1. Larval Rearing facility in National Mariculture Center (NMC), Bahrain (Courtesy: RAIS).

Industry Perspective of Aquaculture in the Middle East 147

2. Concrete raceways in NMC, Bahrain (Courtesy: RAIS).

3. Outdoor broodstock facility in NMC, Bahrain (Courtesy: RAIS).

IRAN

4. Sturgeon – one of the recent commercial culture candidates in Iran. 148 C. Regunathan

5. Birds eye view of a trout farm, Iran.

6. Close view of trout farm in operation.

7. A Sturgeon hatchery facility in Iran (Courtesy: RAIS). Industry Perspective of Aquaculture in the Middle East 149

8. Cage farm in Qeshm island, Iran.

CONCLUSION

Technically, all these countries have high growth potential for commercial aquaculture. However, the aquaculture sector needs to operate under sound macro-economic, institutional and legal frameworks and is lacking in many. One of the prerequisites enabling aquaculture to make a contribution to sustainable development lies with a government’s commitment to provide appropriate support to the sector. Relevant to policies, legal frameworks and institutions a multi-faceted approach is needed for aquaculture development including development of a comprehensive management plan. The government must ensure participation by producers in the decision-making and regulation processes to make policies more effective. Regular dissemination of information by the sector to the regulatory agencies would help to promote a unified understanding of the needs of sector, Conducting regular meetings between different regulatory agencies would help to achieve exchange of information and improved coordination, harmonization of and possible amendments to laws relating to aquaculture and promotion of active inter-regional coordination of national policies as far as is practicable. It is also important that the farmers are updated on the latest developments related to quality, food safety, traceability etc. Health issues are of increasing importance due to intensification of aquaculture, and increasing movement of aquatic organisms within and between nations. The most pressing problem is inadequate disease monitoring and surveillance programmes. In order to address these deficiencies, training in correct sample collection and preparation, distribution and effective use of manuals for identification of etiological agents, establishment of a regional code of conduct and adherence, implementation of a regional alert/notification system for disease outbreaks, and adoption of effective biosecurity practices, needs to be implemented. Overriding all, there is an urgent need to establish a comprehensive regional center of 150 C. Regunathan expertise in fish health. It is imperative that each country has the lab facility to confirm the presence or absence of pathogens. Legislations need to be implemented controlling the movement of exotic species, use of drugs and chemicals in aquaculture. Import risk assessment (IRA) is becoming increasingly a standard tool for ensuring responsible movement and introduction of species and strains for aquaculture. Research and technology transfer between countries, are seen as key solutions to developing suitable new technologies that can be adopted for use in the remaining available sites, particularly those in the marine environment. Much research attention is wanting with relevance to developing technology suited to their conditions or local culture candidate, infrastructure development, research funding etc. To address environmental concerns, undertaking Environmental Impact Assessments for aquaculture projects, and promoting farming systems that make rational use of water, and assist environmental rehabilitation or pollutant mitigation (e.g. integrated agriculture aquaculture projects) is recommended. Certification in aquaculture can have positive effects by spurring new competitive advantages and investments. Enforcement of certification standards, best management practices and food safety regulations is imperative for export. Effective regulation is only possible with an effective information system, demanding improved quality of aquaculture information and statistics. Presently, there is a rush to invest in food sector outside the country by Arab nations to ensure food security for its population (gulfnews.com/.../uae-seeks-east-asia-food-security- links-1.515948). At this juncture it will be worth mentioning that they best utilize their aquaculture (especially mariculture) potential and ensure fishfood security for its people.

REFERENCES

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Cruz, E.M., Almatar, S., Abdul Elah, K. and Al-Yaqout, A. (2000). Preliminary studies on the performance and feeding behavior of silver pomfret (Pampus argenteusEuphrasen) fingerlings fed with commercial feed and reared in fiberglass tanks. Asian Fisheries Science, 13, 191-199. Cruz, E.M., Almatar, S., Al-Abdul Elah, K. and Al-yaqout, A. (2003). Indoor overwintering of silver pomfret (Pampus argenteus Euphrasen) fingerlings in fiberglass tanks. Asian Fisheries Science, 16, 33-40. Elhendy, A.M. and Alzoom, A.A. (2001). Economics of Fish Farming in Saudi Arabia: Analysis of costs of Tilapia production. Aquaculture Economics and Management, 5 (3 and 4), 229 – 238. El Sayed, A.F.M. (1994). Mullet culture in Qatar. Effects of replacing fish meal with soybean meal on growth and feed utilization of Liza macrolepis. Qatar University ScienceJournal, 14(1), 207 211. Faizbakhsh R and Arnason, R. (2004). The Economics of Shrimp culture in Iran and future strategies. Shilat web site. www.shilat.com/english/pics/Annex1.rtf FAO, (2009). The State of World Fisheries and Aquaculture 2008, 178 pp. FAO FishStat Plus, (2010). Global statistics data sets on total fishery production capture production and aquaculture production. http://www.fao.org /fishery/statistics/software/fishstat/en. Farmer, A.S.D. (1981). Prospects for penaeid shrimp culture in arid lands. In: advances in food producing systems for arid and semi-arid lands. Part B. Ed. by J.T.Manassah and Briskey, E.J. Academic Press, NY, pp. 859-897. Goddard, S.J, Al-Oufi, H. and Opara, L. (2004). Tilapia Culture: Farmers Participate in Oman Research. Global Aquaculture Advocate. 7(6), 33-34. Growfish, (2003). Sturgeon grows rapidly in Saudi Farm. http://www. Growfish .com. au/ content.asp?contentid=724. Hussain, N.A., Saif,M. and Ukawa.M. (1975). On the culture of Epinephelus tauvina (Forskal), Kuwait Institute for Scientific Research Report, 12 pp. Hussain, N.A. and Higuchi, M. (1980). Larval rearing of the brown-spotted grouper, Epinephelus tauvina (Forskal), Aquaculture, 19, 339-350. Hussain, N., Akatsu, S. and Al-Zahr, C. (1981). Spawning, egg and early larval development, and growth of Acanthopagrus cuvieri (Sparidae). Aquaculture, 22, 181-194. IFRO, (2003). Iranian Fisheries Research Organization Newsletter, 34 (3) - 36 (4). IFO, (2009). Iranian Fisheries Organisation’s data on fisheries and aquaculture production and export statistics. IFRTO, (1995). Iranian Fisheries Research and Training Organization Newsletter, 7, 4-5. Innovation Norway (2009). INBDP Report- Aquaculture in the Middle East, 36 pp. James C.M. and Almatar, S. (2007). A breakthrough in the spawning of domesticated silver pomfret. Aquaculture Asia-Pacific, 3 (1), 26-28. James C.M. and Almatar, S. (2008). Potential of silver pomfret (Pampus argenteus) as a new candidate species for aquaculture. Aquaculture Asia, 49-50. Kardousha, M. M. (2003). Preliminary assessment of the reuse of treated wastewater in aquaculture of Tilapia and fresh water shrimps in Qatar. Proceeding of the 13th International conference (Environmental protection is a must) 10-12 May 2003, Alexandria, Egypt. 152 C. Regunathan

Kamoonpuri, H. (2007). Oman: Fish culture research project launched. Oman daily observer, July 26. Kneale, D.C., Salman, S.E. and Farmer, A.S.D. (1985). The nursery culture of Penaeus semisulcatus in raceways. Kuwait Institute for Scientific Research, Report no. KISR 1854, Kuwait. Mehrabi, Y. (2002). Coldwater aquaculture in Iran, pp.63-70, in: Coldwater fisheries in the Trans-Himalayan Countries, Petr, T. and Swar, D.B. (Eds.), FAO Technical Paper 431, FAO, Rome. 376 pp. Pourkazemi, M. (2006). Caspian Sea sturgeon conservation and fisheries: Past, present and th future In: Proceedings of the 5 International Symposium on Sturgeons, Ramsar, Iran, May 9–13, 2006. RAIS, (2009). Annual aquaculture statistics from the web site of Regional Aquaculture Information System. http://www.raisaquaculture.net/index.php?id=344. Ridha, M.T., (2006) Tilapia Culture in Kuwait: Constraints and Solutions. Naga The WorldFish Center Quarterly, 29 (3 and 4): 71-73. RECOFI, (2009). Report of the Regional technical workshop on sustainable marine cage aquaculture development, Muscat, Oman, 25-26 January, 2009. 144 pp. Salehi, (2004). Carp culture in Iran. Aquaculture Asia Magazine, 9(2), 8-11. Shakouri, (2009). Islamic Republic of Iran: A review on marine cage aquaculture. www.rais aquaculture. net/ uploads/.../Iran%20-%20Draft%202.doc Saudi MOA Report, (2006). A Glance on the Agricultural development in the Kingdom of Saudi Arabia. Ministry of Agriculture, Kingdom of Saudi Arabia, 24 pp. www.moa.gov.sa/files/Lm_Eng.pdf. Shams, A.J. (2009). Kingdom of Bahrain: National review on marine cage aquaculture, RAIS aquaculture site, 4 pp. www.raisaquaculture.net/uploads/.../Bahrain%20-%20 Draft% 202.doc. Siddiqui, A.Q. and A.R. Al Najada. (1992). Aquaculture in Saudi Arabia. World Aquaculture, 23, 6-9. Teng, S.K., James, C.M., Tareen, I.U. and Dakour,S. (1984). Fish culture project, Phase II. Kuwait Institute for Scientific Research, Report No. KISR 1238, Kuwait. Teng, S.K. (1987). Final report, development of technology for commercial culture of sobaity fish in Kuwait (MB-46), Vol. I. Executive summary and general information, 44 pp. Teng, S.K., El-Zahr,C., Al-Abdul-Elah, K., and Almatar, S. (1999). Pilot-scale spawning and fry production of blue-fin porgy, Sparidentex hasta (Valenciennes), in Kuwait. Aquaculture, 178, 27-41. USAID, (2006). Business Models for aquaculture in Iraq, Report on USAID-IRAQ IZDIHAR project, 41 pp. USAID, (2009). Quarterly Report - Jan-March 2009, Inma Agribusiness program, 44 pp. White, P.G. (1988). A regional survey of the aquaculture sector in eleven Middle East countries, FAO publication, ADCP/REP/88/30. www.fao.org/docrep/ S9727E/ S9727E00.htm Woiwode, J.G. (2005). Iraq aquaculture supporting capture fisheries: food security for marsh arabs, World Aquaculture 2005, Meeting abstract. Yousif , O. M. (2004) . Apparent nutrient digestibility, growth performance and feed utilization of juvenile Nile tilapia, Oreochromis niloticus L., as influenced by stocking density and feeding frequency, Emirates Journal of Agricultural Sciences, 16 (2), 27-38. Industry Perspective of Aquaculture in the Middle East 153

Yousif, O.M., Kumar, K. and Ali, A.A., (2003a). Performance of white shrimp, Penaeus indicus, in highly saline pond waters. World Aquaculture, 34(3), 54-56. Yousif, O.M., Ali, A.A. and Kumar, K.K. (2003b). Spawning and hatching performance of the Silvery black porgy Sparidentex hasta under hypersaline conditions. Naga 26 (4), 13- 15. Yousif, O.M., Kumar, K.K. and Ali, A.A. (2005). Growth performance, feed utilization, survival and body composition of rabbitfish Siganus canaliculatus raised at two different stocking densities in sea net cages. , Emirates Journal of Agricultural Sciences, 17 (2), 14-22. Yousif, O.M., Kumar, K.K. and Abdul-Rahman, A.F.A. (2009). Growth response of cobia Rachycentron canadum (Pisces: Rachycentridae) under the hypersaline conditions of the Emirate of Abu Dhabi. Aquaculture Asia, 14(4), 41-42.

Chapter 9

AQUACULTURE IN ISRAEL: CURRENT STATUS AND INNOVATIVE APPROACHES

W. M. Koven1, S. Harpaz2, J. Van Rijn3 and N. Mozes4

ABSTRACT

In 2007 Israelis consumed about 72,000 MT of fish, which is about equal to 10 kg per capita. About 65% of demand was from frozen imports while approximately 35% of consumption came from locally produced freshwater and marine fish or 24,866 MT. Fresh water aquaculture represented 19,168 MT while mariculture's share was only 2,251 MT. New advances in m1ariculture research included the dietary manipulation of the stress response in fish larvae, determining the environmental and nutritional factors affecting juvenile deformities in gilthead sea bream as well as the quantification of the daily energy and protein requirement for the gilthead sea bream, European sea bass and white grouper during grow-out. The use of the mesocosm approach was implemented for the larviculture of grouper and studies were conducted to increase the female/male sex ratio in the European sea bass through temperature manipulation during larval rearing. In freshwater aquaculture a vaccine against a virus (CyHV–3) that devastated carp and Koi culture was developed and hybrid tilapia was organically grown in polyculture as well as in the desert using underground saline and geothermal water. By 2000 Israel was 10th in the world in revenue from ornamental fish. In 2007, the exports of cold water ornamental fish, mainly the ornamental carp (Koi), were around $12,000,000 annually. Tropical warm water ornamental fish production exceeds $250,000 annually while marine ornamental fish production revolves mainly around 5 species of clown fish (Amphiprion spp.), the major one being A. ocellaris with a monthly production of 7,000-10,000 fish.

1 Israel Oceanographic and Limnological Research, The National Center for Mariculture (NCM), Eilat 88112, Israel 2 Institute of Animal Science, Agricultural Research Organization (ARO), The Volcani Center, P. O. Box 6, Bet- Dagan 50250, Israel 3 The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel 4 Fish and Aquaculture Dept., Ministry of Agriculture and Rural Development, P.O.Box 30, Bet-Dagan 50250, Israel. 156 W. M. Koven, S. Harpaz, J. Van Rijn et al.

An effective approach to the water treatment of in-land fish farm effluent through biofiltration has become the cornerstone of the integrative pond approach in Israel. Organisms involved in biofiltration can be bacteria which convert waste carbon and nitrogen into gasses while microalgae, macroalgae and suspension feeders assimilate nutrients from the effluent into their biomass. In Israel, water and land scarcity as well as potential environmental damage associated from marine fish cage culture have been the driving forces behind the development of recirculating systems. A low-head recirculating concept was developed to produce the Mega-Flow system. This approach is based on providing water circulation and water aeration by means of airlifts. Alternatively, other research has mainly dealt with the development of a zero-discharge recirculating system based on the combined aerobic/anoxic treatment of the culture water.

INTRODUCTION

Israeli aquaculture began in the mid 1930's with the introduction of the common carp which was grown employing traditional European methods. In the 1960s tilapia species and hybrids were introduced where the major part of production was carried out in extensive fish ponds with annual average yields of less than 5 MT/ha. Since then this industry has expanded greatly and today is concentrated in three main regions in Israel. The fresh water culture of tilapia, mullet, carp, trout, striped bass and silver carp is centered in the northern part of the country while the Lake Kinneret (Sea of Galilee) has been stocked with a range of species that have been cultured (S. galilaeus, silver carp) or caught (muglids) in the sea. The focus, until recently, on the mariculture of the main species; the gilthead sea bream (Sparus aurata) and to a lesser extent the European sea bass (Dicentrarchus labrax), has been in the Gulf of Aqaba near the city of Eilat, Israel. In the last few years, marine teleost production has increased along the Mediterranean coast. In fact, a fourth focus has developed over the last decade in the Arava valley in the south of Israel where a number of ornamental fish farms are producing mainly for markets in Europe. In order to find new markets and/or reduce the commercial and sport fishing pressure on populations that are endangered, new species such as the white grouper and blue fin tuna are currently being investigated. In addition, species such as the grey mullet, rainbow trout, hybrid bass, red drum and Australian silver perch are being grown, as well, to expand the industry. Apart from the growing demand for farmed fish, there are two problems that are becoming more acute in the region which have stimulated the Israeli aquaculture sector to be particularly innovative. The first is the chronic water shortage plaguing Israel and its surrounding neighbors while the second is the conflict between aquaculture activity and its resulting effluent on tourism, environmental resources and fish welfare. This was brought into sharp focus in recent years where commercial sea cages near Eilat, primarily raising gilthead sea bream, were removed after a lengthy legal process due to concern of their alleged effect on near-by (8 km) coral reefs. This has lead to a keen awareness in the industry to reduce water use (freshwater and marine recirculating aquaculture systems) and to significantly remove nitrogen based compounds (biological and/or mechanical filtration) in the effluent from commercial operations.

Aquaculture in Israel 157

THE PRESENT STATUS OF AQUACULTURE

The most recently published report by the Israeli Ministry of Agriculture and Rural Development, Fisheries and Aquaculture 2007 (Shapiro 2007) reported that Israelis consumed about 72,000 MT of fish, which is about equal to 10 kg per capita, a slight decline from previous years (Table 1). About 65% of demand was from frozen imports or about 47,000 MT while approximately 35% of consumption came from local resources or about 25,000 MT. The latter was comprised mostly of freshwater and marine fresh fish representing 28% and 7%, respectively, of all fish consumption (Fig. 1). Of the imported products frozen fillet dominated at 56.6%, followed by frozen fish (35.3%) while small percentages of fresh fish (4.5%), crustaceans (1.8%), shellfish (1.3%) and fresh fillet (0.5%) were also imported (Figure 2). It is worth noting that 2007 showed an increasing trend of buying more frozen fish from Asia of species grown in Israel, such as tilapia (3,800 MT of frozen filet), which ultimately lowers the profitability of the Israeli aquaculture sector.

Table 1. Fish consumption in Israel 2004-2007

2007 Average 2004-2006 Source Landed weight Consumption per Landed Consumption per (MT) capita in product (kg) weight (MT) capita in product (kg) Marine 2,607 0.4 2,835 0.5 Lake Kinneret 840 0.1 1,310 0.2 Aquaculture 19,168 2.6 12,720 2.8 Mariculture 2,251 0.3 2,183 0.5 Total domestic 24,866 3.4 19,048 4.0 production Import 47,224 6.5 42,517 6.1 Grand total 72,090 9.9 61,565 10.1 Modified from Shapiro 1997.

Table 2. Sources of the Israeli Fishery 2004-2007

2007 Average 2004-2006 Change Change of value of Source Catch % Catch % Value Gross catch (MT) catch (MT) catch x$1000 income NIS x$1000 % %$ Marine 2,607 10.5 101,200 24,114 2,393 9.3 19,505 8.94 23.63 Lake 840 3.4 4,844 1,041 1,137 4.4 1,321 -26.12 -21.20 Kinneret Aquaculture 19,168 77.1 252,475 61,458 18,949 73.6 50,519 1.16 21.65 Mariculture 2,251 9.1 67,720 16,484 3,275 12.7 18,495 -31.27 -10.87 Ornamental 70,006 17,041 13,526 25.99 fish Total 24,866 100 496,245 120,138 25,754 100 103,366 -3.45 16.2 Modified from Shapiro 2007. 158 W. M. Koven, S. Harpaz, J. Van Rijn et al.

28%

Freshwater Marine Import 65% 7%

From Shapiro 2007.

Figure 1. Fish consumption by production sources.

1.80% 0.50% 1.30% Fresh fillet 35.30% Crustaceans Shellfish Frozen fish 56.60% Fresh fish Frozen fillet 4.50% From Shapiro 2007.

Figure 2. Percent (%) imports by products 2007.

The sources of the Israeli fishery from 2004-2007 and the catch values in the decade from 1998-2007 are shown in Tables 2 and 3, respectively. Of the total Israeli catch from all sources (24,866 MT) in 2007, aquaculture represented 77.1% or 19,168 MT while mariculture's share was only 9.1% or 2,251 MT. The relatively minor marine and Lake Kinneret sources contributed 2,607 MT (10.5%) and 840 MT (3.4%), respectively, to the total fishery. The annual catch values for aquaculture and mariculture over the decade of 1998- 2007 increased somewhat while prices per kg decreased moderately (Table 3). Table 4 lists the yields of the main aquaculture species over the decade 1998-2007. The two fresh water species representing the highest production in 2007 are tilapia (7,973 MT) and carp (6,737 MT), which are 42% and 35% of overall production, respectively. This is followed by mugilids (1,983 MT) and Chinese carp (1,135 MT) while there were modest amounts of trout (431 MT), striped bass (147 MT), barramundi (100 MT) and sea bream (17 MT). The aquaculture production and gross income in the 1998-2007 decade demonstrated a general increase from 16,654 MT to 19,168 MT (Table 4) due mostly to increases in tilapia, mugilids, Chinese carp and other species. On the other hand, gross income fluctuated during this decade falling from $62, 780,000 in 2003 to $57,224,000 in 2004 before increasing over the remaining years to $62, 224,000 in 2007 (Fig. 3). Aquaculture in Israel 159

20000 65000 60000 18000 55000 16000 50000

MT 45000

14000 $x1000 40000 12000 35000 10000 30000 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 Year

Value of yield Yield in MT From Shapiro 2007.

Figure 3. Aquaculture production and gross income in the last decade.

4000 20000

18000 3500 16000 3000 14000 2500 12000

2000 10000

Yield (MT) 8000 1500

6000 Yield value ($x1000) 1000 4000 500 2000

0 0 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 year

Total yield $ yield value

From Shapiro 2007.

Figure 4. Mariculture yield and value in last decade.

Table 3. Annual catch values and average prices per kg ($US) for the last decade

Med. Trawl Inshore Pelagic Marine Fishery Kinneret Aquaculture Mariculture Total Average Year X X X X X X X $/kg X$1000 $/kg $/kg $/kg $/kg $/kg $/kg $/kg $1000 $1000 $1000 $1000 $1000 $1000 $1000 1998 7207 5.11 9964 6.48 2911 2.45 20,077 4.68 3,359 1.55 55,106 3.31 15,016 7.90 93,558 3.76

1999 6612 4.32 9255 6.28 1527 2.07 17,394 4.23 3,168 1.48 45,492 2.78 19,001 7.89 85,055 3.45

2000 7263 4.94 13547 8.44 753 2.28 21,563 5.22 1,666 0.90 54,685 3.18 21,704 7.45 99,618 3.93

2001 8308 4.79 14833 8.99 589 1.67 23,730 5.15 1,615 1.26 57,944 3.19 21,405 6.77 104,694 4.26

2002 7036 4.43 10793 6.99 519 1.52 18,347 4.31 1,096 0.70 45,480 2.37 18,551 6.07 83,474 3.34

2003 6756 4.84 10084 8.82 781 1.73 17,621 5.13 984 0.92 42,725 2.42 19,289 6.20 80,620 3.64

2004 7091 5.08 8063 7.05 607 1.34 15,761 4.49 999 0.88 43,357 2.29 18,525 5.52 78,641 3.35

2005 12702 9.62 11283 8.08 1215 3.40 25,200 7.03 1,642 1.18 55,491 2.89 18,464 5.78 117,519 4.43

2006 10530 7.98 5597 8.08 892 1.97 17,019 6.01 1,938 1.21 55,028 2.84 17,833 6.55 91,817 4.05

2007 13,500 10.28 8815 11.59 1799 4.57 24,114 8.80 1,041 1.24 61,458 3.21 16,484 7.32 103,897 4.83 Modified from Shapiro 2007.

Table 4. Aquaculture Yield by Species from 1998-2007

Chinese Red European Sea Year Carp Tilapia Mugilids Trout Bass Barramundi Eel Other Total carps Drum sea bass bream

1998 7,172 6,691 1,476 451 707 157 16,654

1999 7,062 6,410 1,542 419 583 227 126 16,369

2000 6,281 7,059 1,661 744 605 302 532 17,184

2001 6,208 8,217 1,633 718 448 378 190 123 48 150 44 18,157

2002 7,748 7,819 1,824 616 374 495 107 39 66 95 17 19,200

2003 7,339 6,826 1,705 713 352 385 140 110 0 97 17,667

2004 5,765 9,270 1,792 903 331 292 323 180 15 78 18,949

2005 6,413 7,404 2,108 1,607 424 453 295 193 90 181 40 19,208

2006 6,560 8,235 2,087 1,102 449 290 350 122 115 72 19,382

2007 6,737 7,973 1,983 1,135 431 147 100 17 645 19,168 Modified from Shapiro 2007. 162 W. M. Koven, S. Harpaz, J. Van Rijn et al.

In 2007 fish mariculture production was 2,251 MT, which is down from 2,724 MT in 2006 and from an average of 3274 MT in 2004-5 (Table 5), and was worth about $16,500,000 (Figure 4). The reduction was mainly due to the decrease in the farming of gilthead sea bream (Sparus aurata), which is the main marine fish farmed in Israel (97% of mariculture production). Due to the alleged damage to coral reefs near Eilat, sea cages owned and operated by the private company Dag Suf and the kibbutz cooperative Ardag were removed from the Gulf of Aqaba.

Table 5. Mariculture yield by species in the last decade

Seafood 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007

Shellfish 2 1 2 1 1

Other 21 22 16 80 8 3 3 2 5 2

Striped bass 80 49 40 70 10 5

Red Drum 128 101 197 109 140 298 315 2 41 36

Eur. Sea bass 30 26 150 214 346 251 169 6 36 26

Sea bream 1,643 2,210 2,511 2,688 2,561 2,546 2,860 3,185 2,641 2,187

Total 1,902 2,408 2,914 3,161 3,056 3,110 3,353 3,196 2,724 2,251 Modified from Shapiro 2007.

Table 6. Mariculture production and fry sales in 2007

Product Sea bream Euro. Sea bass Red Drum Striped bass Other Total Harvested fish 2,187 26 36 0 2 2,251 Fingerlings (x1000) 9,296 1,300 2,362 2,370 1,800 17,128 Modified from Shapiro 2007.

Gilthead sea bream (known as denis in Israel) production continues along the Mediterranean coast at the Ardag farm in the Ashdod port (700 MT) and Dag hayam (Subflex submergible cages; 250-400 MT). A land based pilot farm for mainly sea bream, using the "Megaflow" approach (described later in chapter), is currently being operated and tested by Ardag on the site of the National Center for Mariculture (NCM), a branch of Israel Oceanographic and Limnological Research and produces up to 110 MT. Israeli marine fish hatcheries produced about 17.1 million fry of different species (Table 6) worth about $5,000,000 (Table 7). About 87% of the total fry production was for the local market while 13% was harvested for export (Figure 5). Of the total fry produced, approximately 9.3 million were sea bream, 1.3 million European sea bass, 2.4 million Red drum, 2.4 million striped bass and 1.8 million of other species (Table 6). Gilthead sea bream fry weighing 2-3 g sold for $ 0.27 each while juveniles of other species varied from $ 0.29- $0.31 each. The sale of fry in 2007 was about 23% of the total income of Israeli mariculture Aquaculture in Israel 163 which was an increase from about 18% in 2004-2006 and 14% in 2001-2003 (Table 7).There were about 2.2 million fry exported, which included 1.1 million hybrid bass (50%), about 1.1 million barramundi (49%) and 30,000 (1%) gilthead sea bream (Figure 6). The ornamental fish industry, which is mainly concentrated in the collective farms (moshavim) of the Arava valley in southern Israel, has shown a continuous upward trend in recent years and in 2007 was valued at about $17,000,000 (described later in chapter). The production and value of tropical and cold water ornamental fish in the decade 1998-2007 are shown in Figures 7and 8, respectively.

Table 7. Mariculture in the last decade

Fry Income No. Yield Yield ($) Price per Total value Year Production from Fry Farms (MT) $x1000 MT ($x1000) (x1000) ($x1000) 1998 2 1,902 12,414 6,527 9,056 2,647 15,061

1999 7 2,408 14,829 6,158 13,100 4,172 19,001

2000 7 2,914 18,496 6,347 11,664 3,208 21,704

2001 7 3,161 17,665 5,588 13,850 3,740 21,405

2002 9 3,056 16,124 5,276 9,677 2,427 18,551

2003 9 3,110 16,866 5,423 13,527 2,423 19,289

2004 7 3,353 18,525 5,524 14,548 3,757 22,282

2005 7 3,196 18,464 5,778 17,039 4,430 22,894

2006 7 2,725 17,833 6,546 17,307 4,129 21,962

2007 7 2,251 16,484 7,323 17,128 4,959 21,443 Modified from Shapiro 2007.

Fry production for export (13%)

Fry production for local market (87%)

From Shapiro 2007.

Figure 5. Total fry production for local market and export.

164 W. M. Koven, S. Harpaz, J. Van Rijn et al.

Sea bream (1%) Barramundi (49%) Striped bass (50%)

From Shapiro 2007.

Figure 6. Fry production for export.

35000 30000 25000 20000 Tropical fish 15000 Cold water fish 10000

No. of fish (x1000) 5000 0

07 998 999 000 001 002 003 004 005 006 0 1 1 2 2 2 2 2 2 2 2 Year From Shapiro 2007.

Figure 7. Ornamental fish Production: 1998-2007 (no. of fish x1000).

18000 16000 14000 12000 10000 Tropical fish 8000 Cold water fish 6000

Value (x$1000) 4000 2000 0

2 3 0 0 06 07 0 0 1998 1999 2000 2001 20 20 2004 2005 2 2 Year From Shapiro 2007.

Figure 8. Ornamental fish values (value x $1000). Aquaculture in Israel 165

NEW ADVANCES IN THE RESEARCH AND CULTURE OF THE MAIN FISH SPECIES

Gilthead Sea Bream (Sparus aurata)

The most farmed marine fish in Israel is the gilthead sea bream which represents about 97% of mariculture production. The Ardag Red Sea Mariculture Ltd fish hatchery, which has the capacity to produce up to 8 million fingerlings/year, was involved until recently in the grow-out of fingerling gilthead sea bream to market weight in sea cages in the Gulf of Aqaba collectively with the private company Dag Suf Ltd. (both companies producing about 2200 MT in 2007), until 2008. From 2005-2008 the sea cages were incrementally removed by a court decision concerning the alleged negative impact of effluent on the indigenous coral reef. Although the farming of gilthead sea bream is considered commercially successful in Israel and Europe, fish survival by the end of larval rearing remains at around 25-35%. Recent studies have focused on the manipulation of the stress response through the diet as a means to improve survival during larviculture. Koven et al (2001) reported that increased levels of dietary arachidonic acid (20:4n-6; ArA) in the live food markedly improved survival following the acute stress of tank transfer. van Anholt et al. (2004) investigating further the effect of dietary ArA on the response to an acute stressor (90 sec exposure to air) reported that different age sea bream larvae fed high ArA-containing Artemia sp., exhibited reduced cortisol levels compared to cohorts fed lower dietary levels of this essential fatty acid. The physiological underpinning of these findings is the enzymatic conversion of ArA into a broad range of highly biologically active metabolites, collectively known as eicosanoids. These paracrine and/or endocrine hormones participate in cellular regulation, hormone release, osmoregulation, and organ function in fish. The down regulation of cortisol appears to have given a survival advantage to larvae fed elevated ArA levels prior to exposure to acute handling stress. On the other hand, larvae exposed to daily salinity change demonstrated distinctly higher basal cortisol levels that significantly increased with rising ArA levels in the Artemia they consumed (Koven et al. 2003). These findings suggested that the effect of dietary ArA on cortisol production may be intimately linked to stress type. One of the major problems plaguing gilthead sea bream production, particularly in Europe, is the high rate of skeletal deformity (in excess of 30%) in juveniles and adult fish. Abnormally developing fish in production are costly as they have to be removed manually from the stock due to their poor growth and decreased market value. There is accumulating evidence that environmental factors as well as dietary components during larval rearing can have far reaching effects on the incidence of deformity during later development in juveniles and adults. Sandel et al (2010) investigated the effect of the ratio of the dietary phospholipids; phosphatidylcholine (PC) and phosphatidylinositol (PI) in larvae and juvenile gilthead sea bream. These authors found that reducing PI markedly increased jaw deformity which can have adverse affects on juvenile feeding on a dry hard starter feed resulting in reduced growth. These authors also found a strong correlation, in fish fed the high PI diet, between the mRNA expression of osteocalcin (BGP) and dietary PI. BGP is a vitamin K-requiring protein in bone hyroxyapatite that has a strong affinity for calcium and has been correlated with the mineralization of bone (Szulc et al., 1994; Simes et al., 2008). Inside the cell, it is known that 166 W. M. Koven, S. Harpaz, J. Van Rijn et al.

PI functions as a precursor of second messengers such as inositol 3 phosphate (IP3) that regulates calcium ions entry into the cell from the endoplasmatic reticulum (Cahu et al., 2003; Tocher et al., 2008). Sandel et al. (2010) concluded that a PC/PI ratio of 1.28 or a PI level of 3.04 g per 100 g DW diet gave the best larval and fry performance. Vitamin A studies during larviculture and their consequent effect on malformation in older fish was also carried out at our laboratory (NCM). Ginzbourg et al. (2009) found vitamin A fed to gilthead sea bream larvae significantly affected growth and skeletal deformity in the fry. These authors concluded that from 4-20 days post hatching (dph), there was a dose response effect between rotifer vitamin A level and cranium deformity while between 20-34 dph a correlation was found between Artemia vitamin A level and skeletal deformity. It was calculated that the level of vitamin A that is associated with the best performance in terms of growth promotion and reduced rate of deformities is within the range of 0.5-3.9 μg retinoid/g wet weight in the live food and 0.4 μg retinoid/g wet weight in the larvae. The effect of salinity and temperature during larval rearing on the appearance of deformities later on in development in gilthead sea bream was also investigated at our laboratory (NCM). Koven et al. (in preparation) reported that the high ambient salinity of the Red Sea (40%) during larval rearing reduced the percent of swim bladder inflation, survival and increased skeletal deformities in juveniles. On the other hand and at odds with a similar study on sea bass (Georgakopoulou et al. 2007) gilthead sea bream larval rearing temperature had no significant effect on spinal deformities such as lordosis, vertebral compression, pre-haemal kyphosis and pre-haemal lordosis. Noteworthy is that the overall level of deformities in fish examined in this study was very low (1.7%) which is typical of Israeli mariculture and contrasts starkly with the >30% deformity reported in Europe. This may be related to the fact that sea bream broodstock originates mainly from production in the warmer waters of the Red Sea (21-27 °C). Consequently these fish have been indirectly selected for improved performance at higher temperatures leading to the progeny exhibiting lower levels of skeletal abnormality. In addition, there is a very active broodstock selection program in Israel which encourages genetic variability that further reduces skeletal deformity. During grow-out, fish feed can represent more than 50% of the production costs. Consequently it is imperative that the food pellets deliver the optimum balance of protein and energy to the fish in order to realize maximum and cost effective growth that minimizes nitrogen secretion and fish waste. This is becoming particularly important as environmentally-aware regulatory bodies are increasingly limiting waste output and/or feed quotas from commercial farms. A significant step forward was made by Lupatsch et al. (2003a) who quantified the daily energy and protein requirement in gilthead sea bream by using a factorial approach, which has been implemented to optimize feed formulations and feeding regimes. These authors found that sea bream can grow from 1 to 379 g in one year at an average water temperature of 23°C. The protein content per g live weight had an average of 176 mg/g fish. In contrast, lipid increased with fish size (5-11kJ/g live weight) rising from 43 to 186 mg/g live weight for market size fish of about 400g. This means that gilthead are a fattier fish and require more energy per unit weight gain than leaner fish such as the red drum (69 mg lipid/g live weight; Aquaculture in Israel 167

Thoman et al. 1999), turbot (38 mg/g lw; Regost et al. 2001) and rainbow trout (146 mg lipid/g live weight; Dias et al., 1999). Taken altogether, the results facilitate the calculation of the daily recommended energy and protein intakes for growing gilthead sea bream by quantifying the demands of the fish for maintenance and growth. Although protein and energy demands are constantly changing in gilthead sea bream, it is clearly impractical to produce different diets for various stages of growth. A better approach would be to feed lower 15 mJ/kg energy diets to small fish with a capacity for high feed intake as it is difficult to produce a 18 mJ energy, 60% protein pellet for this size fish. Above 200 g a higher energy diet, with a digestible energy content of at least 18 mJ/kg (incorporating more lipid), can be fed as the amount of 15 mJ/kg feed that these fish would have to consume would approach the physical limitations of the fish.

FISH FOOD YIELD (100% NITROGEN) SEA WATER (% NITROGEN)

BIODEPOSITS FISH PONDS FISH 25% PN 54% BIODEPOSITS 10% DN 10% DN SEDIMENTATION BIVALVES PONDS 12%

16% S PN 18.5% T I BIODEPOSITS

DN 18.5% O

N P DN

6% I

B PN 2.0% BIVALVE BIVALVE 4% DN 25% POLISHING ______FILTRATION TOTAL UNIT 32 % PN 1.8% SEAWEED 22% DN 2.3% SEAWEED UNIT

SEDIMENTATION TOTAL 63% ENITRIFICATION SEA WATER Figure 9. Flow diagram of nitrogen in the proposed integrated system. All the numbers are percentages of the N introduced in the fish feed (PN = particulate nitrogen; DN = dissolved nitrogen; Biodeposits = faeces and uneaten food). (After Shpigel et al., 1993a). 168 W. M. Koven, S. Harpaz, J. Van Rijn et al.

Figure 10. Typical layout of Mega-flow Low-head recirculating system.

Figure 11. A semi-commercial scale of Mega-flow system operated in Eilat, producing 100 ton per year. Aquaculture in Israel 169

Grouper (Epinephelus aeneus)

Although it is not a main aquaculture species in Israel, there has been increasing focus on the commercial farming of the white grouper (Epinephelus aeneus) which has high market value (average $10/kg) and a rapid growth rate (1g to 1kg in the first year). During 2009-2010 around 100,000 post larvae were produced at both the National Center for Mariculture (NCM) in Eilat and Kibbutz Magan Michael near Haifa. An F1 grouper broodstock fed a pelleted feed and maintained at the NCM has spontaneously spawned for 12 months (March 2009- March 2010) under ambient photoperiod and regulated water temperature. However, many fish during grow out at both locations have been stricken with viral nervous necrosis (VNN) which presently has no known cure and remains a serious impediment to mass production. Another obstacle to the successful rearing of this promising species is the high mortality characterizing early larval rearing. One limiting factor in the survival of grouper pre-larvae is their minute size following hatching (<1.5 mm) accompanied by a very small mouth gape (≤ 100 µm). This means that once the relatively small yolk sac has been depleted after endogenous feeding a few days after hatching, the larvae, having pigmented eyes and an open digestive tract, must learn very quickly to successfully hunt and feed on zooplankton prey. In fact, if grouper larvae are not sufficiently ingesting a suitably sized and nutritious food particle within the first day of exogenous feeding, they will quickly pass the point of no return (PNR) where the digestive tract deteriorates irrevocably (Yufera and Darias 2007). The period between mouth opening and the PNR varies among species but generally depends on water temperature (Dou et al., 2002, 2005) and larval length (Miller et al. 1988). In grouper, the rapid onset of irreversible starvation makes it highly unlikely the larvae will survive past the PNR. Recently, the NCM has successfully implemented a mesocosm approach in the rearing of the white grouper, which has been modified from a previous published protocol (Papandroulakis et al., 2005). This approach is based on allowing the natural productivity of seawater to develop through exposure to sunlight, warm temperatures and nutrient supplementation resulting in a variety of algal and zooplankton species (e.g. copepods and ciliates) (Russo et al. 2009) many of which will be nutritious and suitably sized for feeding larvae. Unsuccessful metamorphosis in grouper larvae is frequently characterized by heterotrophic growth, poor pigmentation, cannibalism and generally high mortality. Cannibalized larvae are often pre-metamorphosing fish exhibiting elongated dorsal and ventral spines that cause these individuals to be particularly sensitive to handling and vulnerable to their larger more developed siblings who have already passed through metamorphosis (Folkvord and Ottera, 1993; Baras, 2000; Baras and d’Almeida, 2001). The heterotrophic growth resulting from asynchronous metamorphosis and the subsequent cannibalism is a major factor reducing fish production in this species (Fukuhara and Fushimi, 1988; Lim, 1993; Watanabe et al., 1996; Hseu, 2002). A main obstacle in grouper culture has been the development of a grow-out diet that can optimize the rapid growth rate of this species which has made it such a compelling mariculture candidate. Similarly to gilthead sea bream, Lupatsch and Kissil (2005) quantified the daily energy and protein requirement in this species by using a factorial approach which has been implemented to optimize feed formulations and feeding regimes. In this approach the authors defined the potential for growth at different weights and at various water temperatures based on feeding to satiation. They predicted the amount of feed 170 W. M. Koven, S. Harpaz, J. Van Rijn et al. that a fish is physically capable of consuming which can be ascertained by adjusting its energy and protein content which, in turn, determines food intake. Their model predicted that white grouper would grow from 1g to 1kg in 1 year at 24 °C and that the maintenance requirement for energy in grouper was lower than sea bream and sea bass. Taken together, this study facilitated the calculation of the daily recommended intake for growing white grouper.

Figure 12. Scheme of a zero-discharge system configuration used for culture of freshwater and marine fish (not to scale).

Figure 13. A 50 tonnes annual production segment of a zero-discharge, gilthead sea bream production facility operated by Local Ocean Ltd. in Hudson (NY). Aquaculture in Israel 171

European Sea Bass (Dicentrarchus labrax)

The European sea bass in captivity demonstrate a highly skewed sex ratio to males (70- 99%) (Chatain et al. 1999; Gorshkov et al. 1999) in the population while in nature females are reported to be more numerous (Arias, 1980). This suggests that culture conditions prevailing in the farming of this species encourages the predominance of males which grow 20-40% less than females (Gorshkov et al. 1999; Saillant et al. 2001). Mylonas et al. (2005) found that North-West (NW) and South-East (SE) Mediterranean strain females exhibited a growth advantage over males with an average of 17%. Gorshkov et al. (1999) found that larger sea bass females displayed sexual dimorphism in length and weight before sexual maturity (10-12 months) and that these patterns occurred in all strains and crosses. This is primarily due to males maturing faster than females thereby diverting energy for somatic growth to testicular growth, milt production and breeding behaviour. Mylonas et al. (2005) found that lowering the rearing temperatures during the larval and nursery stages influenced sex ratios in the NE and SE Mediterranean strains. These authors concluded that decreasing the rearing temperature from 21 to 15 °C markedly increased the number of females in the population although a further temperature decrease had no apparent effect. Under these conditions the proportion of females in the population reached 65% which agrees well with 74% (Pavlidis et al. 2000) and 66% (Koumoundouros et al. 2002) in other similar studies. Moreover, it appears that the larval period is more sensitive than the nursery period in skewing the population towards females. In fact, Koumoundouros et al. (2002) succeeded to increase the number of females in the population by decreasing the temperature at a very early developmental period (30 h post fertilization to 7 dph). These results are particularly intriguing as environmental temperature appears to influence sex differentiation months earlier than when gonadal differentiation occurs at 125 dph or 6.2 cm TL (Saillant et al., 2003). On the other hand, extending the period of temperature decrease will reduce the percentage of females in the population. A protracted period of low temperature exposure will reduce growth rate and the ability to achieve a critical body size which ultimately hinders differentiation to females. It remains unclear how temperature exposure during early development effects changes in sex steroids. In Nile tilapia masculinization was associated with the repression of brain aromatase expression (D'Cotta et al., 2001). Temperature might effect the pituitary expression of luteinizing hormone (LH) and follicle stimulating hormone (FSH) prior to the period of sex differentiation (Miranda et al. 2001) suggesting that the hypothalamus-pituitary system may be modulated by temperature changing its effects on sex differentiation. In 1976 and 1982 the "French’ strain of European sea bass was imported from France to Israel (Gorshkov et al., 1999). These fish were adapted to conditions of the northern part of the Mediterranean but the strain was unsuitable for the warmer waters of the Red Sea where the dominant culture of this species occurred. This meant that the farming of the French strain remained limited in Israel and was constrained further to due to an outbreak of Mycobacterium marinum that began in 1990. Taken altogether both environmental and genetic factors negatively impacted on commercial sea bass culture in Israel leading to a drastic reduction in production by the mid-1990s (Colorni et al., 1997). Despite the decline in the importance of this species in Israeli aquaculture in recent years, Tibaldi et al. (2006) evaluated the effect of replacing fish meal with differently processed soybean meals on growth performance, apparent digestibility coefficients, activity of alkaline 172 W. M. Koven, S. Harpaz, J. Van Rijn et al. phosphatase and the brush border enzymes leucine amino peptidase, maltase and γ-glutamyl transpeptidase as well as fish morphometrics and flesh quality. It is well documented that soybean meals, although equally palatable to fish meal (Tibaldi et al. 2006), can affect the bioavailability of nutrients. Soybean meals must be heat treated to inactivate anti-nutritional factors (ANF) that can affect protease activity as well as being deficient in specific minerals and sulfur containing amino acids, such as methionine (Viola et al.1983; Wilson and Poe, 1985; Van der Ingh et al. 1991). Tibaldi et al. (2006) found that BBME activity of leucine amino peptidase and maltase was similar when feeding fish diets containing fish meal or various treatments of soybean meals. On the other hand, these authors argued that nutrient availability in sea bass fed soy bean meals is adversely affected due to non-starch polysaccharides affecting digesta viscosity and to a much lesser extent ANFs. These authors reported that, under an unrestricted feeding regime, standard dehulled-toasted and solvent extracted soybean meal successfully replaced 25% of fish meal in sea bass. Feeding levels and conversion efficiencies in European sea bass, as expected, are different than those of other cultured species in Israel. Lupatsch et al. (2003b) compared the maintenance and growth requirements between gilthead sea bream, white grouper and sea bass using, as described previously for digestible energy (DE), a factorial approach. Under similar conditions and satiation feeding, sea bass exhibited the slowest growth over 12 months (325 g) compared to sea bream (380 g) and grouper (750 g). The composition of the growth in 400 g fish was similar in all three species in protein content (170 mg/g) but differed in the energy component, where sea bass was 9.8 kJ/g, sea bream was 10.7 kJ/g while grouper was the leanest at 7.0 kJ/g. These authors measured the daily energy loss of these species and found that sea bass was less (35.3 kJ) than gilthead sea bream (40 kJ) whereas grouper had the lowest maintenance requirement (24.9 kJ) due to its sedentary life style. On the other hand, the energy efficiency of DE to deposit energy as growth was very similar in all species. These authors argued that this reinforces the concept that energy efficiencies for growth are constant and independent of fish weight, feeding level and species where the maintenance requirement is species-specific.

Carp The practical cross breeds of carp exhibiting heterosis, in terms of improved growth performance and other qualitative features, are the basis for carp aquaculture in Israel (Hulata, 2001) and were mainly developed at the experimental station in Dor (Wohlfarth, 1993). Over the years, one of the most suitable cyprinid hybrids tested for production were the two reciprocal crosses between silver carp (Hypophthalmichthys molitrix Valenciennes) and bighead carp (Aristichthys nobilis Val.) which show higher survival and yield than the parental species (Issa et al., 1986). This hybrid was handled more easily than pure silver carp and commercially cultured in Israel during the 1970’s to 1980’s but was eventually discontinued due to limited markets. All female common carp populations (Cherfas et al. 1996) have been established in Israel by employing sex reversal of XX gynogenetic females to males (Gomelsky et al., 1994) and then using these phenotypic males for breeding. The resultant all female fry showed a 10-15% increased yield over existing commercial stocks. Interestingly, Tzchori et al. (2004) induced sex inversion of genetically female common carp to males, at a level of 97%, through the use of the aromatase inhibitor fadrozole in a dose dependent manner. These results verified the central role of aromatase in sex determination during the labile period in common carp regardless of genotype. Aquaculture in Israel 173

A very serious disease outbreak in carp that started in 1998 resulted in 80% mortality of fish stocks in local farms along the coastal plain in Israel by 2000. During 1999-2002 carp production decreased by 60% while Koi export to Europe declined 75%. Clinical signs included severe gill necrosis, dry skin and sunken eyes (Perelberg et al., 2008). It was determined that the causal agent was viral (CyHV–3) and that outbreaks were water temperature dependent. The permissive range was 21-25 °C while clinical signs and mortality decreased significantly in water temperature above 29 °C. Recently Israeli researchers have developed a vaccine based on an attenuated strain that showed 80% survival in carp exposed to the disease (Perelberg et al., 2008). The vaccine has now been patented and the usage rights have been purchased by the Israeli company Kovax Ltd.

Tilapia The most extensive culture of predominant male hybrid tilapias is in Israel. Male progeny are produced by the crossing of brood stock from pure species, generally between the Nile tilapia Oreochromis niloticus and the blue tilapia Oreochromis aureus. There was also all male progeny produced early on by crosses with O. niloticus and O. hornorum but was characterized by low fry production (Wohlfarth et al. 1983, 1990). Fry production was improved by replacing the O. niloticus Bouake strain with the Ghana strain. Nevertheless, these fry did not have an attractive appearance and they were never commercially used to stock ponds. The main obstacle in the hybrid approach is the maintenance of pure stocks which requires extreme vigilance. Managed hatchery systems frequently break down due the infiltration of parental brood stock by individuals of different genotype, predominantly hybrids of the pure stock which are difficult to distinguish from their parents (Wohlfarth, 1994). On the other hand, the advantages of hybridization is that it avoids inbreeding and any adverse effect on the environment with sex hormones (Wohlfarth, 1994). In support of this Sde Eliyahu claims to be the largest tilapia hatchery in the country producing 30 million hybrid fingerlings/year from O. auria and O. nilotica. Another approach to produce hybrid male populations is the use of sex inversion which is relatively easy to use and generally economical to implement. In the past, F1 hybrids were used as brood stock and their progeny (F2) sex inverted (Rothbard et al. 1983) because they may be more fecund than the F1 parents (Verdegem 1987). On the other hand, this approach falters as F2 individuals grow more slowly and variably. Moreover and perhaps more importantly there are regulatory issues in the use of sex steroids and the market product may become increasingly less acceptable to an environmentally aware consumer. The Negev desert and its eastern part, the Arava valley, possess impressive reserves of underground saline and geothermal water. Super intensive tilapia fish farms using geothermal water have developed in these areas (Rothbard 2002). Fry are produced by the crossing of female O. niloticus with male O. aureus or spawning of red tilapia and then sex-reversed using male hormones. Grow out comprises a number of stages. First the fry are reared in intensive nursing ponds to fingerlings of 5 g and then transferred to rearing ponds where they are grown to 80-120 g. These fish are further cultured in "fattening ponds" to the market size of 500-700 g over 6-8 months at densities of 20-27 kg/m3 (Rothbard, 2002). In recent years the organic culture of tilapia has been tested at the kibbutz Geva fish farm in Jezreel valley. From 2000-2003 stocking density in the organic pond varied from 11,000 to 14,000 fish/ha of which 80-90% were tilapia, as well as red drum and Chinese carp with an expected yield of 10 MT. However, a major constraint limiting the profitability of this 174 W. M. Koven, S. Harpaz, J. Van Rijn et al. approach is the cost of organic fish feeds which are restricted in their use of traditional fish and soy meals. A potential solution is to increase the natural productivity by using a periphyton-based system. This is done by placing hard surfaces in the water column to allow the establishment of sessile autotrophic and heterotrophic populations, which increases the natural productivity of the water body that serves as food for the cultured organisms. Milstein et al. (2005) immersed plastic surfaces equivalent to 40% of the pond surface area in polyculture ponds containing hybrid tilapia (Oreochromis niloticus x O. aureus) as well as minor levels of other species. The tilapia were fed 60% of the normal feed ration leading to only a 10% reduction in the tilapia growth rate and yield. This attests to the potential of periphyton-based aquaculture to reduce production costs and facilitating the viability of organic culture of tilapia in Israel. Saprolegnia infections or saprolegniosis is observed on a variety of fish species including tilapia as pale patches of filamentous mycelium on the fins. If left untreated the infection leads to death by haemodilution usually in the colder winter months. Malachite Green was the most effective fungicide for this disease. In 2003, Israel as well as other countries, declared a prohibition on the use of malachite green due to its alleged carcinogenic, mutagenic and teratogenic effects. Until recently, there was no effective alternative fungicide to treat this disease. S. parasitica infections have a serious impact on the aquaculture sector in general and tilapia culture in particular. Consequently, it was an imperative to find an effective alternative to Malachite Green in order to manage saprolegniasis at acceptable levels. Polacheck (2007) has shown that a diaminostilbene derivative compound called Blankophor BA was found to be a very effective at relatively low concentrations against S. parasitica in tilapia while exhibiting low toxicity to the fish. This invention is now is now being patented (USPTO Patent Application 20090252768).

ORNAMENTAL FISH PRODUCTION

Production of ornamental fish is a relatively young branch of aquaculture in Israel. It took off in the 1980's, beginning with hobbyists who decided to turn their love of the ornamental fish into a business. Mag Noy (a coldwater fish producer) pioneered the field in Israel, launching the first serious export of ornamental fish in 1984, and developing a partnership in 2001with Agrexco (the main agricultural produce exporter in Israel). Only in the late 1990's did the business really settle down to become a proper economic branch in Israel. By 2000 Israel was 10th in the world in revenue from ornamental fish. Singapore, which until then had been the world leader in ornamental fish, suddenly experienced problems in its production, which may have been caused by a virus. The vacuum left by the depleted Singapore stock was filled by Israeli producers. The key to breeding tropical fish is the strength and quality of the fish. Reliability and better methods of raising the fish are the key to Israel's ascendance in the field, particularly in European markets. Whereas their competitors in the Far East still raise their fish mainly on traditional farms, using mud ponds dug in the ground which offer little chance for monitoring disease and quality, Israel's fish farms use mainly indoor and controlled systems. Reliability in producing strong healthy fish is serving Israel well against strong competition still offered by countries like Malaysia, Singapore and the Czech Republic. Aquaculture in Israel 175

Cold water ornamental fish are concentrated in five large farms producing mainly ornamental carp (Koi) and predominantly using outdoor earthen ponds. In addition, there are a number of smaller farms using closed re-circulating systems. Exports total around 12 million US dollars per annum. Tropical warm water ornamental fish includes live bearers and egg layers and there are a total number of about 40 farms in the country of which 6-8 can be considered as large i.e. production exceeding 250,000 US dollars per annum. Live bearers are mainly guppy (Poecilia reticulata) and over 40 varieties are produced, including an array of different colors and body/tail shapes as well as many platy (Xiphophorus sp.) varieties. About 40% of the guppies imported to Europe come from Israel. On the other hand, the egg layers are mostly cichlids including various ornamental African cichlids. Of the South American cichlids, the main species reared are angel fish (Pterophyllum scalare) and discus fish (Symphysodon aequifasciata). All farms use closed re-circulating systems. Most of the large farms are located in the desert and their isolated location helps in preventing diseases. The total exports from this branch are around 8 million US dollars per annum. Marine ornamental fish includes one farm close to the Red Sea and three other farms located about 100 km from the sea, all using closed re-circulating systems. They produce mainly 5 species of clown fish (Amphiprion), the major one being A. ocellaris (known as Nemo fish). This is a fairly new branch with a monthly production of 7,000-10,000 fish. The research scientists, extension officers and farmers work closely together to solve problems which arise during the production process. The following selected topics briefly describe several research projects which have been conducted with the aim of enhancing the capabilities of the ornamental fish industry in Israel.

Genetic Improvement of Color and Reproduction

A study aimed at better understanding the patterns of color inheritance in an ornamental cichlid (Cichlasoma nigrofasciatum) was conducted by Itzkovich et al., (1991). They suggested a simple Mendelian model, with two alleles at an autosomal locus for the inheritance of the two color phenotypes of Cichlasoma nigrofasciatum: the dominant (wild type) allele causes a dark grey colouration, while the recessive phenotype is pink. A number of studies have also been conducted in order to induce diploid gynogenesis and polyploidy in ornamental koi carp, (Cyprinus carpio) (Cherfas et al., 1993). The methods used were similar to those employed for the edible carp and showed promise for obtaining better color patterns in the fish.

Koi Herpes Virus Koi herpes virus (KHV) is the cause of a worldwide mortal disease affecting ornamental koi and common carps (Cyprinus carpio). The virus induces a lethal disease at the transient seasons, when water temperature ranges between 18 and 25 degrees Co. The impact of the KHV following its first detection in Israel in 1998 on both the ornamental and edible carp was extremely severe. The production dropped very steeply over a short period of time and the virus spread to many farms. The consolidated efforts of researchers, extension officers and farmers in Israel have led to the isolation of attenuated non-pathogenic viruses that render virus-vaccinated carps resistant to the disease. Furthermore, the vaccinated fish developed 176 W. M. Koven, S. Harpaz, J. Van Rijn et al. high levels of antibodies against the virus (Ronen et al., 2003). This attenuated virus could be used as a live vaccine for the eradication of the lethal disease afflicting common and ornamental carp fisheries in many countries. Further studies have led to better understanding of the virility of this virus (Dishon et al., 2007). The leading role of the research carried out on this virus has led to the establishment of Kovax Ltd - a company specializing in aquaculture vaccines. In 2008 an international workshop on the Koi herpes virus was held in Israel.

Food Presentation A research project was conducted by Harpaz et al., (2005) to test the effects of feeding guppy (Poecilia reticulata) fry a diet offered as either powder or flakes on their growth and survival. The results of the 8 week experiment showed that the growth of both male and female fish was considerably enhanced when the diet was presented in the form of a finely ground powder compared with a flake form. Final average weights of fish given a diet containing the exact same ingredients (44.9% protein and 6.1% fat) from the same batch of raw materials in the powdered form were 280.0 ± 12.1 mg compared with 114.6 ± 19.9 mg for the diet given in the form of flakes. In a diet that had a higher fat level (45.1% protein and 10.6% fat) the difference in final weight attained was even more dramatic 303.9 ± 16.7 mg for the powder fed fish compared with 92.6 ± 12.5 mg for the flake fed fish.

Color Enhancement Harpaz and Padowicz (2007) examined the effects of carotenoids, derived from paprika (oleoresin paprika) added to fish feeds, on their expression in the dwarf cichlid Microgeophagus ramirezi fish, including accumulation levels, color intensity, growth rate and survival. Assimilation of carotenoids in the fish body at varying levels of carotenoid addition 60mg/kg or 240mg/kg were evaluated. The results clearly show that the addition of carotenoids to the diet had no effect on the growth rate or the survival of the fish. On the other hand, a significant difference in levels of carotenoid accumulation over the 75 day period was found between the treatments fed with carotenoids and the control. The fish that consumed food containing 240mg/kg carotenoids accumulated significantly more carotenoids in their body (59.34±3.93µg/gram dry matter) compared with fish that consumed food containing 60mg/kg carotenoids (40.53±2.37 µg/gram dry matter). Fish that had no carotenoid addition accumulated 29.18µg/gram dry matter. Visual examination of the fish showed a strong correlation between pigment accumulation level and color appearance in the fish.

Feed Additives: L-carnitine L-Carnitine (L-β-hydroxy-γ-N,N,N-trimethylaminobutyric acid) is a derivative of the amino acid lysine and a non-essential organic nutrient, sometimes referred to as a quasi amino acid, required for entry of long-chain fatty acids (such as acylcarnitine esters) into the mitochondria. It plays an important role in energy production by chaperoning activated fatty acids (acyl-CoA) into the mitochondrial matrix for metabolism. Carnitine is therefore a normal constituent of animal tissues and plasma, which is required for the transport of long- chain fatty acids to the site of oxidation. Aquaculture in Israel 177

Based on its role in vertebrates, the use of L-carnitine supplementation in fish diets in aquaculture has been advocated for multi functional purposes that include:

(1) As a growth promoter, specifically aiding in the utilization of high fat levels in the diet and thus providing a protein sparing effect (2) Alleviating stress related to toxic levels of ammonia, water temperature extremes and facilitating better acclimation to water temperature changes (3) Enhancing reproduction.

Contrary to its role as a potential growth enhancer, no effect of L-carnitine supplementation on ornamental fish growth was observed by Harpaz et al. (1999) in the ornamental cichlid (Pelvicachromis pulcher) nor by Dzikowsi et al. (2001) who studied the effect of temperature and diets supplemented with 1100 mg/kg food of L-carnitine on the reproductive performance of female live-bearer guppy fish (Poecilia reticulata) and found that the temperature had a significant effect on the brood size and brood interval, but the L- carnitine did not. On the other hand, a marked reduction in stress related cold shock deaths was shown in the case of the warm water ornamental cichlid fish Pelvicachromis pulcher fed varying levels of L-carnitine supplementation (0, 500, 1000 and 2000 mg/kg diet). Fish fed diets supplemented with L-carnitine (at all levels of supplementation) exhibited a higher survival rate after exposure to a severe cold shock, compared with the control fish fed a diet that was not supplemented with L-carnitine (Harpaz et al., 1999). It should be noted that increased carnitine concentrations may be required for oxidation of lipids when there is a clear need for energy as a result of cold acclimation and similar acute environmental conditions.

Enhancement of Reproduction Dzikowsi et al. (2004) conducted research on the effects of exposing fish to a potential predator and they showed that the reproductive plasticity of the guppy Poecilia reticulata can be induced in response to predation cues. The number of offspring produced by guppy female fish was significantly enhanced when the fish were exposed to a potential predator even though it did not have direct contact with the guppies.

Counting and Sorting Ornamental Fish Using Image Processing Ornamental fish farms in Israel practice daily counting of the spawned fry and sorting of fish. Tens of thousands of fry are manually counted daily in the larger farms, for feed management and stock assessment. A system for counting day-old ornamental fry has been developed and tested. Sorting of fish is possible as well, based on image processing and has been found to be very accurate (Karplus et al., 2005; Zion et al., 2008).

INTEGRATIVE SYSTEMS

The nutrient release from aquaculture operations can severely impact on water quality, conflict with regulations protecting recreational areas and multi-use coastlines as well as posing a health threat to marine and freshwater species that are in proximity to commercial 178 W. M. Koven, S. Harpaz, J. Van Rijn et al. cage farming or exposed to their effluent. Only 20-30% of feed protein nitrogen, the most expensive component in aquatic diets, is retained in farmed fish and shrimp, while the rest is secreted in the feces or as dissolved reduced N (ammonia and organic N). This represents a profound waste of this key nutrient as well as being the dominant source of fish farm pollution. Moreover, the public image and expansion of the aquaculture industry is justifiably being questioned by an increasingly environmentally aware public. As a general rule, the treatment of fish effluent from sea cages in open water is very problematic. On the other hand, the mariculture of coral recruits (spats, nubbins, coral fragments and small coral colonies ) in mid-water (depth of 6 m and 14 m above the sea bottom) floating nurseries that were meters from commercial fish cages in the Gulf of Aqaba showed superior growth in the nutrient rich waters (Rinkevich 2007; Amar and Rinkevich 2007). Nevertheless, aquaculture water treatment would be greatly assisted if fish were grown in land based pond systems and facilities. However, the costs of land based operations are considerably higher than sea cages in terms of infrastructure, land use and operation, water pumping, maintenance of acceptable water quality and treatment of organic waste in pond effluent. An effective approach to the water treatment of in-land fish farm effluent is biofiltration and this has formed the basis for the integrative pond approach in Eilat, Israel. Biofiltration of fish pond effluent has the benefit of reducing water pollution and exchange rates which means lower pumping costs. Organisms involved in biofiltration can be bacteria (van Rijn 1996), which convert waste carbon and nitrogen into gasses while microalgae (Neori and Krom , 1991), macroalgae (Neori, 1996) and suspension feeders (Shpigel and Blaylock, 1991; Shpigel et al., 1997) assimilate these nutrients into their biomass. Single pond polyculture systems are limited for intensification due to conflicting requirements of the different organisms grown in the same pond. Alternatively, the integrated system developed in Eilat is modular where the different biofilter species and suspension feeders are reared in separate holding facilities. This means that implementing biofiltration further adds to the production costs per kg fish in terms of added space, infrastructure, manpower and energy. On the other hand, this approach has the potential to boost the profitability of land based fish ponds (Shpigel and Neori, 1996; Neori et al., 2000) by producing commercially valuable aquatic products directly (seaweeds for human consumption and the phycoid-colloid industry) or indirectly (pond detritus fed to mullet, microalgae for oysters and clams, macroalgae for sea urchins and abalone). Microalgae in the fish ponds at the National Center for Mariculture (NCM) in Eilat are efficient biofiltration units that contribute dissolved oxygen to the growing medium while increasing their protein biomass by absorbing CO2, ammonia and phosphate (Krom and Neori, 1989; Neori and Krom, 1991). Pond algae readily bloom in this region due to the copious sunlight, in situ nutrient rich water and low to medium water exchange rates (2 exchanges/day) (Krom et al., 1989a, b; Neori et al., 1989). The dominant algal species in the fish ponds at the NCM are Olithodiscus spp., Chlorella spp., Tetraselmis spp., Chaetocerous spp., or Pyramimonas spp. The result is that high water quality is maintained in these ponds although levels can be reduced by grazing heterotrophic microflagellates and ciliates (Neori et al., 1989). After a series of studies, the macroalgae or seaweed Ulva lactuca has become the selected fish pond biofilter at the NCM (Neori et al., 1989; Vandermeulen and Gordin, 1990; Shpigel et al., 1993b; Jimenez del Rio et al., 1996). The seaweed Gracilaria conferta was also Aquaculture in Israel 179 investigated as a suitable candidate but proved to be lest robust under local environmental conditions. Neori et al. (1993) found the optimal density of U. lactuca was 1 kg/m2 while the nutrient uptake, yield and protein content was also determined (Vandermeulen and Gordin, 1990, Cohen and Neori, 1991, Neori and Krom, 1991, Israel et al., 1995, Neori, 1996). Their findings showed that the rate of ammonia supplied correlated positively with the seaweed removal rate but negatively with the efficiency of extraction. For example a supply rate of 2 less than 2 g of ammonia-N/m /day, resulted in U. lactuca removing over 80% of the NH3 from the water. However, when the supply rate increased to 7 g ammonia-N/ m2/d, which is the annual average, the efficiency of removal of the ammonia-N load dropped to 50% suggesting that a supply of 5 g ammonia-N/m2/d would be the most effective in terms of uptake and efficiency (Shpigel and Neori, 2007). In contrast, U. lactuca yield and percent protein content both increased with ammonia load. As fish are fed less in the cooler temperatures of winter which in turn seasonally affects the ammonia nitrogen flux, seaweed yields varied from 70 g/m2/d in winter to over 350 g/m2/d in summer. Similarly U. lactuca biomass can have 2-4 times more protein (up to 40% DW) during the highest ammonia load fluxes than found in this species in nature (Neori, 1996). On the other hand, other nitrogen molecular species such as nitrate are taken up much less efficiently (Neori, 1996). Filter-feeders such as bivalves filter microalgae which reduces turbidity and converts non-digestible particles into quickly settling feces and pseudofeces (Mariojouls and Kusuki, 1987). The development of a practical intensive culture of bivalves in phytoplankton-rich effluent has been well documented in a series of papers (Shpigel and Friedman, 1990; Shpigel and Blaylock, 1991; Shpigel et al, 1993a, 1993b; Neori and Shpigel, 1999; Neori et al., 2001). An important finding was that algal laden water from fish ponds, containing Chlorella, Tetraselmis, Chaetocerous and Piramimonas spp., that drained into a separate sedimentation pond produced a mixed planktonic microalgae and in situ benthic diatom (Navicula, Amphora and Nitchzia species) mixture. This was particularly nutritious for bivalves and promoted growth much better than oysters in tanks fed algae directly from single or multiple fish ponds. This was primarily due to periodic algal crashes in these ponds precipitated by vigorous grazing by heterotrophic microflagellates and microciliates. It was concluded that three factors are responsible for enhanced growth of bivalves; (1) a highly diverse mixed diet, (2) additional nutritious food from benthic diatoms, and (3) a stable algal concentration. As a result the Eilat integrated system supported high rates and production of the oyster Crassostrea gigas (0.7% d-1; stocking densities of 20-40 kg/m-3 , in tanks) and the clam Tapes philippinarum (0.6% d-1; stocking densities of 5-9 kg m-2 , on the bottom of the sedimentation pond) (Shpigel et al., 1993a; Shpigel and Neori, 1996). These findings further advanced the integrated pond concept in Eilat. Today the fish from intensive culture in outdoor fish ponds assimilate about 21% of feed protein nitrogen. The remaining nitrogen compounds together with copious sunlight produce algal laden water (1-3 g N/m2/d) which drains into an earthen sedimentation pond. From here the water flows through tanks with bivalves (polishing reactors) which will strip particulate matter (0.5-1 g N/ kg/d) from the medium representing about 15% of the original feed nitrogen. At this point, about 32% of the original feed nitrogen input into the fish pond is now trapped in feces, pseudofeces and uneaten fish feed sinking to the bottom. The water then flows into separate modules containing U. lactacus which will remove dissolved nutrients approximating 22% of the original nitrogen load. As a result of biofiltration, close to 60% of the nitrogen input into the fish pond has been converted into commercially valuable biomass which is about 3 times 180 W. M. Koven, S. Harpaz, J. Van Rijn et al. more efficient than present day fish farms. Moreover, it is conceivable that the 32% of the original nitrogen input trapped as detritus could be grazed by detritivores (Lupatsch et al 2003c) such as mullet (Mugil cephalus) increasing the efficiency of the system further. Taken together the resulting seawater returning to the sea will have a markedly reduced nitrogen load (>90%). However, it is important to note that integrative pond approach is still grappling with a number of challenges such as sustaining a careful balance between nutrient production by the main cultured organism (fish or shrimp) and nutrient uptake capacity of the types of algae and shellfish used to reduce the nitrogen load. The market value of biofiltration products may fluctuate resulting in reduced profitability of the system. More infrastructure investment, such as green house construction, may be necessary to minimize heat loss or gain downstream of an integrated system. Moreover, production of cultured organisms could be compromised by disease or poor sanitation which could also influence consumer demand and market price.

RECIRCULATING AQUACULTURE SYSTEMS

Incentives for intensive production of fish in recirculating systems differ from country to country. In Israel, water and land scarcity are the main reasons underlying the development of freshwater recirculating systems while the incentive for development of marine recirculating systems is mainly driven by the environmental effects associated with marine fish culture in cages and coastal ponds. Recirculating technology for culture of freshwater fish in Israel has been explored since the early 1980’s. Initially, plastic and concrete lined outdoor ponds were used for this purpose in which fish (mainly tilapia) were cultured up to densities of 20-30 kg/m3 at harvest. Water from these ponds was recirculated through earthen-bottom, “satellite” ponds for water purification. Since in Israel most intensive culture ponds are constructed in existing fish farms, conventional fish ponds or reservoirs most often served as satellite ponds (Mires et al., 1990; Mires and Amit, 1992). On average, satellite ponds comprised 90% of the total water volume in these systems. Hence, considerable water evaporation in these often shallow treatment ponds contributed to a relatively high water usage with estimated values of around 3 m3 of water for production of 1 kg of fish (tilapia). Although these systems were easier to operate than extensive pond systems (ease of harvesting, seining and treatment etc.), water and land savings were only marginal due to the large treatment areas required. Since the early 1990’s various attempts were made to culture freshwater fish in indoor recirculating systems. One of the earliest systems was a tilapia recirculating system operated at kibbutz Sde Eliyahu (Y. Simon, personal communication). It consisted of indoor raceways (total volume: 480 m3) operated at fish densities of up to 45 kg/m3 from which water was recirculated through a mechanical drum filter and a submerged nitrification filter. The system was operated with a relatively large daily water exchange rate of around 30% of the total water volume with effluent water being discharged into regular earthen fish ponds for further use. Over the years, several commercial, semi-closed recirculating systems have been operated in Israel. A system marketed by the Dutch Hesy Aquaculture B.V. company and operated at kibbutz Ein Hamifratz is the most prominent among these systems. This 200 MT annual production plant has been operated over the last seven years, culturing both freshwater (tilapia) and marine fish (gilthead sea bream, European sea bass) at average stocking densities Aquaculture in Israel 181 of around 50-60 kg/m3. Water in the system is recirculated through a drum filter for solid removal and trickling biological filters for removal of dissolved organic matter and nitrification. Effluent water from this semi-closed system is diverted into conventional ponds. A USA developed recirculating technology (Mr. Gary Myers) distributed by the Israeli AquaMaof company was recently installed in kibbutz Revivim for annual production of 150 MT of African catfish. Research on intensive aquaculture recirculating systems (RAS) in Israel has mainly been conducted at the National Center for Mariculture of the Israel Oceanographic Research Ltd. in Eilat and at the Robert H. Smith Faculty of Agriculture, Food and Environment at the Hebrew University of Jerusalem. At the former research institute, a low-head recirculating concept was developed (Mozes et al 2002) in cooperation with Kora (1980) Ltd. The low-head approach enables the reduction of energy consumption in RAS. The Mega-Flow registered system is based on water circulation and water aeration by means of airlifts (Figure 10). The system includes three water circuits: (1) the main loop, where pond water is pumped through airlift pumps several times per hour creating a massive water flow (hence the name 'Mega- Flow'). This loop fulfils three functions: aeration, CO2 stripping and dispersion of waste and uneaten feed in the water column of the system, (2) a second loop, where water is pumped by smaller airlifts once or twice an hour through an up-flow non-pressurized filter for suspended solid removal followed by a moving bed biofilter for nitrification. In both filters, a 'macaroni' type plastic is used as substrate. (3) A third loop, designed for nitrate removal treatment by denitrification and organic matter degradation using an external sedimentation basin and recently intensive reactors have been developed. Pilot scale experiments were conducted for several years (Haddas and Mozes, 2004) before a semi-commercial application of the methodology in a 100 MT production system for culture of gilthead sea bream was constructed. This system produced over 100 MT per year, showing little energy consumption, limited sea-water exchange and reached the designated water quality requirements (Fig. 11). Research at the Hebrew University’s Rehovot campus has mainly dealt with the development of zero-discharge recirculating system. Water in this system is treated by recirculation through two separate treatment loops, one aerobic and the other primarily anoxic. Ammonia is oxidized to nitrate in the aerobic loop by a trickling filter. Concurrently, organic matter and nitrate are gasified by a combination of organic matter digestion and denitrification in the anoxic loop, which is comprised of a digestion/sedimentation basin followed by a fluidized bed reactor (Figure 12). By means of combined aerobic/anoxic treatment of the culture water, main water quality parameters are balanced to such an extent that successful intensive fish production is possible without the need for discharge of water and organic matter from the system. Water addition is limited to compensate for evaporation losses, resulting in an extremely low water requirement for fish production. Depending on the degree of insulation of the culture facility, water consumption ranged between 40- 200 liters per kg of fish produced. Initially tested for tilapia production (Shnell et al., 2002), the technology was later tested for production of marine fish (gilthead sea bream). Based on these tests (Gelfand et al., 2003; Neori et al., 2007), commercial application of this patented technology was recently initiated. A beta-site, 50 MT annual production unit for gilthead sea bream was operated for 18 months in Israel by GFA Ltd. prior to the operation of a full-scale production system established in 2009 by Local Ocean Ltd. in Hudson (NY, USA) with a total projected annual production capacity of 600 MT (Figure 13). 182 W. M. Koven, S. Harpaz, J. Van Rijn et al.

At present, recirculating technology in Israel is still used to a limited extent. Despite the advantages of this technology, its application is hampered for several reasons:

(1) Use of the capital-intensive recirculating systems is only justified in case of production of high valued fish species. As such, the relatively low valued carps and tilapia, the main freshwater species cultured in Israel, are unlikely candidates for these systems. In case of marine fish, a need exists for diversification of aquacultured species. In addition to gilthead sea bream and sea bass, the commonly cultured marine fish species with wholesale prices that justify their production in recirculating systems, culture experience with other high-priced marine fish species is still lacking. (2) Despite their development and refinement over the past thirty years, “off-the-shelf”, reliable recirculating systems are not easy to come by. Even recirculating system configurations that have been widely used elsewhere still require considerable adaptation before successfully applied by new operators. Hence, lack of skilled and experienced local manpower and inexperienced management, are often main reasons for failure. (3) Weak environmental regulations or the lack of implementation of environmental laws still allow fish culture by non-sustainable culture methods.

Current developments in the Israeli aquaculture industry point to prospects for increased application of recirculating technology. It is expected that in addition to the above mentioned incentives, i.e. efficient use of land and water and reduced environmental impact, others will further contribute to the expansion of recirculating systems in Israel. Marketing advantages such as predictable harvest schedules and year-round production as well as consumers’ demands for sustainable produced and safe seafood (e.g. free of chemicals and heavy metals) are among those additional factors. Moreover, with the expansion of recirculating technology it is expected that investment costs will be reduced considerably. Such cost reduction might enable culture of lower valued species (e.g. tilapia) in addition to the high valued fish species thus far cultured in these systems.

CONCLUSION

The aquaculture industry, including both freshwater and marine culture, has expanded impressively over the years in Israel. On the other hand, the clear regional restraints of land and energy costs, water shortage, limited sheltered bays and the environmental awareness of the impact of commercial cage culture on natural resources and multi-use coastal areas has presented formidable obstacles to its continued expansion. However, these limitations have also been the driving force for innovation of new technologies and research to increase the efficiency and productivity of the aquaculture sector while reducing the adverse effects of its effluent. Israeli aquaculture research has made inroads understanding how nutrition and environmental parameters during larval rearing can influence juvenile quality and ultimately market price, in terms of the incidence of deformity, metamorphic success, growth and sex ratio. New vaccines were developed to grapple with viruses that potentially can decimate fish Aquaculture in Israel 183 stocks and alternative therapies for fungal infection were found. Studies that determined the daily energy and protein requirement during grow-out in mainstream mariculture teleosts have facilitated the optimization of feed formulations and feeding regimes. This makes diets more economical and reduces the release of nitrogen compounds to the environment. Environmental impact was also considered in the organic culture of tilapia in pond polyculture or using geothermal water to grow this species in arid regions. The integrative pond concept, as developed in Israel, is designed to strip the vast majority of dissolved and particulate nutrients in fish pond effluent through the co-production of plankton and filter feeders of high market value. The removal of the sea cages from the Gulf of Aqaba and the chronic shortage of water in the region have stimulated the development of novel and promising technologies for land based intensive aquaculture such as the Megaflow design and the zero-discharge recirculating system. Moreover, by increasing the use of recirculating systems and implementing methodologies that ensure the strength and quality of the production of ornamental fish, this promising new Israeli industry has expanded rapidly in recent years and is steadily becoming an important economical component of Israeli aquaculture.

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Chapter 10

AQUACULTURE STATUS AND NEEDS IN THE ISLAMIC REPUBLIC OF IRAN

Mehdi Soltani∗ Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, and Center of Excellence of Aquatic Animal Health, University of Tehran Tehran, Iran

ABSTRACT

Aquaculture development in Iran commenced in the early 1970's with technical assistance from the former Soviet Union for the artificial propagation of sturgeon (Acipenseridae) fingerlings for restocking the Caspian Sea. Since then, the capacity to mass produce other species such Rutilus frisii kutum, Caspian trout (Salmo trutta caspius), bream (Abramis brama), pike-perch (Stizostedion lucioperca), rainbow trout (Oncorhynchus mykiss) and four cyprinids species for restocking other suitable inland water bodies was rapidly acquired by the Iranian Fishery Organization (Shilat). Aquaculture has since expanded to culture of food fish in raceways (trout) and ponds (cyprinids). Other species such as Hamor and Barbus sharpeyi are also being targeted for future culture. Development projects on the farming of penaeid shrimp (Feneropeneaus semisulcatus, F.vannamei and F. indicus) in the Persian Gulf region and along the southeastern area of the Caspian Sea are currently underway. Iran has also initiated projects to evaluate the feasibility of culturing Artemia cyst, grouper, pearl oyster, and aquatic plants. Also, for a sustainable aquaculture new species of fish and shrimp such as tilapia, sea bass and F. vannamei have been imported inside the country. Despite the rapid development of this industry during the recent years it is faced with several constraints including lack of modern technology, insufficient financial resources, and negative impact of environmental pollution and occurrence of devastating infectious diseases. Poor environmental conditions, inexperienced health managements and outbreaks by some economically important infectious diseases such as white spot viral disease (WSD),infectious heamatopoeitic necrosis (IHN), infectious pancreatic necrosis (IPN) and streptococcosis/lactococcosis are the major constraints faced in Iran

∗ Email address: [email protected] (Mehdi Soltani, DVM, PhD, professor of aquatic animal health). 192 Mehdi Soltani

aquaculture causing considerable losses each year. Although both veterinary and fishery organizations approved some roles and legislations to improve health management criteria, there is a risk of exotic and economically important diseases that can be imported through the importation of eyed-egg, larvae, brood stock and ornamental species into the country. However, some viral diseases including IHN, IPN and WSD have become a part of endemic diseases in Iran aquaculture sector.

INTRODUCTION

At present, the average per capita of fish consumption in the Islamic Republic of Iran is low, at 6 kg compared with the world average of 13.5 kg and is to increase average consumption to the desired 13kg level by the year 2020. Total fishery output including aquaculture and fishing in Iran increased from 382,000 metric tones (mt) in 1995 to 670,000 mt in 2007. In 1998, the Caspian Sea region and other inland waters produced about 60,000 and 59,000. mt of fish, respectively. Aquaculture production reached 110,000 mt/yr at the end of the second 5-year development plan (1995-2000), a 2.5 fold increase in production since the beginning of this plan i.e. 1995 (Hosseinzadeh, 2003). The industry grew rapidly with a production of about 130,000 mt in 2005 and is projected to reach about 493,000 mt in 2014. Although aquaculture sector has been rapidly developing during the recent years, it has been faced with several problems. Outbreaks by some economically important contagious diseases, use of inappropriate technology, inadequate financial resources and negative impact of environmental pollution are some of major obstacles faced by the aquaculture industry. This commentary is intended to give an account of different aquatic animal production systems in Iran and the challenges faced by the sector.

AQUACULTURE STATUS IN IRAN

Background to Aquaculture Development

Aquaculture activities were initiated in Iran with different species of fish including, Cyprinids, sturgeons and rainbow trout (Onchorincus mykiss) before 1922. Sturgeon and rainbow trout aquaculture started in 1922 and 1959, respectively (Hosseinzadeh, 2000). In 1970s the hatcheries of rainbow trout, cyprinid species, sturgeons and Mahisefif (Rutilus Rutilus frisi kutum) were established. Rainbow trout and four species of cyprinids consisting of common carp, grass carp (Ctenopharyngodon idella), bighead (Aristichthys nobilis) and silver carp (Hypophthalmychthis molitrix) are the major commercial species currently grown using inland waters. Also, for many years the wild brood stock of some species including sturgeons, Mahisefid, Caspian trout (Salmo trutta caspius), bream (Abramis brama), pike- perch (Stizostedion lucioperca), and cyprinids were used for the production of fingerlings for restocking the wild, the Caspian Sea and the rivers. Some species including Barbus sharpyii, B. grypus, B. xanthopterus, grouper (E. coioides) have been recently propagated. To compensate the shrimp population in the Persian Gulf, a joint project was carried out in collaboration with the UNDP to establish a pilot hatchery for shrimp production in 1987. Later the prawn farming with Feneropeneaus indicus and in some cases F. semisulcatus was Aquaculture Status and Needs in the Islamic Republic of Iran 193

developed in 1993 with15 tones production. The shrimp industry is developing, although the shrimp aquaculture production is faced with problems including marketing and outbreak of viral diseases. Recently marine fish cage aquaculture has been supported by the department of fisheries but so far except for some experimental works no mass production has been accomplished.

Current status of Aquaculture Production

The government of Iran has been successful in its efforts to raise aquaculture output and this is reflected in the overall expansion rate of the sector at 8.2 %/ per year during 1990- 1996. To date, five major fish species consisting of common carp, silver carp, bighead carp, grass carp and rainbow trout contribute to aquaculture output in Iran (Figure 1). In 1996, production amounted to about 30,000 mt, valued at US$ 306.6 million. The production swelled by 4.3 times to about 130,000 mt in 2006 contributed mainly by rainbow trout, , silver carp, and bighead. These species showed an increase by 27, 11 and 7 % per year, respectively between 1991 and 1996. Common carp and Chinese carps including silver carp, grass carp, and bighead carp contributed to the total production until 1996. In 1996, these two groups of carps accounted for 93% (about 28,000 mt) of aquaculture production in Iran. Following the introduction of Chinese carps in the 1970s, there has been a shift from traditional common carp monoculture to polyculture system of Chinese carps and common carp. The increasing production of silver carp was mainly due to the higher stocking ratio of the phytoplankton feeder in the polyculture system despite its lower retail market price compared to grass carp. Development of rainbow trout aquaculture was also carried out during 1987 till 1996 with a total production of 820 mt in 1987 and 1900 mt in 1996 (Figure 1). The aquaculture production of this coldwater species of fish was developed during 1997-2006 and reached a production level of over 46,000 mt and 60,000 by 2006 and 2008, respectively. The development of F. indicus aquaculture was rapid during 1999 till 2004 with a production of about 8,900 mt in 2004.

Figure 1. Major species of aquaculture production in Iran (1987-2006). 194 Mehdi Soltani

However, the production of shrimp decreased to 3,500 mt in 2005 because of the white spot viral disease outbreaks and probably weakened market. Also, crayfish (Astacus leptodactylus) production obtained from the rivers was about 2 mt in1997 which increased to 270 mt in 2006. Commercial aquaculture production of this valuable species has been recently initiated mainly in the north and North West provinces of the country.

Attempts for Expanding Aquaculture Industry

Iran is actively pursuing a holistic approach for aquaculture development, building on one of its key strengths--technology for mass artificial propagation of seed and infrastructure for restocking inland and coastal waters. To promote aquaculture as an independent economic activity, Iran has taken several initial steps till the year 2000 to encourage private sector involvement. These included 1. Making the private sector solely responsible for fingerling production for on growing, 2. Providing low interest loans, 3. Subsidizing feed ingredients for feed production, 4. Providing low price fingerlings from the state hatcheries, 5. Granting twenty-year tax exemption for fish/shrimp farms, 6. Providing free or low price lands and constructing the necessary roads and water canals for shrimp and trout farming, and 7. Consistency in the effective public promotion activities to increase fish consumption, particularly in the central region of the country, where the food habits of including fish in the diet are not well established yet. During the last 10 years activities of the Iran Fisheries Organization have proved successful in attracting the private investors to both seed production and grow out segments of the aquaculture sector. In 1996, around 20 cyprinid and 10 trout fingerling production private hatcheries were operational. In the case of rainbow trout, 80 private on growing farms were operational in 12 provinces. Between 1992 and 1996, the area under rainbow trout production increased from 80,000 to 166,000 m2 (raceway area) and production increased from 775 to 1,900 mt.

Aquaculture Production of Major Species

The culture of carps, trout and marine shrimp is currently active in Iranian aquaculture.

Carps Carp culture is the main fish farming industry in four main provinces of Gilan, Mazandaran, Khozestan and Golstan (Figures 2-5). In these regions four species of carps consisting of common carp, bighead carp, silver carp and grass carp are produced in earthen ponds, rice lands and in waters of temporary dams. Total production was 24,000 mt in 1987 and increased to 27,500 and 77,000 mt in 2000 and 2006, respectively (Figure 1). In Gilan province, total carp production was 10,544 mt in 1999 which increased to 30,500 mt in 2006 (Figure 2). In Mazandaran and Golstan provinces these productions were about 9,200 and 450 mt, in 1996-1997, respectively which increased to 47,500 and 8,960 mt in 2006, respectively (Figures 3 and 4). Also, in Khozestan province aquaculture production of warm water species was about 6,500 mt in 1995 increased to 8,200 and 25,200 mt in 2000 and 2007 (Figure 5). Aquaculture Status and Needs in the Islamic Republic of Iran 195

Figure 2. Total aquaculture production of warm water fish in Gilan province during 1999-2006.

Figure 3. Total aquaculture production of warm water fish in Mazandaran province during 1996-2006.

Figure 4. Total aquaculture production of warm water fish in Golstan province during 1997-2006. 196 Mehdi Soltani

Figure 5. Total aquaculture production of warm water fish in Khozestan province during 1995-2007.

Production of carp is now primarily under taken by the private sector. Carp brood stock selection is usually based on head-size, color, and gill structure (surface and shape of filter) and adult’s fish are usually used for a period of 3-4 years. A key factor in the successful egg production by the private sector was the switch over from the Hungarian method of egg production to the Chinese method. The former had small incubators resulting in high mortalities compared to the latter with large concrete circular tanks having egg collecting devices for spawning and egg collection/incubation, in which there is a minimum intervention in the spawning process. Carps are grown to a marketable size in production systems that vary from simple ponds managed on a part-time basis to capital intensive and professionally engineered and constructed farms managed on a full time basis. In 1994 there were around 2,583 registered warm water fish farms in the country, with a combined pond water surface of approximately 8,000 ha. The Gilan province has more than 12 private carp hatcheries and 2,200 grow-out carp farms with around 3,500 ha of fish ponds. The bighead, silver, grass and common carps are the major species reared under semi- intensive polyculture system in the earthen ponds where the organic and inorganic fertilizers are used for the production of natural food. The use of supplementary feeds is also sometimes common. Under this polyculture system fish are grown up to the market size within a period of one year of culture. Fingerlings of 5-10g are usually stocked at 2,000-6,000 fish/ha during March-April. The lower densities are stocked when large sized fish is required. The ponds are fertilized with urea compost at 135-1500 kg/ha/yr, ammonium phosphate at 80-575 kg/ha/yr and compost at 3-10 mt/ha/yr and the fish are fed using a supplementary diet consisting of a variety of grains at 100-6,000 kg/ha/yr. Some farmers practice intensive monoculture of common carp in well-aerated ponds using pelleted feed with a high protein level of 30-40%. The fish of marketable size are harvested during November-February and the production scale varies between 1.6 to 5.5 mt/ha depending on the level of management.

Rainbow Trout Rainbow trout farming was initiated in 1950s with the importation of eyed-eggs from Europe. The trout farming was limited to two farms located one each in the east and west of Aquaculture Status and Needs in the Islamic Republic of Iran 197

the capital city, Tehran for about 20 years. The trout aquaculture industry was then gradually developed after 1980s in the cold and temperate areas of the country mainly in the areas of Alborz and Zagros mountains. At present, Choharmohal-va-Bakhteyari, Lorstan and Mazandaran are the leading provinces in rainbow trout aquaculture producing about 50% of total trout production in the country. Most of rainbow trout farms in Iran produce more than 50 mt per year. However, there are some bigger trout farms with a potential production of up to 1000 mt per year. Most of the trout farms have the raceway system, although there are about 150 recirculation biofilteration systems. Also, recently a few Norwegian and Danish recirculation biofilteration systems have been established in different parts of country including Lorstan, Azarbayejan and Tehran provinces. However, inadequate financial resources, poor training level and insufficient technology are still main problems of recirculation biofilteration systems in the country. More recently, the first specific pathogen free (SPF) trout farm has been established in the centeral province of country to supply the SPF fingerling trout to the industry particularly to those of recirculation biofilteration systems. The egg production and intensive grow-out systems have been well developed although the final outcome is low in some trout hatcheries. This is because of inadequate experience, insufficient training, low quality of feed and poor health management practices. Also, currently some of the trout farmers import eyed-eggs from different countries including Denmark, Finland, Canada, Australia, Scotland and Norway with a different survival rate (up to 80%) up to the alevin stage. Selection of the brood stock is mainly based on the phenotypic criteria. Total production of trout fingerling is dependant on a numbers of parameters including water quality, feed quality and health management factors. In 1996 about 10 million trout fingerlings were produced by the private sector which increased to over 250 million in 2006. Total production of rainbow trout increased from 820 mt in 1987 to 2572 mt in 1997. The trout aquaculture production has been about 60,000 mt in 2008 (Figure 1) and based the governmental working plan a production of above 100,000 mt has been expected by next five years. Almost, all trout farmers use commercial pellets produced by private feed manufacturers with some of them being supported by the Government. Also, recently, the trout farmers started to import the trout feed from Europe, Canada and the USA. Conversion efficiency of the pelleted feed is in the range 1: 1.1 - 1.4 (wet fish: dry feed weight basis). Some trout farmers produce their own feed, mainly for the feeding of brood stock and fattening fish. Slow growth rate, mainly due to low water temperatures, extends the production cycle to take a longer time of above 14 months, whereas at water temperatures of 13-16oC this gets reduced to 9 months. In some regions high water temperatures of above 17oC, particularly during the summer season, increases the levels of morbidity and mortality due to lower oxygen, occurrence of some bacterial infections including streptococcosis/lactococcosis and motile Aeromonas septicemia.

Sturgeon Farming Sturgeons are among the aquatic organisms that are severely influenced by the effect of pollution in their natural habitat, the Caspian Sea. These species are of the most economically valuable species that are protected and conserved through various means. Although climatic and geological processes affect the fish stocks, human activity has the most destructive impact (Debus, 1995). 198 Mehdi Soltani

These highly valuable fish species such as great sturgeon (Huso huso), Persian sturgeon (A. persicus), ship (A. nudiventris) and A. gulednstaedti are the major economically important species of northern Iran that play a significant role in the income of the Iranians in the regions of the southern Caspian Sea. These commercially valuable species of fish generally spend their adult life in both freshwater and salt water environments, spawning in the upper river stretches of the Gorgan and the Sefid-Rud which are contaminated by organophosphates such as diazinon and malatinon (Rezvani-Gilkolaei, 1997).

Figure 6. Caviar production in Iran during 1998 till 2006.

Sturgeons can live up to 100 years with a maximum recorded weight of up to 1500 kg. The fish matures usually after 12 years of age and therefore, the process for caviar production takes a long time. Such biophysiological features of the fish may make them to be frequently exposed to toxicant chemicals commonly contaminate the rivers and the Caspian Sea coastal waters. In the last decade the average annual sturgeon harvest from the South Caspian Sea was 2068 tones. About 1619 mt of caviar, worth $191 million was exported during the ten year period of 1975 to 1984. A slight increase both in the sturgeon harvest and the world caviar market price led to a higher export of 1434 mt, ($319million) during the seven years from 1988 to 1994. Nowadays, because of both overfishing and water pollution the sturgeon stock has sharply declined throughout the Caspian Sea (Pourkazemi, 1996). The total production of caviar was 91.3 mt and it decreased to 15.45 mt in 2006 (Figure 6). Similar to caviar production, the total meat production of captured sturgeons from the Caspian Sea has remarkably decreased during last decade. For instance, sturgeon meat production was 2170.7 mt in 1970 and it reduced to 1496.1 mt in 1980. In an attempt to keep a steady caviar production level and increase the sturgeon meat supply, sturgeon farming was initiated with the assistance of Iran Fisheries Organization. So far 47 sturgeon farm licenses have been issued by Iran Fisheries Organization to produce 2500 mt meat and 72 mt caviar. However, one of major problems to establish such sturgeon farming is the difficulty to access to the required brood fish for production of larvae.

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Marine Shrimp Developing of penaeid culture in the southern parts of Iran along the Persian Gulf and Sea of Oman was started in 1992. To date some 40,000 ha of coastal areas has been allocated for developing shrimp farming mainly in this region. Also, shrimp culture of F. semisulcatus and F. indicus has been recently started in the eastern parts of the Caspian Sea including Gorgan and Gonbad regions. So far, 12,000 ha ponds have been prepared from which 8,000 ha are actively used for growing F. indicus and the imported F. vannamei. However, in year 2009, because of a number of obstacles including outbreak of white spot viral disease, occurrence of red-tide caused by Cochlodinium prykricoides and low market price, about 2000 ha of these shrimp farming were used for shrimp production. In the southern provinces the government is developing each shrimp culture site by providing the necessary primary infrastructures such as road, main water channels and electrical power. Shrimp farming is centered on the development of species indigenous to the Persian Gulf, particularly F. semisulcatus and F. indicus. The total production was 150 mt in 1995 mainly produced by the private sector. Total shrimp production then, increased to about 8,880 mt in 2004 (Figure 7). However, because of outbreaks by white spot viral disease, difficulties to obtain the necessary brood stock and probably low price of harvested shrimp in the market; the shrimp production in Iran reduced to 3845 and 2500 mt in 2005 and 2008, respectively (Figure 8). In the Caspian Sea region, production yield of 4 mt/ha has been recorded.

Figure 7. Actual and expected shrimp aquaculture production in Iran during 1999-2008.

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Figure 8. Actual and expected shrimp aquaculture price in Iran during 1999-2008.

To compensate for the shrimp production and keeping a sustainable shrimp aquaculture, the brood stock of F. vannamei was imported for the first time in 2007. To improve the shrimp aquaculture industry in Iran, a UNDP/FAO mission on "Development of National Strategy for Aquaculture Shrimp Management" (IRA/97/020/A/08/12) is currently underway. Because of a significant decrease in shrimp production, a total expected price of about $54 million reduced to $12.8 million in 2008 (Figure 8).

Other Crustacean Species (Artemia, crayfish) Growing of Artemia uromia in the hyper-saline of 100-150ppt is one of aquaculture activities in Iran. Artemia is used currently as a live feed for the shrimp and sturgeon farming. The Uremia Lake with an area of 6000 km2 has the potential to produce 300 mt of Artemia cysts per year. A pilot processing plant has already been established at the lake shores and, in 1996, a 20 mt of Artemia cysts were produced (Abdolhay, 1999). The aquaculture production of crayfish (Astacus leptodactylus) and Macrobracium rosenbergii is also in the initial stages of development in Iran, although there are few small farms established in the north and south parts of the country.

Marine Mollusks The mollusk aquaculture activity was initiated in Kish island where the black-lip oyster culture project was established by Iranian Fisheries Organization in 1984 (Hosseinzadeh, 2003). However, because of some difficulties its commercial production has been unsuccessful so far.

Aquaculture for Stock Enhancement (restocking)

Because of the degradation of natural habitats and reproduction places of some valuable species such as sturgeons, Mahisefid and the Caspian trout, the restocking plan of the Caspian Sea and the rivers joining the sea has been a national plan work of Iranian Fisheries Organization since 1950s. For this purpose, 24 fish hatcheries were established of which 13 Aquaculture Status and Needs in the Islamic Republic of Iran 201

are run by the Governmental body and the remaining ones are run by the private sector (Hosseinzadeh, 2003). Over 15, 160, 233 and 250 million fish fingerlings including that of the above mentioned species have been produced for restocking in the sea and rivers during 1978, 1990, 1999 and 2000, respectively. At present, the Fisheries Department produces 200- 300 millions fish fingerlings each year for restocking of the Caspian Sea.

Marine Fish Although Iranian Fisheries Organization made some attempts for the production of some marine fish species such as bream (Abramis brama), grouper and sea bass (Lates calcalifer) in the Persain Gulf, the marine fish cage aquaculture has been seriously taken neither in the Caspian Sea nor in the Persain Gulf so far. The preliminary cage culture of grouper, bream and sea bass have been carried out in the coastal areas of the Persian Gulf, Mahshar harbor and Hengam Island. One of the main obstacles for developing of such cage culture is the lack of adequate technology inside the country. However, at present there is demand by the private sector to establish cage culture especially in the Persian Gulf and therefore, it is predicted to have a large marine cage aquaculture industry in both north and south Iran in the nearly future.

Potential for Further Aquaculture Development in Iran

Hatchery technology exists in Iran for the several fish species that are mainly used for restocking programs. Therefore, some of these potential candidate species include sturgeon species, Caspian trout (Salmo trutta caspius), Mahisefid (Rutilus rutilus), bream, mullet, barbus (Barbus sharpyii, Bsrbus grupus, Barbus xanthopterus), grouper and F. semisulcatus. Although species of sturgeons such as great sturgeon and Persian sturgeon are suitable candidates for commercial aquaculture, more research works are required on their commercial feed, hatchery technology and brood stock consolidation. ‘Bream in polyculture systems’ is a common interest among the fish farmers and more studies are required to identify the fish water quality and feeding regimes. This species has a higher market valuable in Iran compare to the Chinese carps so a remarkable increase in its production is expected in the future. Mahi sephid is also one of the valuable candidate species for commercial aquaculture in Iran. However, attempts to grow this species has been limited to the fingerling stage, and so more research works are required to grow this species up to market size. Although aquaculture development is relatively new, Iran has made significant progress in promoting aquaculture sector. The following activities have been carried out by the government so far:

1. Allocation of adequate land and water resources for aquaculture development. 2. Improvement of processing, marketing and related infrastructure. 3. Investment in strengthening human capacity. 4. Successful efforts for raising the demand for aquatic products such as rainbow trout.

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However, to maintain and extend this progress several efforts needed to be addressed. These include:

1. securing all year round supply of high quality trout seed 2. providing technical information on production systems and their management, 3. providing training and dissemination of information on reproductive biology and genetics, brood stock management techniques, feed and feeding technologies, 4. The availability of required facilities/equipments 5. developing research and training programs, 6. strengthening the extension service, 7. facilitating procurement of equipment, 8. improving transportation system for farm to market, and 9. improving the manufacture artificial fish/shrimp feed.

Iran Fisheries Organization is also currently involved in some aquaculture activities to meet the immediate challenges to a sustainable aquaculture development through a national brood stock program for some species such as rainbow trout, bream, grouper, sea bass, barbus sp., F. indicus and F. vannamei.

HEALTH MANAGEMENT IN AQUACULTURE SECTOR IN IRAN

Coldwater Fish Farming

IHN was first identified as one of the main causative agents of fry trout mortality syndrome in rainbow trout farming in 2002. Further serological and molecular studies of geographical distribution of the disease outbreaks shows that almost all major trout producing are infected. Molecular and serological studies have been also confirmed the occurrence of IPN infection in a number of farmed trout. Although, the incidences by SVC and VHS are suspected in carp and trout farming, more works are required to clarify these important viral diseases in Iran aquaculture. At the moment Lacotococcus garveiae and Streptococcus iniae outbreaks are one of main bacterial diseases in farmed rainbow trout in different parts of Iran where the trout farms are located (Figure 9). The disease outbreak is associated with water quality parameters particularly high water temperature (>14º) and poor health management. The peak of outbreaks occurred during late spring till late summer with mortalities varying from 5-70% (Figures 10). Also, infections by Cytophaga/Flexibacter like-bacteria occurred in farmed rainbow trout of different size causing saddle back lesions and the mortality went up to 16%. The epizootiological studies of such outbreaks shows that unsuitable long transportation, poor water quality, long exposure to the sunlight and nutritional deficiency, particularly vitamin deficiency, are probably the main predisposing factors involved in the infections by Gram negative filamentous bacteria.

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Figure 9. Geographical distribution of streptococcosis/lactocccosis inside Iran.

Figure 10. View of a rainbow trout pond in north Iran containing fattening diseased rainbow trout affected by L. garvieae showing typical bilateral exophthalmia (Photo by author).

The first outbreak of yersiniosis with a total mortality of 10-20% was reported in some farmed rainbow trout in Iran during summer 1997 and 2000. The disease outbreaks can become a serious problem mainly in those trout farming that use the rivers as their water sources. In addition, infection by Ichthiophtirius multifiliis is sometimes an obstacle in trout recirculation biofilteration systems. Infection by Saprolegnia genera is also the most 204 Mehdi Soltani important fungal infectious diseases currently occur in rainbow trout, sturgeon and cyprinids hatcheries. The losses due to saprolegniosis in trout hatcheries is more than other species because of low water temperature and longer period of hatching period required for rainbow trout. In trout culture, an increase in levels of unionized ammonia, trite, carbon dioxide, low dissolved oxygen, high level of total suspended/dissolved solids and high fluctuation in water temperature are the main environmental problems encountered the industry. Such water quality parameters are more serious in trout recirculation systems.

Warm Water Fish Farming

Infection caused by Flavobacterium psychrophilum-like bacteria has been reported from silver carp farming during the winter seasons in the southern regions of the country. Also, for many years the cyprinid farming including grass carp and silver carp are suffering from significant morbidity and mortality when water temperature increased. Various etiological agents including motile Aeromonas bacteria, Aeromonas hydrophila and Aeromonas veronii, a reoviral like virus and poor water quality conditions have been so far discriminated as the main causes of such losses. Many protozoans and metazoans have been reported by several workers from different species of fish including both wild and cultured fish. Among them infections by Ichthiophtirius multifiliis, Trichodina sp., Diplostomum spataceum, Dactylogyrus sp., Lernea sp. and Botirocephalus sp. are the more economically serious parasitic infections currently occurring in the farmed cyprinids.

Sturgeon Farming Despite the value of sturgeon species as a part of aquaculture activity in Iran minimum data are available on the health status particularly infectious diseases of these valuable species both in wild and cultured conditions. The most available data has been focused on the identification of the external and internal parasites in these species. Cucullanus sphaerocephalus, Skrjabinopsolus semiarmatus, Leptorhynchoides plagicephalus, Pseudotracheliastes stellatus, Diclybothrium armatum, Nitzschia storionis, Eustrongyluides excisus, Anisakis sp., Amphilina foliace and Corynosoma stroumosum .have been reported by various workers from different species of sturgeons including Persian sturgeon (Acipenser persicus) and great sturgeon (Huso huso). Motile Aeromonas, Edwardsiell sp., Ichthiophthirius multifiliis, Trichodina, monogenic trematods and Saprolegnia spp. are the main causative agents identified so far in sturgeon aquaculture. There is no information on the possible viral diseases in these fishes. Similar to trout and carp culture systems, an increase in levels of unionized ammonia, nitrite, carbon dioxide, low dissolved oxygen, high level of total suspended/dissolved solids and high fluctuation in water temperature are also the main environmental problems encountered the sturgeon industry.

Ornamental Fish Despite the frequent and large scale importation of different species of ornamental fish from different regions including East Asia, minimum data are available on their health status. Infections by Edwardsiella tarda, Aeromonas hydrophila, Aeromonas veronii, Flavobactria, Aquaculture Status and Needs in the Islamic Republic of Iran 205

some protozoa and metazoans occur infrequently in some ornamental species such as Oscar, catfish, goldfish, guppy and guramy.

Shrimp Farming The first outbreaks of WSD causing a rapid and high mortality occurred in farmed Penaus indicus in Abadan region, south Iran during June till July 2002 causing remarkable losses. The second and third outbreaks were also seen in Busheher and Systan-va-Balochestan provinces during 2004 and 2008, respectively causing high losses. Outbreaks by baculoviral agents such as Monodon baculovirus have been also occurred in shrimp farming in south country. However, the exact impact of such viral diseases in Iran shrimp industry remains unknown. The risk for the occurrence of other economically important shrimp viral diseases such as tura viral disease, yellow head viral disease and infectious hypodermal and heamatopoeitc necrosis viral diseases in Iran shrimp farming is high because of probably low level of quarantine and inadequate inspection measurements. Also, vibriosis caused by Vibrio anguillarum, Vibrio harveyi, Vibrio alginolyticus and Vibrio parahemolyticus is infrequently involved in F. indicus, F. vannamei and F. semisulcatus in south Iran.

Nutritional Health Problems

Disease Control and Veterinary Medicine in Iran

Usually strategies that may be adapted to control fish and shellfish diseases such as viral diseases range from no action to test and slaughter, with intermediate interventions as appropriate. These include surveillance, therapy, and modification of physical /environmental conditions, alteration of production schemes, vector control, carrier elimination, quarantine and mass vaccination of target species which is under investigation. In Iran, because of a number of gaps in our current knowledge about the outbreaks of viral diseases in both fish and prawn farming, the use of one or a combination of some of these strategies is vital. At the moment because of no confirmation for some economically important diseases, e.g. VHS, SVC, KHV and VNN in Iran aquaculture, the use of current surveillance on epizootiology of exotic diseases and quarantine legislation are critical.

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Control of Exotic Disease Risks

The exotic viral disease risks exist in aquaculture species in Iran because of poor control measures in quarantine, husbandry, and vaccination/chemotherapy activities. Husbandry measures should be based on recognition of a number of potential risk factors for transmission and maintenance of disease. e.g. the risk of importing diseases with a stock of IPN, IHN, VNN, VHS, herpesvirus and iridovirus carriers or vectors. Importation of aquatic animals in particular ornamental species of fish are the main risk factor for both farmed rainbow trout and cyprinids in Iran. Evaluation of brood stock health is also an important disease control measure. However, there are currently no particular available tests for brood stock of cyprinids, sturgeons and rainbow trout in Iran. Information on larval health is also critical and recently the veterinary organization has approved some roles and regulations to minimize the transmission of vectors, carriers and affected larval or brood stock inside the country.

RECOMMENDATIONS AND PROSPECTIVES

The main aquaculture activities planned to reach the aquaculture goals in Iran are to: 1. develop individual and complex aquaculture of warm water species, 2. enhance the aquaculture management through the improving water quality criteria, feed quality etc 3. Employ new and modern technologies such as recirculation systems and cage culture, 4. Improve the integrated aquaculture to reduce the environmental pollutions, 5. Support sufficient financial resources 6. Improve the aquaculture marketing and 7. Improve the health management criteria. Although both Veterinary and Fishery Organizations approved some roles and legislations to prevent outbreaks by contagious infectious diseases in Iran aquaculture, there is still a risk of exotic and economically important infectious diseases that can be imported through the importation of eyed-egg, larvae, brood stock and ornamental species into the country. This is because of: insufficient routine screening programs for disease detection, no adequate data collection from fish/shrimp farmers and no sufficient training/education plans for many fish/shrimp farmers to get more familiar with the impact of predisposing factors, eradication, quarantine and other aspects of health conditions in their farmed animals. Therefore, the use of current surveillance on epizootiology of contagious diseases and quarantine legislation are highly recommended.

ACKNOWLEDGMENTS

Thanks to Dr H.A. Khoshbavar-Rostami and Dr H. Abdolhay and also Dr Sh. Kakolaki, Dr M. Mazandarani and Dr Z. Omidzahir for their assistance on preparation of some required data.

Aquaculture Status and Needs in the Islamic Republic of Iran 207

REFERENCES

Abdolhay, H. (1999) Aquaculture in Iran.country report. Regional Aquaculture Planning Workshop, 105 September, 1999, Thialand. Anon. 1998. Caspian Sea Environment National Report of I. R. Iran. Deparmtent of the Environment. Debus. L., 1995. Sturgeon in Europe and causes of their decline. Sturgeon Stock and Caviar Trade Workshop. 9-10 October 1995. Bonn, Germany. Bartley D. and Rana, K. J. (1998). Evaluation of Artificial rehabilitation of the Caspian sea fisheries and genetic resources management. FAO report prepared for the SHILAT (Fisheries Department). Esmaeili, F., Soltani, M. and Sayari, M. (2001) Occurrence of Flavobacterium psychrophilum-like infection in silver carp (Hypophthalmychthy molitrix). Iraninan Journal of Fisheries Sciences, 10(2), 103-111. Fallahi, R.; Soltani, M.; Karegar, R.; Zorrieh Zahra, M.E.J.; Shchelkunov, I.; Hemmatzadeh, F.; Nouri,A. (2003). Isolation and identification of the IHNV-like agent from farmed Rainbow trout (Oncorhynchus mykiss) from Iran. Archives of Razi, 56: Gorogi A. (1996) Identification of blood and intestinal parasites of Huso huso in southern part of the Caspian Sea. Iranian Journal of Fisheries Sciences, 4: 43-47. Hosseinzadeh H. (2000) Status of aquaculture in Iran: Past, present and future. The Third World Fisheries Congress, Beijing,China, Book of Abstracts, p.10-12. Hosseinzadeh H. (2003) Status of aquaculture in Iran: Past, present and future. Aquaculture Fisheries Society Symposium,.By the American Fisheries Society, pp.9. Iranian Fisheries Sector Study (1997). Final report. Part 1. Prepared by COFREPECHE and Abzigostar Consulting Engineers. Khoshbavar-Rostami, H.A., Soltani, M., Hassan, H.M.D., 2004, Acute toxicity and some hematological and biochemical changes in giant sturgeon (Huso huso) exposed to diazinon. Bulletin of the European Association of Fish Pathologists, 24(2), 92-99. Khoshbavar-Rostami, H.A., Soltani, M., Hassan, H.M.D. (2006a). Some hematological and biochemical changes in blood serum of Beluga (Huso huso) after chronic exposure to diazinon, Iranian Journal of Fisheries Sciences, 5(2), 53-66. Khoshbavar-Rostami, H.A., Soltani, M., Hassan, H.M.D. (2006b) Immune response of great sturgeon (Huso huso) subjected to long –term exposure to Sublethal concentration of the organophosphate, diazinon. Aquaculture. 256: .88-94. Khoshbavar-Rostami,H.A., Soltani, M., Hassan,H.M.D. (2006c). Immune response of great sturgeon to Aeromonas hydrophila bacterin. Journal of Fish Biology, 70, 1931-1938. Pourkazemi, M., 1996. Molecular and Biochemical Genetic Analysis of Sturgeon stocks from the South Caspian Sea, Ph.D.Thesis, pp.20. Rezvani Gilkolaei, S.1997. Molecular population genetic studies of sturgeon species in south Caspian Sea, Ph.D Thesis, pp.26-29. Rohani, K., Payghan, R and Jehanshahi, AA. (1996) Isolation of a Reovirus from grass carp in Khosestan province. Pajohesh va Sazandegi, 3: 104-105. Sattari, M. (1999) parasites of sturgeons from the southwest of the Caspian Sea. PhD dissertation, Faculty of Veterinary Medicine, Univesity of Tehran, 280p (in Persian). 208 Mehdi Soltani

Sattari, M, Mokhayer B. and Shafii, S. (2006) Parasitic worms of Persian sturgeon (Acipenser persicus) from the southwest of the Caspian Sea. European Association of Fish Pathologists, 26, 131-136. Soltani, M. and Rostami, M. (1997) A Cytophag/Flexibacter like bacterium (CFLB) infection in farmed rainbow trout in north Iran. Journal of Veterinary Research (previously Journal of Faculty of Veterinary Medicine, University of Tehran), 52(3): 13-22. Soltani, M., Fadaii Fard and Mehrabi, M. (1999) First report of a yersiniosis-like infection in Iranian farmed rainbow trout. Bulletin of the European Association of Fish Pathologists, 19(4), 173-177. Soltani, M., Sharifpour, I. and Ismaeili F. (1999) The effect of some environmental variables on the course of infection by Vivrio harveyi in white Indian shrimp (Penaeus indicus). Journal of Veterinary Research (previously Journal of Faculty of Veterinary Medicine, University of Tehran), 55(4):9-13. Soltani, M. and Tarahomi, M. (2000) Pathogenicity of Yersinia ruckeri-like isolates recovered from farmed rainbow trout in Tehran province. In second Convention of Iranian Veterianry Clinics, Book of Abstracks, p.37. Soltani, M., Kakoolaki, Sh. and Kisami, M. (2000) Isolation and identification of dominant Vibrio species in farmed prawn of Heleh station, Busheher, Journal of Veterinary Research (previously Journal of Faculty of Veterinary Medicine, University of Tehran), 55(2), 28-32. Soltani, M. and Ebrahimzadeh Mousavi, H.A. (2000) Isolation of Aeromonas hydrophila and Aeromonas veronii from the farmed grass carp (Ctenopharyngodon idella) mortality in Gilan and Tehran provinces. Iranian Journal of Veterinary Medicine (previous name: Journal of The School of Veterinary Medicine, Shahid Chamran Unviersityof Ahwaz, 4, 24-29. Soltani, M. and Kalbassi, M.R. (2001) Protection of Persian sturgeon (Acipenser persicus) fingerling against Aeromonas hydrophila septicemia using different agntigsn. Bulletin of European Association of Fish Pathologists, 21, 235-239. Soltani, M. (2003) The status of aquaculture health management in Iran. Aquaculture Europe 2003, Trondhim, Norway. Exteneded Abstracts and short communications, European Aquaculture Society, p.321-322. Soltani M, Jamshidi Sh and Sharifpour I (2005). Streptococcosis caused by Streptococcus iniae in farmed rainbow trout (Onchorhynchus mykiss) in Iran: Biophysical characteristics and pathogenesis, Bulletin of the European Association of Fish Pathologists, 25, 95-106. Soltani M. (2008) Lacotoccosis caused by Lacotococcusgarvieae in farmed rainbow trout (Onchorhyncus mykiss) in Iran. The 7th Symposium on Diseases in Asian Aquaculture, Taiwan, Book of Abstracts, p.163. Soltani, M. Nikbakht, Gh, Ebrahimzadeh Mousavi, H.A and Ahmadzadeh H. (2008) Epizootic outbreaks of lactococcosis caused by Lactococcus garvieae in farmed rainbow trout (Oncorhynchus mykiss) in Iran. Bulletin of the European Association of Fish Pathologists, 28(5), 207-212. Tokhmafashan, M, Akbari, S., Tamjidi, B., Laloi, F. and Soltani, M (2004) Occurrence of white spot syndrome disease in farmed Penaus indicus in Iran, Applied Fisheries and Aquaculture, IV (1), 42-47.

Chapter 11

REVIEW OF MOROCCAN AQUACULTURE

Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla National Institute of Marine Fisheries (INRH), Morocco

ABTSRACT

In Morocco, the practice of aquaculture is under two different public administrations. The marine aquaculture is managed by Marine Fisheries Department (DPM) of the Ministry of Agriculture and Marine Fisheries (MAPM). Whereas, freshwater aquaculture is under the supervision of the High Commission for Water, Forests and Fight Against Desertification (Haut Commissariat aux Eaux et Forêts et à la Lutte Contre la Désertification) (HCEFLCD). Both aquaculture types have followed different development histories and different development strategies. Freshwater aquaculture started in Morocco in 1924, when the initial objective was the promotion of sport fishing in lakes and dam reservoirs of the Middle Atlas region, through restocking of hatchery-produced juveniles of ecologically and socio- economically valued fishes. Since the 80's, the semi-intensive aquaculture systems were adopted using both natural and artificial ponds. After the 90's, the private sector, with the support of the HCEFLCD, exhibited limited aquaculture investment in small areas. Since then, several active private aquaculture farms started breeding many fish species such as eels, trout, common carp, Nile tilapia, etc. Marine aquaculture began in Morocco in the 50's. Oyster farming was the first marine aquaculture activity, originally practiced in Oualidia lagoon located in Moroccan Atlantic coast, then spreaded to other coastal sites such as Nador lagoon, Khnifiss lagoon and Dakhla Bay. Some oyster companies are still operational with a total annual production maintained around 200 to 300 tons. During the 2000's, mussel culture began to develop in some coastal areas, mainly in Imessouane Bay (Atlantic coast) and M'diq Bay (Mediterranean coast). On the other hand, marine fish aquaculture was initiated during the 80's and focused only on the Mediterranean coast. It was first developed in Nador lagoon before spreading to other sites such as Saidia, M'diq and Azla. Out of the 4 fish farms that were established, only one of them is still operational and producing an annual amount less than 100 tons. National aquaculture production reached a total amount of 1,161 tons in 2006, registering a significant decline of about 48% compared to 2005 (2,239 tons). This decline was caused by a severe 80% drop in marine aquaculture production (291 tons in 210 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

2006 compared to 1,449 tons in 2005), whereas freshwater aquaculture showed a little increase of about 9% (870 tons in 2006 compared to 790 tons in 2005). The national total aquaculture production represents only 0.2% of total national fisheries production. The complexity of administrative procedures affects the development of aquaculture industry. Furthermore, the development of aquaculture in Morocco relies on sequential development plans, which are integrated in national plans and established as action programs for periods of three or five years. However, the aquaculture industry in Morocco suffers from a lack of clear vision and strategy of the government. In the light of new global socio-economic situation and trade competitiveness in the Euro- Mediterranean context, the current thinking seems to converge towards a real interest to alleviate the administrative, institutional, legislative and regulatory constraints. The establishment of local plans for potential aquaculture sites is based on eco- systemic studies as well as environmental and socio-economic integration. Both of which are considered as fundamental criteria. Regarding freshwater aquaculture, this plan is developed, based mainly on strengthening and enhancing the potential for restocking of dams reservoirs, lakes and main rivers for environmental, touristic (sport fishing) and socio-economic (commercial fishing) purposes. Thus, such plan supports the diversification of potentialities of freshwater aquaculture (increasing of hatcheries, establishment of pilot plants for experimental practices and commercial demonstration scale, development of locally produced aqua feeds, scientific and technical support for projects of aquaculture production units, etc.). Currently, aquaculture industry in Morocco is confronting a critical period that requires collective and coordinated efforts of all public and private sectors to support basic structural foundations and to strengthen the conditions for integrated and sustainable development of aquaculture activities. There is no doubt that all administrative, scientist and professional actors are aware of the need for a new strategy for aquaculture development, which should be concerted, credible and long-term established. An effective action program for the development of marine and freshwater aquaculture is required. It will contribute to create regional poles of integrated development, which will benefit local economy and may encourage foreign investments and market organizations with a proper insurance system.

INTRODUCTION

The Kingdom of Morocco is located in the extreme north-west of the African Continent. Its total population is estimated at about 30 millions and its total area is about 710,000 km2 with 3,500 km of marine Mediterranean, Gibraltar Strait and Atlantic coastlines. Its Atlantic zone (of about 3,000 km of coastline) is one of the most productive in the world. According to Orbi, et al. (1998), Larissi, et al. (2001) and Makaoui, et al. (2005), the Moroccan Atlantic coast is an important upwelling area characterized by a strong primary and secondary production (Ettahiri et al., 2001; Somoue et al., 2003 and 2005). Since long time ago, fisheries played an important economic and social role in Morocco which is considered as one of the leaders in fisheries products, particularly in the region of North-Africa and Middle- East. That is because of its large marine fishing area and its important sea-products landing, of which significant quantities are exported to world markets. Since the beginning of the year 2000, the annual fisheries production of Morocco varied between 0.9 and 1.2 million tons. The average seafood consumption in Morocco per capita per year is almost 10 kg, whereas the world average is estimated at 19 kg. Review of Moroccan Aquaculture 211

While the world aquaculture industry is steadily growing, the Moroccan aquaculture is declining. Indeed since 2006, the Moroccan aquaculture suffered a significant decrease in domestic production comprising less than 0.2% of the annual national fisheries production. Therefore, the support of the government is highly needed for further significant aquaculture development since aquaculture industry can play a major role in food security and create opportunities for employment and rural economy enhancement. This article presents a general review of aquaculture in Morocco. It is focused on the history of Moroccan aquaculture, its current situation, major constraints to the industry, its sustainable development and finally prospects that could be achieved to improve the aquaculture industry status. The authors are providing information using available data and documented sources, also based on their own working experiences for many years in the aquaculture field.

HISTORICAL OVERVIEW

In general, Morocco is not among the countries with strong aquaculture tradition (Catanzano, 1998). The first trials to culture marine organisms in Morocco for human consumption commenced in the middle of the last century, using traditional aquaculture species, practices and techniques imported from Europe. However, the history of freshwater aquaculture is quite different as described below. According to the FAO statistics (Figure 1), the total aquaculture production in Morocco was insignificant between the 50's, when it started, and the end of the 60's. However, from that point onward it began to increase gradually at a slow pace reaching an annual amount of 200 tons in 1984. Then, again it slowed down during the 6 years that followed before exhibiting an important growth starting from 1989.

Figure 1. Aquaculture production in Morocco (since 1950), (Source: FAO Fishery Statistic, 2007). 212 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

This increase in production amounts was relatively higher compared to the previous period, reaching within a short time (about 10 years) a maximum annual production value of 2,800 tons in 1999. From that date onward, the growth of aquaculture started going into a decreasing trend falling down to about 1,200 tons in 2006. The maximum produced quantity (2,800 tons) registered in 1999, was mainly due to the carp production (grass and silver carp) which was about 1,400 tons.

MARINE AQUACULTURE

Marine aquaculture in Morocco has a relatively short history of about 60 years. However, this short period can be divided into three main stages, according to the significance of the events.

The First Stage

This stage began during the 50's, when marine aquaculture, or to be more precise shellfish culture, was started in the Oualidia lagoon. French investors have introduced oyster species to investigate its potential for culture in this and other lagoons, such as Moulay, Bouselham and Sidi Moussa sites. Thus, three different species of oysters were investigated. The first species was the European flat oyster, which seemed to have suffered serious survival problems with no successful attempts reported. The second species was the Portuguese cupped oyster. Its culture assays have provided satisfactory results. However, after a certain while, it was abandoned because of the many pathological problems, which impacted the culture of this species in Europe from which spats were imported. Consequently, a third species, the Japanese cupped oyster also called the pacific cupped oyster replaced it. From the first culturing attempts, this species demonstrated good adaptation to local rearing conditions and showed highly interesting results compared to its performance in its native area from which it was imported. Since then, it became commonly cultured on commercial scale in the Oulidia lagoon and small many oyster farms were established. Spat supply was, and still is, based on the naturally collected spats imported from France. Thus, oyster culture in Morocco demonstrated good success locally and the production quantities were almost entirely for the domestic market. Oulidia lagoon became, for a couple of decades, a well-known commercial oyster culture site both on the national and regional scales.

The Second Stage

This stage started from the middle of the 80’s, which marked the beginning of the first commercial operations in terms of cultured species diversification and technological rearing practices that characterized the modern marine aquaculture development in Morocco. Modern aquaculture in Morocco was then initiated benefiting from examples and experiences of neighboring European countries and Japan. Promoting aquaculture was achieved through technological and professional knowledge transfer, and skills and capacity building were Review of Moroccan Aquaculture 213 achieved in the framework of the FAO’s Mediterranean program for aquaculture promotion (MEDRAP). In this program framework, the former ISPM (Institut Séperieur des Pêches Maritimes), replaced by the National Institute of Fisheries Research (INRH) (Institut National de Recherche Halieutique) since 1996, has achieved, in joint cooperation with the FAO experts, a numerous filed studies on Mediterranean coast of Morocco, particularly in Nador lagoon. These works have effectively contributed to the creation of the largest Moroccan marine aquaculture private company in 1985, called MAROST (MARoc OSTréiculture) which was a commercial-scale enterprise. Through its operations it produced several marine fish species (sea bass, sea bream and European eel), shellfishes (flat oyster and European clam), and prawns (Japanese prawn, called also kuruma prawn). Almost all the production of cultured species was intended for export to Europe, especially to Italy, Spain and France, with a little amount sold in the domestic market. On the technical level, this stage constituted the turning point in Moroccan aquaculture history. On the Mediterranean coast of Morocco, broadly three types of aquaculture systems were developed from the middle of the 80's to the middle of the 2000's. The first type of these systems was the lagoon aquaculture, developed in Nador lagoon in the late 80's. This system utilized the use of floating net-cages for fish culture, floating long-lines and fixed metallic tables for oysters and shallower areas enclosures for clam culture. The second type of these aquaculture systems was land-based developed in the beginning of the 90's using earthen ponds located in the extreme north-east of the Mediterranean coast of Morocco in Moulouya Estuary, south of Saidia,. At the beginning, these facilities were used for prawn culture. Soon after that, they were utilized for sea bass and sea bream aquaculture. The third type of aquaculture systems was also employed in the early 90's which was open-sea aquaculture. This type was initiated in M’diq bay using large floating net-cages for the blue-fin tuna culture. Consequently, this experience encouraged the use of open-sea technology, since the late 90's, on other marine species especially the sea bream and sea bass. In which these species were cultured in floating open-sea conventional cages that were established in M’diq bay and in Martil bay (in Azla site) and for mussel culture using wooden floating rafts. Similarly, the lagoon aquaculture system prevailed on the Moroccan Atlantic coast, mainly in Oualidia lagoon situated in the centre of the Moroccan coastline. Oyster culture methods remained generally based on the use of wire and weave trays and the use wooden fixed table. The latter was however partly become made of concrete. In the late 90's, floating submerged lines and immerged pearl net and lantern net were attempted for mussels and scallop, respectively, in Immessoune bay, whereas in Agadir bay, floating lines were experimented for mussels. Furthermore, fixed lines in shallow waters were used on small scale for commercial oyster grow-out in Khnifiss lagoon, located in the south of Morocco. The most important shellfish culture operation that was recently achieved was in Dakhla bay in the early 2000's, based on local integrated aquaculture planning, using enclosure culture techniques in shallow waters to grow mainly clam and oysters in significant quantities. Parallel to these advances in aquaculture technologies and the diversity of cultured species, the necessary skilled work force was developed through domestic and education abroad, field and practical training, etc. This has contributed to the mastery in aquaculture techniques, especially the intensive culture systems including hatchery, nursery, long-lines and floating net-cage techniques. During this stage, the progress of marine aquaculture development has yielded a significant increase in the national production (Figure 1). 214 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Figure 1. Production of mariculture sector of Morocco during the last 10-12 years.

Figure 2. Sea bream and sea bass production and price trend in EU.

The reason behind this progress was the belief that the aquaculture industry could widely expand into many other potential areas, and to catapult the private sector's investments, both on the Mediterranean and the Atlantic coasts. This situation demanded effective cooperation between the professional and scientific communities as well as the administration to join forces in many aspects of the industry especially in the risk assessments in foreign markets, which has completely influenced the national aquaculture industry outcome. Consequently, the Moroccan aquaculture industry confronted serious market problems. For example, Marost Aquaculture Company has been obligated, in the early 90's, to review its Review of Moroccan Aquaculture 215

strategic production choices, particularly in terms of which economically suitable species the farm should continue to culture. Then, shellfish culture (flat oyster and European clam) was highly impacted by the stringent European sanitary restrictions at the end of the 80's, which led to the reduction of Marost’s bivalve production amounts. Eventually, sales dropped significantly and became very limited to small quantities sold in the domestic market. Even fish culture operations (sea bream and sea bass) were not saved from this negative outcome, where at the beginning the industry went through a steady increase in demand during the 90's before getting seriously impacted by the drop in the European market prices (Figure 2). Although developing to a high technological level, the Moroccan marine aquaculture was very vulnerable to the competitiveness of foreign aquaculture markets. It suffered a great deal from the drastic drop in the prices of their commercially cultured species on European markets since the middle of the 90's. During which the sale price was sometimes a little bit lower than the production coast. In contrast, Oualida oyster culture remained stable in production (Figure 3) and was harmonious and compatible with its domestic market. Although still reliant on wild collected spat imported from France, it was able to keep its annual production rate around 200 – 300 tons for many years. This stage was also characterized by the development of applied aquaculture research, mainly by INRH. The latter has executed numerous pilot scale experiments such as: open-sea aquaculture (blue-fin tuna, red porgy, meager, scallop and mussels), controlled reproduction in new candidate species, fish nutrition and diets formulation based on local ingredients, pathology of cultured fish and shellfish, integrated aquaculture planning, etc. The most challenging research work was achieved in the joint cooperation between Morocco through INRH and Japanese Government through its Overseas Fishery Cooperation Foundation (OFCF) on blue-fin tuna aquaculture, in which the project lasted from 1993 to 1999.

Figure 3. Production trend of Moroccan marine aquaculture by group species (1990-2006). 216 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

The Third Stage

This stage is very important and critical, and probably started in the middle of the 2000’s. From production standpoint, it is characterized by a sudden drop in marine aquaculture products because of the eventual failure of Marost Company at the end of 2006. All its land- based facilities and lagoon-based growing facilities have been removed. The lagoon of Nador is currently subjected to many development projects, mainly of touristic nature. Moreover, the lagoon of Oulidia also facing some environmental quality problems shifting its sanitary status from A grade to B grade, which required the establishment of a purification station. In contrast, the Khnifiss lagoon has been downgraded for oyster and mussel culture operations because of its significantly high environmental risk on the culturing of these species. Khnifiss lagoon is naturally very rich in the heavy metal Cadmium which is relatively highly bio- accumulated in cultured and wild shellfishes.

FRESHWATER AQUACULTURE

The development of freshwater aquaculture in Morocco has started since the 20's. From a historical standpoint, it could be addressed over four main phases:

Phase 1, from the 20's to the 40's

The beginnings of freshwater aquaculture in Morocco dated back to the early twenties, when she built the first public fish culture station in 1924 in Azrou, situated in the Middle Atlas Mountain range. The initial duty of this station was to work on the native trout (Salmo trutta fario var. Macrostigma Duméril), both for preservation and propagation into watercourses where it did not exist before. Rainbow trout (Oncorhynchus mykiss), previously called Salmo Gairdneiri, was introduced in 1925 from USA by French parties for sport fishing purposes. However, these efforts could not achieve its artificial breeding systematically until 1936. The foreign community and a limited number of national amateur anglers used trout for sport fishing, a mainly practiced fishing activity. The common carp was also introduced between 1924 and 1935, (Mouslih, 1987).

Phase 2, from the 50's to the 70's

The second public fish culture station was built in Ras-Elma in Ifrane region (1957) along with yet another station, the Azro Station. All hatchery produced trout fingerlings were intended for release into the wild, in lakes, watercourses, and other water-areas. Later, a dozen of 2-14 ha artificial ponds were constructed for Rainbow trout culture that were intended only for sport fishing purposes. This period was characterized by an important development in sport fishing (Figure 4). It corresponded to a period characterized by a proliferation of fishermen associations.

Review of Moroccan Aquaculture 217

Figure 4. A graph showing the trend of issuing sport-fishing permits for water-areas (1953-2005).

Several exotic fish species were introduced in order to enhance fish wildlife and to promote sport fishing. Out of 30 introduced fish species that were selected from the most important European and North-American ones, only half of them were able to adapt well to local conditions. In fact, some of them were well known for their sport-fishing value and their highly appreciated flesh quality, such as rainbow trout (Oncorhynchus mykiss), pike (Esox lucius), largemouth bass (Micropterus salmoïdes), pike-perch (Stizostedion lucioperca) and European perch (Perca fluviatilis). Other species were introduced for consumption purposes as food such as common carp (Cyprinus carpio), roach (Rutilus rutilus), the Rudd (Scardinius erythrophtalmus) and tench (Tinca tinca). The introduction of such alien fish species was carried out without prior scientific studies of their possible impact on the environment and the endemic fish stock. Eventually, these alien fish species have caused the extinction of the Moroccan endemic species Salmo pallaryi (Pellegrin, 1924; Mouslih, 1987). Moreover, two crayfish species were also introduced. The American species, Spiny- cheek crayfish (Orconectes limosus), which was widespread in several natural lakes of the Middle Atlas, and the Australian species, Noble crayfish (Astacus astacus), which was more appreciated by consumers. However, the latter required more favorable water conditions, mainly clarity and temperature, than the American species. Mosquito fish (Gambusia affinis) were also introduced but for ecological and human health purposes. It was used to fight against malaria disease using its ability to feed on mosquitoes larvae. All of the artificial breeding operations of fish species were first carried out within the fish culture station of Azrou. Later, these operations were expanded to two other fish culture facilities, Ras-Elma in Ifrane and the National Centre of Hydrobiology and Fish-culture (CNHP) in Azrou which was built in 1980.

Phase 3, from the 80's to the 90's

This phase was first characterized by the establishment of the CNHP in Azrou in 1980. This Centre is a research institution devoted to applied breeding research on freshwater 218 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla fishes and to hydro-biological studies of freshwater areas suitable for fisheries exploitation. Also, during this phase (from 1981 to 1999) three Chinese carps were introduced: Chinese (or Grass) carp, Ctenopharyngodon idellus (Valenciennes, 1844), silver carp, Hypophthalmichthys molitrix (Valenciennes, 1844) and bighead carp, Aristichthys nobilis (Richardson, 1845). These species were introduced in order to reduce eutrophication in lakes, reservoirs of dams and irrigation canals (Azeroual et al., 2000). CNHP has effectively played a crucial role in the enhancement of artificial breeding of freshwater fish. It has undertaken hydro biological studies of all aquatic environments concerned with fishing and farming (physical and chemical water quality, weeds, aquatic wildlife, fish pathology, etc.). Also, it has gradually implemented important procedures such as breeding design with respect to ecological considerations, selecting the most favorable adaptable species, defining the suitable size for releasing, etc. Through its artificial breeding programs, culturing and releasing fishes, and in maintenance and monitoring of rivers, and natural and artificial lakes, it became indeed the pedestal foundation for the inland water's permanent richness, allowing preservation and development of diversified fish resources. Hatchery produced fingerlings was enhanced increasing the release capacity of fingerlings for inland water areas. The construction and the launch of the Deroua station designated mainly for carp culture, in Beni Mellal region, have contributed significantly to the large fingerlings production capacity. The fingerling hatchery production component became an important tool for freshwater fisheries. The latter became almost entirely dependent on restocking programs, which is one of the most active working plans of HCEFLCD. As a matter of fact, aquaculture operations for restocking purposes has increasingly played important roles, particularly in improving good water quality and proving aquatic protein for local populations. On the socio-economic aspect, fishermen communities were setting-up their operations near the important restocking freshwater fish areas, particularly large dams reservoirs. Encouraged by this healthy development of events, HCEFLCD focused its activities towards promoting freshwater restocking aquaculture with special emphasis on promoting fish farming to supply rural populations with sufficient quantities of food-fish. According to this trend, carps became a major rural food fish species in some localities in Morocco. Although they were initially introduced to fight off the biological eutrophication in the irrigation canals and reservoirs dams, they have later caused a spectacular spontaneous development in local water conditions. Indeed, they have propagated naturally at high rates leading to further development in commercial fishery, and generating social and economic benefits for both aquatic environment quality and rural socio-economy. Even though, the sustainable success of such important speculation is dependent a lot on the well organization of the profession. In this regard, CNHP has undertaken socio-economic surveys and awareness sessions for the largest reservoirs dams’ fishermen in Morocco.

Phase 4, the Current Period of 2000's

Once the feasibility of freshwater fish farming and the management of water areas have been established, private investment sectors were encouraged through leasing fishing rights or the installation of aquaculture units. Indeed, it has been expected that the support provided by HCEFLCD would encourage the private investment in freshwater fish farming. However, Review of Moroccan Aquaculture 219

only few private fish farms are currently active in culturing carps, rainbow trout, European eel and Nile tilapia. Carps and rainbow trout are the most cultured freshwater fish species by private aquaculture ventures in Morocco (Figure 5). Although hatchery-produced carp fingerlings are mainly intended for release in dams’ reservoirs, a little part of this production is also used for commercial production. The total hatcheries production of carp fingerlings is 6.5 million, of which 4 millions are produced by private hatcheries and 2.5 millions by CNHP’s Stations. Some private farms use earthen ponds, such Pisciculture-Smir farm to grow carps. Trout commercial production is practiced by the same farm since many years in Azrou (HCEFLCD, 2008). Its production attained 98 tons in 2007, of which 52 tons were processed (filets, smoked, etc.).

Figure 5. Evolution of freshwater aquaculture production by fish group species (1998-2006).

Recently, Nile tilapia was introduced in 2002 from Egypt for commercial aquaculture production. It was introduced by the freshwater private fish farm, “Pisciculture du Nord”, which was recently established and has opted for an integrating culturing system including all phases of production, from hatchery to processing and selling. Nile tilapia is currently well bred in local hatcheries and is successfully cultured in three culturing systems (intensive, semi-intensive and extensive), using Fiber-glass polyester, concrete and earthen ponds that are managed separately in the same location. First results seem to be encouraging in mass selection and in breeding of selected fish populations.

CURRENT STATUS OF MOROCCAN AQUACULTURE

Aquaculture Production

Today, with the unexpected failure of Marost, there is only one operational fish farm that cultures marine fish on the Mediterranean coast of Morocco (Aqua-M’diq located in M'diq 220 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla bay). Its production capacity is about 200 tons per year of sea-bass and sea-bream. Also, there are currently eighteen active shellfish farms culturing oysters, clams and mussels, of which seventeen farms are on the Moroccan Atlantic coast and only one on the Mediterranean coast. The latter is based in M’diq bay and cultures mussels. Among those located on the Atlantic coast, there are ten oyster farms based in Oualidia lagoon, four oyster and clam farms in Dakhla bay and two mussel farm in Immessouane bay. There is also one oyster farm still existing in Khnifiss lagoon but without having the right to sell its products. Moreover, there are some small shellfish farmers, constituting local small cooperative associations. They are currently mainly involving local fisherwomen, particularly in Moulay Bouselham and in Sidi Moussa lagoon’s. These small shellfish farmers grow European clams. Their total production capacity is about 50 tons / year. In the time being, the total production of marine aquaculture farms currently in operation seems to not exceed 600 tons for a national potential production of largely higher value. The development of Moroccan marine fish aquaculture has been in fact seriously hampered by significantly important subsidies granting policy of European Union to their aqua-farmers which has greatly lowered non-European aquaculture products competitiveness. Moreover, production costs are very high, particularly on marine land-based aquaculture which faces, among others, land problem and high cost energy that is significantly slowing its competitiveness on the international markets. While marine fish culture faces a critical development phase, shellfish culture remains relatively constant in terms of production since many years ago. This is due the equilibrium between standing domestic market demand and shellfish farming supply. However, prawn culture has failed to survive. Some attempts toward culturing Japanese prawn have taken place in the late 80's and early 90's, but at present, although some particular projects have gotten initial authorization to start their activity, there is no prawn culture farm at all in Morocco. Prawn-culture has very short history in Morocco. Although two farms in the north-east of the Mediterranean coast of Morocco have tried prawn-culture and both have established their own prawn hatchery, this activity was not able to flourish due to economic reasons. In fact, the competition with tropical and Asian countries was so high, and market prices were not favorable for continuing the prawn-culture operations in Morocco. Considering the short lived-operation and the past trend of production fluctuation in the prawn culture, there is no possible predictable trend for the prawn aquaculture in Morocco. But, its future could rely on the efficiency of site management and domestic market demand. In terms of freshwater fish culture, this activity consists mainly in restocking operations based on hatchery-produced fingerlings. The main propagated species are common carp, silver carp, Chinese carp, rainbow trout, and brown trout. There are many other bred fishes which are getting some progress in breeding procedures and may be mass produced in the near future. The annual fingerlings production of the most common cultured species can reach more than 8 millions. Enhancement production plan is in fact being considered in an in-depth operational study. Competent administrative department is required to significantly increase the production quantity of cultured organisms for domestic needs. To achieve the target objectives, it has been recommended to improve the quality of culture propagating units, culturing units and feeds processing units.

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POTENTIAL SITES FOR AQUACULTURE

Marine Aquaculture

Morocco enjoys an excellent geographical situation with two distinct maritime fronts (Atlantic and Mediterranean) that have a combined length of around 3,500 km. Thus, the national coastline offers several natural potential sites where aquaculture activities can be practiced (Figure 6) (Orbi et al., 1996).

Mediterranean Coast

Atlantic Coast

Figure 6. Geographical location of the potential sites of marine aquaculture. 222 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

However, in Morocco, the marine aquaculture development is not only a complementary and strategic element for fisheries, but also assures preservation and planning of the coastal zone as well as their economic and social improvement. For this reason, two options are foreseeable: to implement development on the existing social and professional class and/or to implement development on external funds and competencies (to attract some national and foreign investors). Therefore, the main potential sites are subdivided into three categories:

Potential Sites with a History in Aquaculture

In this case the objective is the preservation and rehabilitation of the aquaculture sites.

Nador Lagoon: It is a large lagoon system with an area of 120 km², situated in the Northeast of Morocco, it connects with the open sea through a single passage that is 80 m wide. (Lakhdar Idrissi et al., 2005). Due to the geological structure of this region and the formation of the lagoon fishing area with considerable potential for aquaculture (Orbi et al., 2008b). During the past 20 years (1986 to 2006), this site achieved an aquaculture production of about 1000 tons (sea-bream, sea-bass, oyster and clam). Currently, this activity is completely stopped due to serious problems essentially linked to market conditions, pollution and urbanization development. However, with the expansion of natural algae fields (Gracilaria), this site could be dedicated to seaweed culture (Abdellaooui et al., 2005). Oualidia Lagoon: It is the oldest aquaculture site in Morocco (Hilmi et al., 2005; Orbi et al., 2008b), and is located on the Atlantic side, 76 km south of El Jadida. This tidal lagoon is shallow and is influenced by freshwater ecosystem.

There are 10 oyster farms around the lagoon and its yearly production turns around 300 tons (Rharbi et al., 2001). Currently, aquaculture activities in this site meet serious problems related mainly to the environmental deterioration as a result of different anthropogenic pressures (organic and chemical pollution). But now, many actions which are undertaken by the government are focused on preservation and rehabilitation.

Potential Sites for Industrial Aquaculture

In this case the objective is the development of commercial aquaculture activities integrated with a management concerted with different coastal users (fishing, tourism, etc.). Review of Moroccan Aquaculture 223

M’ Diq Bay: It is located on the Mediterranean side, between Sebta in the North and Cape Negro in the South. Characterized by a weak slope, current and hydrological conditions favorable to aquaculture development (Lakhdar Idrissi et al., 2001a and b). There are 10 farms in the area but only two of them are operating with an annual production of approximately 500 tons (300 tons of fish and 200 tons of shellfish). This location is considered a potential site for industrial aquaculture. Thus, a development plan of aquaculture as well as an integration of this activity in the light of the global development of the region is under elaboration by the Marine fisheries Department.

Agadir Bay: located in the south of Morocco with an orientation of Southwest - North. This bay is characterized by a large morphological and geological diversity. The depth of the region does not offer any particular advantage. The sea bed rises gradually from 100 m between 6 to 10 miles away from the coast to 20 m within one mile from the coast. This bay represents an ecosystem with strong primary production privileged by different oceanic currents (Upwelling, the Canary current) with temperature variations more important than in the Northern marine ecosystems.

224 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Indeed, these factors (food availability and temperature) have some important consequences on the growth rate of cultured shellfish. Furthermore, with the present development (tourism, agri-food industry, etc.), this region constitutes a potential market for aquaculture products (fresh and processed). Also, in order to contribute to the aquaculture development in this bay, a specialized research center in aquaculture is in the process of establishment in Agadir under the framework of the Spanish cooperation. Dakhla Bay: Among all identified bays along the coastline, Dakhla bay is distinguished by its configuration and diversity of biotopes. Situated at the Sahara coastline, this bay, is oriented NE – SW with a length of 37 km and a varying width between 10 and 12 km.

Edged along its whole length by a narrow dune ridge elevated at 5 meters that naturally protects the area against strong surges (very protected zone). It is separated from the Atlantic ocean by the Oued Edahab peninsula, but it has a large connection with the ocean (10 km) which makes it relatively enclosed environment. The bay possesses a shallow depth of 1 to 3 m on the periphery and 6 to 9 m in the center. Also, with high number of canals that were created by the swing of tides and whose maximal depths do not exceed 20 m, this lagoon is an important potential site for aquaculture and particularly for shellfish culture. Indeed, this activity is currently practiced by 4 oyster- culture farms and 1 clam-culture farm and the annual average production is about 100 tons.

Emerging Potential Sites

In this case the objective is the development of a income-generating aquaculture activity in synergy with developing fishermen’s village and natural reserves. Imessouane bay: It is a small bay located 100 km south of Essaouira and 90 km north of Agadir in southern Morocco. This site has been transformed into a fishermen’s village. Localized in an upwelling zone, this site has a good potential for shellfish culture. Currently, there are two farms of mussel culture with an annual production close to 50 tons. Through Review of Moroccan Aquaculture 225 their organization in cooperative, local small-scale fishermen are involved in the culture practice in order to diversify their activity and improve their income.

Khnifiss lagoon: This lagoon is located in the south Atlantic coast of Morocco, 170 km north of Laâyoune. It has a length of 20 km and an area of 65 km² surfaces and is oriented on a NE – SW axis. It opens into the Atlantic Ocean by a narrow passage of about 100 m and continues toward a saline area known as ''la Sebkha Tazgha''. The depth of the main canal vary between 5 and 6 m in front of the passage and decrease in the upstream direction (Lakhdar Idrissi et al., 2001c and 2004). The first aquaculture facilities were established there in 1995 by the introduction of scallop culture.

Currently, only oyster culture is practiced, but with its new status as a National Park, this lagoon is undergoing new activity development such as tourism, bird watching, etc. Therefore, for the environment and resource preservation, an income-generating aquaculture activity could be well developed there (Orbi et al., 2008a).

226 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

FRESHWATER AQUACULTURE

The current situation of freshwater aquaculture is still below its real development potential. HCEFLCD has recently carried out a study of the continental fisheries and aquaculture in order to establish a master plan for its sustainable development. This study has highlighted that Morocco has effectively significant potential water areas for restocking aquaculture and fish farming development. These potentials water areas were estimated at 200,000 hectares (ha) in total, of which 1,500 km of watercourses, 60 ha of artificial ponds, 700 ha of natural lakes and more than 100,000 ha of reservoirs dams. It has been shown that such development could contribute to socio-economic development, with the most significant impact being in the rural areas.

CULTURED AND INVESTIGATED SPECIES

The species produced through aquaculture in Morocco include mainly fishes and bivalves. Also, some species of crustaceans and seaweeds have been investigated with less success. Among cultured species, some are considered as traditional for Moroccan aquaculture while others still need more research efforts to be successfully cultured.

Major Marine Species Cultured or under Investigation

Sea-bream, (Sparus aurata) At the beginning it was produced using wild local caught juveniles. Then, hatchery produced fry were produced by Marost fish hatchery since late 80’s. Sea-bream hatchery produced fingerlings varied annually from 2 to 5 million individuals which were all used only for Marost own culture needs. The other farms relied on the importation of fry from Spain and France to meet their own needs. In terms of rearing, experiences achieved in the collaboration between the INRH and MAROST showed that juveniles with an average weight of 130 g cultured in floating net cages in Cape de l’eau, reached 400 g four to five months before those that were reared in identical cages in Nador lagoon (Figure 7). On the other hand, juvenile having an average weight of 2g showed a very weak growth in Cape de l’eau. This discrepancy in growth rates is probably attributed to the strong currents characterizing this site.

Sea-bass, (Discentrarchus labrax) Similar to the sea-bream, sea-bass was first produced using wild local caught juveniles. The captured juveniles often contained a small percentage of sea-bass Discentrarchus punctatus. Hatchery produced sea-bass fry were thereafter produced locally by Marost fish hatchery since late 80’s. The annual amounts of hatchery produced sea-bass fingerlings varied from 2 to 6 million individuals. All this entire production was used only for Marost own culture needs. The other farms depended on the importation of fry from Spain and France to satisfy their own needs.

Review of Moroccan Aquaculture 227

Figure 7. Differences in mean growth rate of sea-bream in floating cages.

Figure 8. Mean growth rate of sea bass cultured in floating cages.

Trials to culture this species in M’Diq Bay showed that, sea-bass juveniles with an average weight of 12 g, cultured in floating net cages reached 400 g in 16 to 18 months (Figure 8). Sea-bream and sea-bass are the most important cultured marine fish in Morocco (Figure 9). They both exhibit the same trend in culture production. First, an important steady increase of production was achieved during the first half of the 90's, to reach mean production values of 500 to 600 tons each. Then, this trend was followed by a broad decrease since 1997, to be stabilized around 300 to 400 tons each during the most part of the first half of the 2000's. 228 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Figure 9. Evolution of marine aquaculture production from 1990 until 2006.

The maximum production amount recorded for sea-bream and sea-bass were respectively 792 tons in 1994 and 845 tons in 2005. Three of the 4 farms which used to culture these two species failed successively on 1997 (La SAM), 2001 (DORALOUP) and 2006 (MAROST). All of these fish farms were located on the Mediterranean coast of Morocco. Currently, only one farm (AQUA-M’DIQ) still continues to culture sea-bream and sea-bass while there are many projects which have got basic license without succeeding to achieve their establishment.

Bluefin Tuna, (Thunnus thynnus) This species has been the subject of an eight year experimental captive breeding and grow-out project, which has lasted from December 1992 to August 2000. This project was executed in the framework of the scientific and technical bilateral cooperation agreement between Morocco and Japan involving Moroccan researchers from INRH and Japanese experts from OFCF (Overseas Fishery Cooperation Foundation). Two main experimental phases were conducted for more than three year duration each, using wild caught blue-fin tuna. The first phase was initiated using local trap-caught giant tunas (76 fishes) with an average weight of about 250 kg each. These tunas were caught while migrating back to the Atlantic Ocean through the Gibraltar Strait after their spawning in the Mediterranean Sea. Subsequently, they were kept in large floating net cage moored in 45~50 m deep open sea site. They were fed two times per day on mackerel, horse mackerel and squid every day, except Sundays. The second phase utilized medium sized tunas (109 fishes) with an average weight of 55 kg each. These tunas were caught in Spain by purse seine and brought to M’diq by suitable maritime transferring means. The duration of this maritime transfer was 11 days, during which tunas were kept in a Bridgestone transporting fish cage which was towed by a tugboat. The velocity of the transfer towing was about 1.5 miles and tunas were regularly fed trash fish (Iioka et al., 1999 and 2000).

Review of Moroccan Aquaculture 229

Other Species under Investigation

Red porgy, (Pagrus pagrus), Common Dentex, (Dentex dentex), Golden grouper, (Epinephelus alexandrinus), Brown grouper, (Epinephelus marginatus) and Meagre, (Argyrosomus regius) are the main fish species subjected to applied breeding research by INRH during the 2000's. The broodstocks of these species were collected from local caught fishes, except for the meagre which was imported as juveniles from France. While Red porgy and Dentex have been successfully reproduced in captivity for many years, the other species still face some difficulties. Red porgy was investigated in a pilot scale trial rearing them in floating net-cages. This work which was done in a joint partnership with a local farm (Aqua-M'diq) showed very interesting results. The process of gonad maturation in the adults has largely occurred in the fish natural habitat prior to catching them. The majority of individual adults were captured while they were in an advanced stage of sexual maturity. Therefore, spawning was spontaneous and was achieved through several successive spawning patches. Spawning started from March and continued until May (Talbaoui et al., 2002). The photo and thermo - periodic cycles during spawning (Figure 10) show that Red porgy spawning occurs during the ascending phase of temperature (15.8 to 17.8°C) and photoperiods (12 h 14 min to 13 h 58 min) (Talbaoui et al., 2006b). Growth curves of obtained Red porgy larva are represented in Figure 11. These curves show a more active growth trend than those of Sea Bream Sparus aurata in our rearing conditions (INRH Aquaculture Center). The cultured fishes reached an average weight of 400 g in 18 months, feeding on sea-bass commercial pellet ((Talbaoui et al., 2006b).

Figure 10. Spawning season of Red porgy Pagrus pagrus during 2000 and 2001. 230 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Figure 11. Linear growth of Red porgy Pagrus pagrus larva.

Common Dentex (Dentex dentex) Under the umbrella of the Morocco- Japanese cooperation project, larval and alevins rearing trials were taken to a pilot scale level. In these trials several biological and physical parameters were tested such as initial larval stocking density, dissolved oxygen, temperature, photoperiod, luminous intensity, food, etc. To achieve that, 4 series of larval rearing trials were conducted in order to improve the aquaculture technology and the requirements of the captive environment of Dentex larval culture. From a total of 127 spawning trials (Figure 12), about 17 million eggs have been collected. Of that amount, 13.6 million eggs were viable (77% viability rate) ( Ait Ali et al., 2003).

Figure 12. Spawning trials and egg production of Common Dentex. Review of Moroccan Aquaculture 231

Figure 13. Growth rate of common dentex fingerlings exhibiting promising results.

This rate decreased considerably to 0% at the end of the season. However, growth rate of fingerlings exhibited a positive linear relationship indicating very promising results (Figure 13).

Japanese (Pacific) cupped oyster, (Crassostrea gigas) The culture of this species has a relatively long history in Moroccan marine aquaculture, and is considered the most valuable seafood product. The production rate of this species is indeed the highest among all cultured bivalves in Morocco (Figure 14).

Figure 14. The aquaculture production of several marine bivalves exhibiting variable growth rates from 1990 to 2006. 232 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Since its beginnings many decades ago and still today, its culture remains dependant on spats imported from France which are collected from the wild. Oualidia Lagoon is considered the first site where commercial grow out operations are carried out. Also, oyster culture operations in Khnifiss lagoon have lately achieved some technically successful productions with very significant growth results. Nevertheless, this site still requires more environmental investigation studies, especially regarding the impact of naturally existing heavy metals (Cadmium) brought to the site by seawater currents flowing from the surrounding upwelling. Since the late 90’s, studies have indicated that Dakhla Bay can also be an important culture area for the same species. Further more, data collected are suggesting that more investors are willing to invest in this site providing the opportunity for this site to be the most important bivalve culture site. Indeed, the research studies concerning the growth and mortality of cultured oyster in this bay indicate that spats with a length of 8 and 27 mm have grown to 114 and 121 mm, respectively during one year of rearing (Berraho and al. 1998) (Figure 15). These growth rates are very promising and are superior to those observed in other sites. In general, the growth rate of oysters in this bay is very rapid from October to May and then becomes slightly constant until September (Zidane et al., 2008)

Figure 15. Growth of cultured C. gigas in Dakhla Bay (A: 8 mm spat; B: 27 mm spat). Review of Moroccan Aquaculture 233

Flat oyster, (Ostrea edulis) It is a native species in Morocco, particularly on its Mediterranean coast. In the 80's, a large natural stock exists in the Nador’s lagoon. Marost used it to produce, in its own bivalve’s hatchery, a few millions spat of this species and locally grown for commercial purposes. Problems faced to export Moroccan cultured fat oyster to Europe have been the main cause to give up and to renounce its breeding. However, in early 2000s, hatchery produced spat of flat oyster were introduced from Canada, by a private farm (Aquasur), for experimental growing purposes in Khnifiss lagoon. This experience was not being able to be renewed because of low zoo-technical results and the uncertain quality of the imported spat.

European clam, (Ruditapes decussatus) This species is native to Morocco and its natural stocks cover almost all Moroccan lagoons, estuaries and bays (El Moussaoui et al., 2005). These stocks are all heavily over- fished. Thus, the remaining stocks are too weak to support any kind of fishing effort (Labbardi et al., 2005). Clam culture operations began in Nador’s lagoon during the late 80’s, relying on local hatchery produced spats. These operations were not sustainable because of the difficulty and complexity of the culturing techniques in addition to the physical characteristics of some of these sites like muddy sea bed which lowered the production efficiency (Shafee et al., 1998). Thereafter, several attempts were carried out in other lagoons such as Oualidia and Moulay Bousselham to culture this species of clam, but all of these attempts failed eventually. However, since the late 90's other clam aquaculture operations emerged in Dakhla Bay. The first results from that site showed good growth of clam length (Figure 16). At the beginning, these emerging new aquaculture projects of this species were totally relaying on the locally available wild juveniles, which were caught inside the exploited area. Thereafter, all clam culture projects were required to produce their own spats from their hatcheries in order to preserve the remaining local stock of this species. Currently, a private local clam hatchery is planned to be established with a production capacity of more than a 100 million spat per year.

Figure 16. Length growth of cultured clam Ruditapes decussatus in Dakhla Bay. 234 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Japanese Scallop, (Patinopecten yessoensis) This species is not native to Morocco and was introduced in 1995 from Canada by the private company, Aquasur, for experimental growing trials in Khnifiss Lagoon. Due to the encouraging positive growth rates observed, the experimental breeding trials were further extended in 1998 to other potential sites like the Imssouane Bay, located north of Agadir. The decision to select other sites was made to reduce the high mortality rates observed in Khnifiss Lagoon which was attributed mainly to temperature regime. Once this problem was solved by moving these trials to Imessouane Bay, encouraging results were recorded and sea ranching of this species in this lagoon was possible. However, other types of problems emerged with changing the original locality which was mainly due to difficulties related to spat provisions. Consequently, these trials were stopped in 2004. The main results obtained from this productive experience in Imessouane Bay point to important growth success where commercial size of scallops was attainted in 13 months (Figure 17) with varying mortality rates (Idhalla et al., 1998 and 2000).

Figure 17. Encouraging data regarding growth and mortality rates of cultured scallop Patinopecten yessoensis in Imessouane bay. Review of Moroccan Aquaculture 235

Japanese prawn (Parapenaeus japonicus) In 1997, 250,000 post-larva (PL-70) were imported from Spain for growing purposes at a commercial scale. In 1998, other prawn breeders were imported to initiate reproduction trials in the shrimp hatchery of Marost. The first hatchery post-larva production reached an amount of 1.5 million of PL-75. The grow-out phase was carried out in permanently submerged rearing structures (enclosures). However, the site for the submerge enclosures has required fastidious survey, control and servicing works. Additionally, there were many commercialization difficulties due to the low European market prices compared to the high production cost in Morocco. Also, many other constraints have appeared, particularly prawn losses due to predation and inefficient harvesting techniques. No follow-up commercial attempts were thereafter made by Marost, except for another company (La SAM) which has tried in the early 90's to breed this shrimp species in earthen ponds, using its own hatchery produced post-larva. The recorded productions numbers were very low, less than 40 tons per year. In fact, 35, 31, 7 and 1 tons were recorded in 1992, 1993, 1994 and 1995, respectively, before giving up for the same reasons of low European market prices and high competition with Asian cultured shrimps. Thus, La SAM halted their prawn production operations in 1995 and shifted to sea-bream and sea-bass culture since 1993.

Mediterranean Mussel (Mytilus galloprovincialis) and African Mussel (Perna perna) Both are native species to Morocco. Their wild stocks cover almost all Moroccan coastlines (Idhalla et al., 1998). Most of these wild stocks are heavily over fished and the remaining are too weak to support any kind of fishing effort. Mussel aquaculture began in Cala Iris Bay during the late 70’s. Thereafter, several investigations on mussel culture have been conducted in Agadir Bay. The results showed that for both species, the growth rate in length is fastest in the early phases of culture reaching from 5 to 5.8 mm/month, then after 180 days of culture the growth rate slows down (1st test). Besides, the growth rate of P. perna is faster than that of M. galloprovincialis rate in the two tests. It is also more elevated for spat bet in culture in June than those bet in March (Idhalla et al., 2005). The commercial size was reached at 6.5 to 7.5 months of culture for P. perna and at 7.5 to 8.5 months for M. galloprovincialis. The monthly variations of growth of meat and dry weight are similar for both species. The weight gain for both species decreased in summer and autumn. The growth rate in meat weight varied between 11.2 and 13.1 g/year for P. perna and between 8.2 and 10.8 g/year for M. galloprovincialis (Figure 18). These growth rate values are very promising and superior to those observed in other sites. Currently, emerging mussel aquaculture is being developed in other sites as M’Diq Bay, Imesssouane, etc (Rafik, 2007).

Algae Species Morocco is known for its high agar-agar production (2nd rank in the world). The most important and exploited industrial algal species is Gelidium sesquipedale. Its natural stocks are subjected to heavy exploitation for local agar extraction industry more than for exportation abroad in its raw state. Attempts for algae culture started in the late 90's. Gelidium was tested for mass culture in the coastal area of El Jadida and in Dakhla Bay. Unfortunately, these attempts faced continuous acts of vandalism in El Jadida which is considered a very important area containing large natural Gelidium stocks. Whereas other problems occurred in Dakhla Bay that were in the form of high predation occurrences by the Gold line fish Salpa 236 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla salpa. Other attempts were carried out in 2004 using Gracilaria species in Nador Lagoon without any significantly conclusive results.

Figure 18. Length growth (A) and weight growth of cultured mussel (M. galloprovincialis and P. perna) in Agadir Bay.

European Eel, (Anguilla anguilla) Due to the physiology of this species, its culture attempts were carried out in locations where both the marine and freshwater environments can be utilized efficiently. Commercial scale culture of Eel started in the late 80's by catching eel from the wild followed by rearing until the commercial size. Each culture cycle would last between 3 to 5 months duration of captive holding before selling. Although eel culture gained great interest because of its simple Review of Moroccan Aquaculture 237

rearing/holding techniques and because of its relatively good return on investment, exports did not exceed 100 tons. Cultured eel is exported live to Italy. Major Freshwater Species Cultured or Under Investigation. As is the case elsewhere, freshwater fishes in Morocco, both native or alien species, have been threatened by various factors, particularly domestic and industrial pollution, drought, dam building, water diversion and over fishing. According to Azeroual et al. (2000) there are 30 native and 16 introduced species that are endangered in Morocco which require practical measures to improve the chances of preserving them. Restocking aquaculture is a valid and suitable solution, which can be implemented specifically for this purpose. The most part of freshwater cultured fish species are intended for release in the wild (rivers, natural lakes, etc.) and artificial water areas (dam reservoirs, large earthen ponds). There are currently three major freshwater species that are under commercial aquaculture. In fact, restocking fish activity is the main purpose of the current freshwater aquaculture practices (Figure 19). Almost the all-exotic species brought from Europe and North America, which have been successfully bred in local captive conditions and were well acclimatized to local conditions, are used in restocking programs of several water areas localities. This has allowed the development of fisheries in all concerned regions.

Rainbow Trout, (Oncorhynchus mykiss) It has been introduced in Morocco in 1925 from USA. This cold water fish species is anadromous and since its introduction, it has been released in water areas located in the Middle and High Atlas Mountains range, such as rivers, dam reservoirs and artificial lakes (large earthen ponds). Rainbow trout is a carnivorous species feeding on a wide variety of prey including insects, crustaceans, mollusks and fishes. Despite its relatively long culture history, rainbow culture in Morocco is still less important than what it could be. This species could not reproduce naturally in Moroccan wild water areas.

Figure 19. Development of freshwater aquaculture production by fish species (1998-2006). 238 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Therefore, the use of hatcheries to sustain production seems to be the only possible way to get rainbow trout fingerlings. However, although hatchery reproduction phase is well mastered, the annual fingerlings production in CNHP’s facilities still did not exceed 600,000 individuals even if, in recent years, rainbow trout has become very popular for sport fishing. Commercial trout culture is practiced mainly by one private farm (AIN-AGHBAL Domain), located in the middle Atlas Mountain range where weather conditions are more favorable for rainbow trout breeding.

Brown trout (Salmo trutta fario var. Macrostigma Duméril) This species is endemic to Morocco where it inhabits rivers, tributary streams and rivulets, and lakes of the Rif, the Middle Atlas and the High Atlas Mountains range and some high-altitude lakes. It is well known for its pronounced territorial behavior, it is carnivorous and macrophage. It feeds on live prey, insect larvae, and crustaceans and, under certain circumstances can become ichthyophagous and even cannibalistic. Like the rainbow trout, this species is also artificially propagated and mostly used for restocking purposes using hatchery produced juveniles in the main traditional trout water areas, and lakes. The annual hatchery-fingerling production in CNHP facilities is around 120,000 individuals. Both brown and rainbow trouts remain the key species for restocking mountain watercourses and water areas. CNHP manages yearly to produce sufficient number of trout breeders for eggs and fingerlings production necessary for restocking needs. Moreover, Moroccan wild brown trout stock is considered to be endangered. Its small natural remaining wild stocks are on the decline following the degradation of its natural habitat. Efforts are underway to rehabilitate its habitat and to restore and preserve wild stock trout species which are among the main tasks of the CNHP.

Common carp (Cyprinus carpio), Chinese (or Grass) carp, Ctenopharyngodon idellus and silver carp, Hypophthalmichthys molitrix These three exotic species were introduced to control eutrophication in lakes, dam reservoirs and irrigation canals. Their fingerlings are produced both by CNHP and some private hatcheries. CNHP total production of carp species fingerlings (Deroua Station) reached more than 2.6 million fingerlings in 2007 of which 1.5 millions were Silver carp fingerlings, 900,000 were Common carp fingerlings and 200,000 were Chinese carp fingerlings (HCEFLCD, 2008). Private producers are represented by three major commercial hatcheries situated on rivers shore of Oum ER-Rbia, Loukkos and Smir. The major part of their hatchery produced carp fingerlings are sold to ONEP, (Office National de l'Eau Potable) for stocking in dam reservoirs to biologically control the eutrophication process. The remaining of their production is sold to ORMVA, (Offices Régionaux de Mise en Valeur Agricole), for stocking in irrigation canals to control aquatic weed overgrowth. Originated from China and southern Russia, the common carp was introduced to Morocco in 1924 from France. It was first introduced into the natural lake Merja Sidi Boughaba located in the south of Kenitra. Currently, this species has colonized most of the natural lakes and dam reservoirs. This species prefers calm, warm and stagnant water lakes. Its growth depends essentially on its introduced race and farming conditions. Its introduction in natural lakes has resulted in a negative effect, causing the destruction of other species spawning grounds and increasing water turbidity (e.g. Ifrah Lake). Review of Moroccan Aquaculture 239

The silver carp is native to the Amur River in Central Asia. It was introduced in Morocco from Hungary in 1983 and was released in the irrigation canals of Loukkos. This fish has been well acclimatized to Moroccan continental waters. Its feeding behavior is based on phytoplankton through its water filtration ability. It presents a major factor in controlling the phytoplankton proliferation. The silver carp has colonized the majority of Moroccan dams, depending on the release operations of artificially produced fingerlings. There is no natural reproduction of this species in the water areas where it was stocked. Silver carp has produced good results in Morocco in terms of growth, reaching 3 kg in 1 year, 6-8 kg in 2 years and over 10 kg in 3 years in dam reservoirs. The Chinese (grass) carp is native to large rivers in China, particularly the Amur River. Like the silver carp, grass carp was introduced in Morocco in 1983 from Hungary and was first introduced in the irrigation canals of Loukkos. It was very well acclimatized to Moroccan inland waters. Propagated through artificial reproduction, it has colonized the majority of dam reservoirs and irrigation canals showing a high rate of growth. Exclusively herbivorous, grass carp feeds on aquatic plants and also some terrestrial plants that could be introduced into its habitat (lawn grass, trefoil, etc.). Since the process of digestion is not complete, the ejected feces seem to contribute to water fertilization.

Nile Tilapia, (Tilapia nilotica) Introduced in 2004 from Egypt, by a private promoter for experimental scale culture. It was then stocked in Deraou fish culture public Station, in the framework of cooperative partnership, to check its performances under Moroccan culture conditions. Breeding and culture results were very successful. It is considered as a suitable species for valuating unused and improper water-areas.

Pike-perch (Stizostedion lucioperca) Originally, this species was imported from North Eastern Europe (Finland), through Lake Constance (Switzerland). It is a carnivorous fish which prefers high altitude (up to 2000 m) and calm water areas. Currently, it is well spread through Moroccan inland waters and exists in the largest dam reservoirs (Al Massira, Bine El Ouidane, Mohamed V, etc.), collinear lakes and natural lakes. Because of the good flesh quality and the scarcity of the pike, it became increasingly sought and became subjected to selective fishing.

Pike (Esox lucius) The pike was also introduced in Morocco from Europe (Switzerland and France) since 1939. It was first imported as pike eggs through air transport to Azrou Station where hundreds of thousand fingerlings were produced. Pike is a strictly carnivorous fish. It has taken 10 years of continuous efforts to succeed in acclimatizing the pike to local conditions. In 1954, fishermen started to catch naturally-living sexually mature pike breeders, from fish spawning grounds in a natural lake (Dayet Aoua). Consequently, eggs were obtained from these breeders and were incubated in Azrou Station. Since 1993, pike artificial gonad maturation and spawning techniques were achieved using common carp or salmon pituitary gland extract injection technique. Also, artificial feed for pike larvae was developed and thus fry culture was maintained at high rates allowing the production of more disease resistant fingerlings which are more suitable for release. Consequently, hatchery produced fingerlings 240 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla were of high quality and were better fit for release programs enhancing the stocking of pike fingerlings in some lakes and reservoirs of large dams and collinear dams. Release programs are still practiced by CNHP’s Azrou Station. Pike currently exists in most natural lakes, in some dam reservoirs and one watercourse (Tigrigra in Azrou).

Largemouth Bass (Micropterus salmoïdes) This species was introduced in Morocco in 1934 from USA, through Western Europe. Currently, about 200,000 fingerlings are produced yearly by CNHP’s Stations and released for both sport and commercial fishing purposes. There are many areas in Morocco where it was perfectly acclimatized. It can reach between 5 to 6 kg in Moroccan conditions. This cannibalistic species is considered as one of the higher predators in freshwater aquatic ecosystems where adult fish feed almost exclusively on other fish and large invertebrates such as crayfish. Largemouth bass Fry feed first on zooplankton and insect larvae at the early stages of its life, then as it grows older it becomes active predator. The fingerlings produced by the CNHP hatchery are used in the stocking of some lakes, dams reservoirs and collinear dams.

Tench (Tinca tinca) The tench was introduced in Morocco in 1934, and was stocked in some isolated natural lakes of the Middle Atlas range such as Tifounassine and Aziza. This species is omnivorous which feeds on insect larvae, mainly Dipteral and various mollusks with a trend towards herbivorous diet. It is more resilient than carp and can tolerate low levels of D.O. better than most other fish species. It can stay alive out of water for long periods of time. Currently, the tench is nearing extinction in Morocco and it requires immediate plans of artificial propagation to restore wild stocks.

Red-claw crayfish (Cherax quadricarinatus) This species was introduced from Australia in 2002 by the private fish farm, “Pisciculture du Nord” located in Had Gharbia, in Tangiers region. Since then, this crayfish has been successfully bred in hatcheries and grown out locally in intensive culture systems c It was introduced from USA and released in many aquatic ecosystems of the Middle Atlas range between 1930 and 1992, (Benabid et al., 2003). But, the acclimatization of this species was only successful in the region of lfrane (in water-area Zerouka II). The juveniles production of this crayfish is managed by CNHP which is later released in rivers.

Spiny-cheek crayfish (Orconectes limosus) This carnivorous species is native to North America. It was introduced in Morocco through importation from France. Currently, it is found mostly in Hachlaf water area. In Moroccan waters this species could reach a maximum size of 15 cm. Over time, this species has become a pest presenting a hazard on the dam dikes structures because of its burrowing behavior. Therefore, the idea of eradicating its population seems as a good strategy at this point of time. Review of Moroccan Aquaculture 241

AQUACULTURE TECHNIQUES

Seed Supply

The earlier attempts to culture aquatic organisms in marine or continental waters, relied on imported seeds. In freshwater aquaculture operations, many public and private hatcheries were established and were able to produce their own fingerlings. These fingerlings were stocked most of the time in different water areas with diverse objectives in mind such as improvement of water quality, and enhancement of sport and commercial fishing, etc. On the other hand, marine aquaculture operations still rely on imported seeds, particularly for oyster culture and to a lesser extent for fish culture. The first experimental attempts to produce bivalve seeds by controlled hatchery techniques were performed on the Japanese oyster during 1984 and 1985 in a joint venture between IAV Hassan II “Agronomic and veterinary Institute Hassan Second of Rabat” and a private oyster farm in Oulidia Lagoon. These attempts did not score any satisfying success, nor they have shown that the possibility of local artificial seed production is even possible. Moreover, Oualidia oyster growers have tried to use Marost hatchery-produced Japanese oysters for many reasons. These reasons were to avoid spat importation cost, to overcome substantial initial losses related to transport and other spat settlement techniques and to have a continuous and steady local supply of spats. However, the use of Marost spat was found to be difficult to pursue further due to the high losses incurred in the initial stage of the culture process. While some of these problems could partially be solved by the use of pre-growing equipments and some technical modifications during the initial hatchery single spat stocking phase, oyster growers seemed really not prepared to accept or proceed with any changes or modifications to their normal routine culture practices which were based on the collection of wild oyster spats then settling them on scallop or oyster empty shells. In fact, oyster farmers in Oualidia were not familiar with the techniques required to handle and to rear small single oyster spats. The use of hatchery produced small size (spats retained on a 3.0 mm2 mesh sieve) single oyster seed involves some changes in the routine of the culture procedures, particularly by setting up of pre-on-growing equipments. Local farmers considered this important step as an overly-cautious and labor-intensive addition to the procedure (frequent spat grading operations by hand held sieves of different mesh sizes, etc.). The supply of larger size spats is of course more desirable but it demands a significant raise in cost. For that reason, Oualidia oyster growers still depend on foreign importations of oyster seeds collected from the wild. Flat oyster and European clam were the first bivalve species in Morocco that have been reproduced in the hatchery on a commercial scale. This was achieved by Marost farm in Nador Lagoon on the Mediterranean coast. The hatchery design was made by an American expert using large rearing tanks (20m3 each) for larval rearing. The first spat production of these two species was achieved in 1986. While European clam spats were produced in free single seeds, flat oyster spats produced were settled on mussel's empty shells. In the following years spat production trials of flat oyster were also carried out in free single seeds. The hatchery produced single spats were pre-on-grown in nursery to reach suitable sizes (oyster spats retained on 3 to 6 mm2 mesh sieves and clam spats on 2 to 3 mm2), before being transferred to the sea on-growing facilities. 242 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

In the late 80's, sea-bass and sea-bream culture relied on hatchery produced fingerlings. The first marine fish hatchery was established by Marost farm. The operation of this hatchery started in 1988 and remained in full production for 19 years. Its design concept was based on the ability to use both flow-through and re-circulated systems utilizing borehole water to reduce heating costs. The production capacity of the hatchery was 10 million sea-bass and sea-bream fry. French experts were involved in the daily management of this hatchery, providing on-site training for local staff. The original broodstock used for this production were first acquired locally from the wild. Most of the acquired brooders were kept for spawning for several years. However, new brooder fishes were selected from the first generation reared in captivity. The selection of these brood fish was conducted based on their higher biological performance, and then they were added to the main broodstock population every year. Since sea-bream is a protandrous species where the males sex reverse to females as they grow, new males were yearly supplemented to the captive population. Whenever possible, wild fishes were also added at a rate of 10 to 20 % to renew captive broodstock. After many years of hatchery practices, a proven procedure has been established for broodstock management, in addition to mastering techniques for advancing or delaying spawning for some broodstock in order to extend the spawning season and the hatchery fry production. Hormonal spawning induction was achieved for both, sea-bream and sea-bass, using hCG at the beginning, then later replaced by LHRHa. Currently, these techniques were replaced by manipulating environmental rearing conditions such as the temperature and photoperiod. The latter technique has enabled to extend the spawning process to almost an all year round season. Larval rearing was performed in 4 m3 circular FRP tanks. Operational runs were modulated in groups of 4 tanks each, which were linked to their own independent recirculating system. Improved intensive larval rearing techniques have been successfully achieved for both species as they have been developed in the Mediterranean region. Optimization and control of the major environmental parameters have been undertaken to improve the fry quality and performances in the grow-out phase. Morpho-anatomic deformities, mainly related to skeleton, opercula and swim bladder, have been significantly reduced. Among the 4 marine fish farms, only two (Marost and la SAM) have fish hatcheries to secure their own needs for sea-bream and sea-bass fry. Whereas the other two farms (Aqua- M’diq and Doraloup) import their fry from Spain and France. Prawn seeds were also secured through two hatcheries, one belonged to Marost in 1997 to 1999 and the second one to La SAM in early 90's. Japanese prawn broodstock were imported from Italy. Lack of expertise, shortage of sewing-up and starter feeds, as well as improper design of growing-out facilities were the main constraints for prawn seed production. However, the highest hatchery produced prawn seeds were about 1.5 million for Marost and about 3 millions for La SAM. The Mussel culture operations rely usually on the wild spat collection due to the availability and abundance of local wild mussel populations. Natural mussel beds are important in many coastal areas in Morocco, where they are heavily exploited for domestic market consumption. Out of 7 private experimental farms which were developed for mussel culture using rafts or long-lines anchored in moderate depths of water, only 3 are presently in operation. Mussel culture in Morocco was proven to be technically feasible but largely dependant on the regular spat supply from the local natural stocks. Mussel spats are collected by local fishermen from the surrounding areas of the farm site location. In M’diq for example, Review of Moroccan Aquaculture 243

where a private mussel farm was established since one year and half using floating raft technique, mussel spat settlement occurs all year-round, indicating that mussel spawning occurs through out the year. Therefore, the productivity and efficiency of the culture operations are closely associated with the farmer's efforts to ensure sufficient spat supply. Freshwater fish seeds intended for release operations were imported for many years until the 80's. The first public hatchery for freshwater fish fingerlings research and production was established in Azrou in 1980 (CNHP). This hatchery undertakes applied research to develop and improve freshwater fish breeding techniques. It also produces fingerlings for economical and ecological reasons such as improvement of water quality in some areas and for sport and commercial fishing. Currently, CNHP has three public hatcheries in Azrou, Ras Elma, and Deroua. While Azrou Hatchery is producing carnivorous fish species, Ras Elma and Deroua hatcheries are mainly producing trout species (1.5 million fingerlings) and Carp species (2.5 million fingerlings), respectively. The total hatcheries production of carp fingerlings is 6.5 millions, of which 4 millions are provided by private hatcheries and 2.5 millions by CNHP’s stations.

Feed Supply

Various feeds for cultured fish are imported from foreign markets. Feeds were first imported from England in the late 80's, then at a later stage from France and recently from Spain. In 2004 and 2005, pilot scale trials of sea-bass grow-out were conducted using several experimental fish feeds formulated locally. The formulation of these feeds was carried out under a joint venture between Aqua-M’diq (fish farm), Aquamed (poultry feed manufacturing plant), INRH and IAV Hassan II. These pilot scale trials produced satisfactory results, such that 4 out of the 5 feeds produced from local raw materials, yielded some of the best performances compared to that of imported commercial feeds. All these feeds presented inferior energy contents and P/E reports superior to those of the standard feed (Figure 20).

Figure 20. Continued on next page. 244 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Figure 20. Weight gain of Sea-bass by food type (A) and Variation of the weight gain according to P/E report of different applied regimes (B).

This experimental work elaborates the feasibility of manufacturing formulated feeds from locally available ingredients for marine fishes to the extent that such feeds can be as effective as the imported commercial feeds (Talbaoui et al., 2005 and 2006a). Therefore, it became possible to provide fish pellets domestically for both marine and freshwater cultured fishes, using local ingredients. Two animal feed manufacturers have invested to diversify their production outputs by including fish feed manufacturing equipment. One of the two manufacturers is based in Kenitra and the other is in Hakama village, near Tangiers. The latter manufacturer is owned by an industrial group, which possesses a freshwater fish farm, also located in the Tangiers region, that breeds and grows Nile tilapia. This feed manufacturer uses by-products of shrimp decorticating factories owned by the owner group. Thus, it utilizes shrimp carapaces in the formulation of their fish feeds. Research efforts are still underway to improve the quality of local manufactured fish feeds according to the cultured fish species.

CULTURE HUSBANDRY

Broadly, different rearing techniques and management procedures were employed by Moroccan aquatic species farms. For marine bivalves and freshwater fish culture, the most common method used is the extensive system. Whereas for marine fish, both intensive and semi-intensive systems are employed in floating net cages in lagoon and open sea sites, and in coastal land-based earthen ponds, respectively. Since water quality is the most important factor in aquaculture, monitoring of essential water parameters was always among the main concerns of all farmers. In earthen ponds Particular attention was given to Dissolved Oxygen (DO) and Biological Oxygen Demand (BOD) which are considered extremely important for the cultured fish or prawn growth and Review of Moroccan Aquaculture 245

survival and for the aquatic environmental management. Also, abundant clean water is required to maintain a disease-free culturing environment. Low water exchange rate is also one of the main concerns in cage culture. Depending on site location, fouling of the net cages due to dense algal growth resulted in the deterioration of rearing water quality and fish losses. Fish farmers have tried to use improved quality of rearing nets and to optimize net cages service (frequency of nets change, drying and cleaning procedures of collimated nets, etc.). Other major concerns for the farmers were the stocking densities in limited space, the structure and distribution of cages in terms of their distance from each other and the efficiency and the stability of the mooring system. Another environmental concern was that the long term usage of aquaculture sites for many years led to unfavorable sedimentation of the farm waste materials mostly from feed. Such sediments may produce significant amounts of hydrogen sulfide leading to very low DO conditions. With respect to fish health, systematic diagnosis of diseases is regularly practiced by fish farmers. Marost has a pathological survey laboratory for monitoring and preventing diseases outbreaks and pathogenic organisms from spreading to or from wild species. Some of aquaculture farms have established an effective quarantine system for imported species to prevent unknown diseases from invading local aquaculture and wild environments. Medical treatment procedures, based on the use of specifically authorized medicines and their proper recommended dosages, have been developed and improved through on-site experiences. In general, prophylactic efforts are mostly directed to prevent infestation rather than to cure disease which could sometimes be difficult to eradicate once established. Generally speaking the lack of expertise, scientific breeding techniques, and culture plans and research programs are the main obstacles that face aquaculture farms and hatcheries. INRH and CNHP have always provided as much information as possible on site-selection, choice of appropriate type of techniques and facilities for selected sites, applications for site permits, mooring system installation and improvements on floating culture facilities, start-up operational production trials and management of the rearing environment. Sometimes, both organizations were even involved in the design of facilities, equipment specification and installation, and the first steps for launching the production process. As far as freshwater aquaculture is concerned, it is mainly based on extensive polyculture system which is practiced in dam reservoirs using various fish species. Such aquaculture system and facilities pose practical problems such as refrigeration facilities of captured fish and deficiencies in logistics as well as efficient infrastructure of commercialization.

Manpower

Since the practice of aquaculture and many other related fields are fairly new concepts to the workers in this field, the availability of sufficient qualified manpower was a problem. Some fishermen were converted to aquaculture workers simply by receiving on-site education and training to acquire basic aquaculture operational skills. Since then, development of the human resource element has become an urgent task requiring the design of an appropriate training programs. These practical programs were either conducted locally or abroad to acquire the necessary skilled workforce. Applied training courses and practical programs have recently been arranged for private aquaculture technicians and new young potential investors in joint cooperation with Spain. 246 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Also, training plans have been organized for persons who are involving in aquaculture research and related administrative affairs, in joint cooperation with FAO (CIHEAM) and Japan. On the national level, the number of manpower involved in marine aquaculture field in 2005 was about 344 people distributed over 261 permanent employees, 42 temporaries and 41 service staff including fishermen and divers ( (El Ahdal, 2005). This number did not include research staff. The academic education in the field of fisheries existed since 1975. The aim of these education programs was to meet the increasing domestic needs in maritime and continental fishing sectors. Since then, several strategic education and training methods have been adopted to monitor developments in fisheries sciences and thus was able to adapt academic education to the emerging jobs market. Since 1997, a program was established so that students who graduated from the general agronomy discipline can specialize in fisheries, including aquaculture, over a period of two years. IAV HASSAN II and some Moroccan universities have been trying to offer adequate academic education to respond to the development needs in the field of aquatic live resources exploitation and aquatic environmental management. However, the general problem still exists which is the inability to respond, in a relatively short period of time, to the most urgent and variable requests that are considered as obstacles to aquaculture development, particularly in terms of skilled qualified manpower. Preserving and enhancing productive potentials of wild and aquacultural resources must also be based on integrated strategic approaches with multiple objectives in order to incorporate human resources needs which should correspond to the progress in aquaculture design, planning and management.

REVIEW OF AQUACULTURE RESEARCH AND DEVELOPMENT

INRH and CNHP represent the two public institutions that are dealing with the operation and development of aquaculture research in Morocco (Figure 21). Veterinary Directorate is also involved with INRH and CHNP tasks but mainly in the framework of providing service support for aquaculture establishments in Morocco, by organizing and coordinating the setting up of environmental monitoring and fish pathology survey for existing farming exploitations. INRH and CNHP undertake applied research, field farming and studies on potentially exploitable sites, technical feasibility of new aquaculture species, etc. They are also involved in providing scientific and technical advice and recommendations in aquaculture policy development and management. Additionally, they are involved in aquaculture site license granting procedure for private investors, by providing scientific opinion regarding the biological and technical feasibility of potential projects. These two institutions also support developing private aquaculture projects and farms through joint cooperation with the private sector by giving advice on husbandry improvement of traditionally cultured species, up to date developments on culture techniques of local species, preparation of environmentally integrated farm design, construction specifications and equipments, etc.

Review of Moroccan Aquaculture 247

Figure 21. INRH’s network structure along the Moroccan coastline.

MARINE AQUACULTURE RESEARCH AND DEVELOPMENT

In accordance with its mission, INRH conducts research and experimentation in order to contribute to promoting and developing viable and sustainable marine aquaculture in Morocco (Figure 22). Its marine aquaculture research and development programs are in harmony with the global fisheries strategy defined by the Fisheries Ministry, taking into account the recommendations of INRH’s Administrative Board, comprised mainly of professionals, INRH’s Scientific Committee and the Fisheries Superior Council “Conseil Supérieur de l'Exploitation et la Sauvegarde des Ressources Halieutiques”. Therefore, the main efforts of the marine aquaculture research of INRH have focused on two key aspects:

1. Site identification and classification for aquaculture purposes through 3 main axes: • Identification of potential aquaculture sites through classical selection criteria, (sheltered areas, semi-exposed areas, restocking areas, etc.). • Ecological studies on selected areas which present potential for aquaculture activities. • Conducting breeding attempts for selected marine species in the selected sites.

2. Development of culture techniques for marine species through 3 programs: • A species-diversification program that aims at developing the reproductive technology of some potential candidate marine fish species. • A zoo-sanitary program by the establishment of pathological surveillance protocols to survey and monitor the main wild-captured and cultured marine species of fish and shellfish; • Aqua-feed formulation and production program that aims at developing fish feed from local ingredients based on studies of the fish nutritional requirements. 248 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

Figure 22. The experimental fish hatchery of INRH Aquaculture Center in M’diq. Top: Broodstock culture unit (left), Larviculture unit (right). Bottom: Live food culture unit (left), Biological Lab (right).

Since INRH has acquired significant experience in marine aquaculture, it has actively contributed to the establishment of guidelines, programs and development protocols to support the aquaculture industry. The actions undertaken so far by the INRH can be summarized as follows:

• Examples of INRH studies on potential aquaculture sites and other achievements: a) Contribution to the preparation of the master plan for aquaculture development in accordance with Fisheries Ministry Policy aiming at responsible and sustainable aquaculture development. b) Identification of potential sites for marine aquaculture and conducting investigations on environmental, biological and hydro-biological parameters (Lagoons of Nador, Moulay Bousselham, Sidi Moussa and Oualidia; Bays of M'diq and Dakhla; Estuaries of Tahadart and Loukous, etc.). c) Conducting studies on quality and sanitary aspects in the framework of the National Network Survey of Coastal Sanitary: studies and survey of live captured and cultured aquatic organisms through biological and chemical parameters. d) Animal Health Monitoring Network of captured and cultured marine species: prevailing diseases study and survey. Review of Moroccan Aquaculture 249

e) Multidisciplinary study (physical, biological and sedimentological) of the Dakhla Bay in the south of Morocco and assessment of its potential for aquaculture. f) Contribution to the establishment of locally integrated management plan for Dakhla Bay including shellfish aquaculture component. g) Applied studies conducted for earthen pond aquaculture investment projects in the Tahaddart site (located in south of Tangiers).

• Examples of INRH efforts in the development of aquaculture techniques: a) Conclusion of experimental aquaculture project on blue-fin tuna which was conducted in M'diq Bay during the 8 years framework of Moroccan-Japanese cooperation (INRH and OFCF). Significant results were obtained in terms of growth (average annual growth rate of about 50 kg). Difficulties in captive breeding were attributed to low temperature profile of the culture facility compared to those of the natural spawning areas. However, this project has technically contributed to the development of local open-sea fish culture cages, and to the blue-fin tuna fattening practices in the Mediterranean region. Unfortunately, there were no successive private commercial investments with the exception of the previous commercial blue-fin tuna fattening activities (late 80's and early 90's) to commercially and qualitatively re-evaluate the thin trap caught tunas for Japanese market. b) Applied studies on new candidate marine fish species for aquaculture. These studies are in progress since 2000 by INRH’s Aquaculture Centre in M'diq, in the framework of Marine aquaculture fish species diversification. c) Pilot scale trials on cage grow-out of hatchery-produced red porgy, in joint cooperation with a local private fish farm in M’diq Bay produced significant growth and survival results. However, the final color of the culture fish was grayish instead of the natural reddish color which render the produced fish commercially worthless. Investigations are ongoing to find practical solutions. d) Educating and training fishermen on applied breeding techniques of the European clam. This extension service was made in Moulay Bousselham Lagoon. It was carried out in conjunction with INRH and the Japanese International Cooperation Agency (JICA). e) Monitoring and control of European clam breeding practices which are carried out by local fisherwomen in the two lagoons of Sidi Moussa and Oualidia. These two sites are known for clam fishing activity which constitutes one of the main income sources of the local population. This work was conducted within Fisheries Department Support Program. f) Feasibility study on the breeding of Mediterranean and African mussel species in Agadir and Imessouane Bays. Hydrodynamic and hydrological survey was previously performed to gather useful information and knowledge about the local area environment and to select a suitable open-sea site for mussel culture settling up facilities. g) Experimental culture of Japanese Scallop using long-lines techniques. This activity was conducted in joint cooperation with a private shellfish farm (Aquasure) in the Bay of Imessouane, which hosts a fishing village. 250 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla

FRESHWATER AQUACULTURE RESEARCH AND DEVELOPMENT

CNHP which is located in Azrou was established in 1980. Its main mission was to manage fish resources of inland waters, training of the private sector staff to deal with operations spills, environmental and biological monitoring and control against eutrophication, monitoring of biodiversity, and changes in the environmental and ecological factors of different aquatic ecosystems. The center is linked directly to the Directorate of Desertification which falls under the tutelage of the High Commissioner for Water, Forests and the Fight against Desertification. From organizational point of view, the center includes 5 departments and 2 fish stations, according to the Administration of Water, Forests and Soil Conservation in 1995 (Instruction No. 7, 16/2/95). These departments and stations are:

1. Ichthyology Department. 2. Physical Chemistry Department. 3. Algology and eutrophication Department. 4. Zoology and fish diseases Department. 5. Production department. 6. Deroua Station for Carp culture in Beni Mellal. 7. Azrou Station for fish culture and its annexes.

The missions that are assigned to the National Centre of Hydrobiology and Fisheries are:

a) The hydrobiological study of all aquatic ecosystems of the Kingdom. b) The design, development and fisheries planning through exploitation by fishing and fish farming. c) Propagation and rehabilitation of indigenous fish species and the introduction of new economic species.

PROSPECTS

Although aquaculture is a slow developing industry which suffered several considerable setbacks, the prospects are very promising. Indeed, it relies on the general societal acceptance whether or not to promote and strengthen aquaculture development efforts. It is surely quite fortunate to have such a vast marine coastline, favorable climate conditions and highly skilled national expertise. Therefore, a reorientation of the fisheries policy toward giving more real interest in aquaculture as well as support research and development, will definitely pave the way to establish a solid aquaculture industry. There are many aspects of aquaculture that need development. One of the most important of these is the selection of suitable species for aquaculture. It is crucial to select candidate species of which capture fisheries cannot satisfy domestic and/or foreign market demands. Utilizing modern techniques of biotechnology, it is possible to conduct many high quality research to identify different wild stocks and exploit the richness of the gene pool of many species for purposes of improving the end product of the aquaculture industry. Recent advances in biotechnology, particularly in artificial breeding, will open new venues in Review of Moroccan Aquaculture 251

culturing a diverse range of aquatic organisms which eventually leads to the mass production of new target species fingerlings. Applied marine and freshwater aquaculture research is currently conducted in joint cooperative actions between research institutions and private farms, to develop and optimize local fish feeds. It still has to integrate social and economic aspects on appropriate scale to reconcile local development interests and environmental protection and concern. A human resource development program is being developed through technical and scientific cooperation and assistance which makes aquaculture a suitable income generating business for interested fishermen who have the sprit of entrepreneurs. Certain types of aquaculture such as spat collection do not require large capital investment because of low level of technology involved and because it relies on methods that are suitable for rural and under-developed areas. Thus, aquaculture can offer many jobs opportunities with substantial income for local fishermen. Large sheltered and suitable sites are relatively limited, but a well technically conceived aquaculture projects could however be established even on a small scale. Such project can be operated at many economic levels, such as the family level, small fishermen cooperatives, local communities, or even a commercial-scale enterprise arrangements. Aquaculture could then play an important role in local area economy, creating new economic added-values and employment opportunities. Moroccan people prefer sea-food as a healthy and nutritious alternative despite the fact that they do not consume large quantities. Generally, they prefer the wild fish over the cultured ones, with considerable appreciation of marine species over the freshwater ones. For that reason, accurate information and promotion of marine and freshwater cultured fishes can increase the consumption of cultured organisms. Processing is a suitable way to increase consumer acceptance.

CONCLUSION

Within more than 60 years, Moroccan aquaculture has gone from exclusively traditional exploitation targeting mostly shellfish culture especially oysters for domestic market, to a relatively more industrialized activity targeting various cultured species of increased export value. However, aquaculture production rate did not follow this trend and remained very low and sometimes even decreased relative to aquaculture potential in Morocco. It is worth noting that in general Morocco is looked at by the rest of the world as a large fishing country with no interest or need for aquaculture. Adding to the fact that Morocco has vast and valuable fisheries resources and well developed marine fishing technique, which could provide significant sources of protein to Moroccan people. Despite its very long marine coastlines, its important freshwater areas and its favorable climate, Morocco is not a country with a traditional aquaculture custom. Indeed, among the Mediterranean countries, Morocco probably presents the lowest aquaculture production. Fundamental questions still arise about its real potential that could be effectively exploited. However, suitable choices for aquaculture development should be discussed and emphasized on the national level. This current situation of uncertainty regarding aquaculture development, and the long-term economical risks are the main factors disrupting and hampering private initiatives investments and achievements. Therefore, there is a need to direct current efforts and emerging interests toward a 252 Abdellatif Orbi, Hassan Nhhala and Mohamed Id Halla synchronized emphasis on aquaculture development in Morocco. A clear aquaculture policies, planning and proper management should be developed based on solid, realistic and tangible advantages. Nowadays, aquaculture in Morocco is still not considered as a strategic priority in the fisheries development national plan. Only recently, the issue of aquaculture was included for the first time in the 5 year development plan (2000-2004). The findings of current applied aquaculture research reflect good potential opportunities for investments which may warrant the re-examination of all previous challenges and achievements, particularly under the more recent technical and environmental considerations. Many aspects of a successful aquaculture operation are still lacking such as a comprehensive site selection management plan, technical skills insufficiency, scarcity of fundamental equipments and lack of proper infrastructure facilities. Therefore, there is an urgent necessity for strategic planning of aquaculture development that addresses these controversial issues including specific rights of parties involved and proper legislation and regulating measures. Competent administration efforts should focus on the establishment of specific and concerted strategy based on overall review of the previous policies and the real development needs and assets. Qualified experts who are involved in the administration and in the research and development should conduct regular national surveys on freshwater and marine aquaculture. They should discuss the findings with all concerned parties and partners to evaluate the main problems and constraints affecting aquaculture achievements and to ensure sustainable aquaculture operations in Morocco. Among the controversial issues that are of importance is the culture of highly valued commercial species using more intensive and high cost culture technology. This issue raises the question about what type of aquaculture system should the state promote when the organism involved is of high value. Another issue that should be addressed is the capability of Moroccan aquaculture farms to culture species intended for foreign markets and whether or not it can withstand serious foreign competition. To ensure sustainable aquaculture development, it is important to learn from past experiences and to draw conclusions that could address critical issues. Traditional aquaculture, which is mainly intended for domestic markets, should be rigorously consolidated. Its poses valuable contribution in maintaining adequate seafood supply to meet local demands of the growing national touristic economy. However, as discussed earlier, the development of traditional aquaculture is not quite clear, although there are many coastal areas suitable for shellfish culture, which could highlighted through appropriate research and management efforts. Although in Morocco there are few public and private freshwater fish hatcheries and used to have a marine fish, shellfish and prawn commercial hatcheries, yet there are many stumbling blocks for the much needed development of traditional aquaculture. Most of these blocks are of domestic nature such as local seeds supply, local feeds manufacturing and the social and environmental integration of aquaculture activities. On the regional level, there is a great need for technical cooperation through the establishment of strong working relationships with international partners. Both Mediterranean and Arabian cooperation should be encouraged and strengthened through the existing respective organizations and networks. This may allow undertaking aquaculture research and development within a jointly coordinated actions to ovoid duplication of efforts. The application of results of the cooperative applied research and technology development may contribute to the complementary development of aquaculture at a regional level. The Mediterranean and Arabian populations are growing at a rapid rate and the focal point of the Review of Moroccan Aquaculture 253

present challenge is to ensure sufficient protein supply to cope with the current and future population growth. Aquaculture could be play a major complementary role for fishing and agriculture as a food source.

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sud de l’atlantique marocain (21 N - 26°30’N). Journal de Recherche Océanographique, Vol (28), 1-13. Somoue, L., El Khiati,N., Ramdani, M., L. Hoai T., Ettahiri, O., Berraho , A.M. and Docchi, T., (2005). Abundance and structure of the Copepod communities along the Atlantic coast of south Morocco between 21°N and 26° 30’N. Journal Acta Adriatica, 46 (1), 63- 76. Talbaoui, E., Nhhala, H., Akharbach, H., Ben Bani, A., Ait Ali, A., Abrehouche, A., Sedki, S. Et Chebbaki, K.(2002). Projet de diversification : Reproduction en captivité, élevage larvaire et pregrossissement du pagre commun (Pagrus pagrus, linnaeus 1758). 2002. 36 p. Talbaoui, E., Chebbaki, K., Ben Bani, A., Sedki ,S. Akharbach, H., Nhhala , H., Ait Ali, A., Et Abrehouche, A.(2005). Étude expérimentale de l’effet de cinq aliments formules à partir d’ingrédients locaux, sur les performances de croissance et de conversion alimentaire chez le loup bar (Dicentrarchus labrax): étude du rapport protéine/énergie. 2005. 21p. Talbaoui, E.M.; Chebbak ,K.; Benbani, A.; Sedki, S., Akharbache, H.; Nhhala, H., Ait Ali A., Abrehouch ,A., Kheyyali, D. et Camara M.L.(2006a). Etude expérimentale de l’effet de cinq aliments formulés à partir d’ingrédients locaux, sur les performances de croissance et de conversion alimentaire chez le loup bar (Dicentrarchus labrax) - Etude du rapport Protéine/Energie. Actes et colloque du 2ème Congrès International de Biochimie. Agadir, 09-12 Mai 2006. Talbaoui,E.M., Nhhala, H., Benban,A., Ait Ali, A., Abrehouche, A., Akharbache, H., Chebbaki, K., Sedki, S.et Nagai, A. (2006). Reproduction en captivité et essais d’élevage larvaire et de prégrossissement du pagre commun (Pagrus pagrus, L.). Actes du 3ème Congrès Franco-tunisien de Zoologie. Tabarka (Tunisie), 3-7 novembre 2006b. Zidane, H.; Orbi, A., Mouradi, A., Zidane, F. et Blais J.F.(2008). Hydrological and edaphic structure of an oyster-farming site: Duna Blanca (Bay of Dakhla, south Morocco). Environmental Technology, 29, Issue 9 September 2008, 1031-1042.

Chapter 12

AQUACULTURE IN THE KINGDOM OF SAUDI ARABIA: GROWTH, PROSPECTS AND PROBLEMS

Feisal Bukhari∗ Consultant, Fisheries Research Centre, Ministry of Agriculture, Jeddah, Kingdom of Saudi Arabia

ABSTRACT

Saudi Arabia, an important country in the Middle East with over 2400 km of coastal length, has a major role to play in the seafood production and supply in the region. Presence of this aquaculture-potent country is increasingly felt with considerable and gradual increase in its fish production. Aquaculture sector contributes to about 10% of the average annual fish production (0.17 mmt) with sizeable contribution coming from tilapia, African catfish, common carp and giant freshwater prawn among the cultured freshwater species. Groupers, rabbit fish, breams, milkfish, mullets and the tiger shrimp contribute to the marine aquaculture production. The National Prawn Company (NPC) is a private venture success story of the region in the field of aquaculture. The company has established fairly high standards of productivity with quality output. King Abdul Aziz University has been one of the leading Universities that cater to the R andD needs of the aquaculture sector in the country. This chapter deals with all aspects of aquaculture in the country with a focus on possible prospects and problems.

INTRODUCTION

Saudi Arabia has a large geographical area of 2,150,000 square kilometers and covers about 80% of the Arabian Peninsula. It is located between 15° 20΄ to 32° 15΄ N latitude and 34° 30΄ to 52° 00΄ E longitude. The country has two coastlines of 1800 km and 600 km on the Red Sea and the Arabian Gulf respectively. The climate of Saudi Arabia is sub tropical to tropical (hot and dry). Annual aridity indices in the interior parts are over 90%. The rainfall is low and irregular. The annual

∗ E mail:[email protected] 258 Feisal Bukhari average rainfall ranges from 30-90 mm in the north-central areas to over 300 mm in the mouth plains of Hijaz and Asir. The Raba Al-Khali in the south-east has seen long spells of draughts of even 10 years. Water balance situation in less than 100 mm rainfall areas remains deficit all the year round where evaporation exceeds precipitation. Summer months are extremely hot and the air-temperatures cause excessive water losses from the soil and from the water surface. Seasonal and diurnal fluctuations in temperature are wide resulting in climatic extremes (Table 1). However, coastal areas, particularly along the Red Sea, have small seasonal variations in temperatures largely due to the stabilizing effect of warm maritime air masses. Much of the seasonal temperature variation is along the broad central axis extending from Qurrayat in the north to Sulayyil in the south. The winters in the north-eastern and central parts are cold and wind waves intermittently sweep down the region from December to February causing frost and below 0°C nocturnal conditions. The temperature regime in the open shallow water environments may become highly trying during winter for tropical aquaculture species. Saudi Arabia has three main types of water resources: non- renewable ground water, renewable ground surface water and desalinated water. About 88% of potable water requirement of Saudi Arabia is met by the coastal plains, particularly the southern part, the Tihama which receives 60% of the country's total rainfall. Rainfall in this region turns out to be a catchment for a series of dams and reservoirs such as Jizan, Najran and Abha. These reservoirs are rain-fed and provide an average supply of about 1.85 billion m³ of water, accounting for about 9% of total annual water consumption. Desalinated water production is about 2.87 Million m³ per day. Desalinized water is used for drinking. Despite harsh climate and limited water resources, Saudi Arabia has been among the world's fastest food producers and its agricultural share of total GDP and it is the sixth largest exporter of wheat and among the largest producers of dates. It has attained self sufficiency as well in other crops, eggs and dairy products. Outputs of vegetables and fruits have increased significantly over the last decades.

Table 1. Mean monthly air-temperature ºC of some major agriculture regions of Saudi Arabia

Riyadh Dhahran Hail Al-Qasseem Al-Kharj Tabuk Month 1 2 1 2 1 2 1 2 1 2 1 2 Jan. 8.5 20.4 10.7 20.7 3.6 16.5 12.4 18.2 5.9 21.5 2.8 16.9 Feb. 9.9 22.7 11.3 21.9 5.5 18.9 14.9 21.5 8.7 24.9 4.3 20.1 March 14.2 27.9 15.5 26.6 9.2 21.9 19.7 26.7 12.9 29.1 10.6 26.9 April 18.8 32.5 18.9 30.7 13.9 27.9 23.9 30.7 17.5 35.3 13.9 31.2 May 23.8 35.9 23.8 39.8 19.1 31.2 29.5 36.9 21.7 42.0 16.4 35.8 June 25.7 40.9 27.2 41.2 20.1 36.9 32.9 40.0 23.3 44.1 20.9 37.7 July 27.4 42.5 28.5 42.1 22.5 37.6 33.9 41.5 24.3 45.2 21.6 39.1 Aug. 26.6 42.2 27.8 41.6 21.9 37.5 33.6 41.1 24.8 45.0 21.3 39.1 Sep. 24.1 39.8 25.1 39.6 20.0 36.6 31.6 39.5 21.2 42.9 18.6 37.7 Oct. 19.4 34.6 21.4 32.5 13.7 28.8 25.6 34.3 16.6 36.9 13.6 30.7 Nov. 13.2 26.7 17.1 28.3 9.5 23.1 19.3 25.7 10.7 30.2 8.7 24.3 Dec. 10.9 22.5 12.7 23.1 5.1 16.8 13.7 20.5 7.9 24.4 4.6 18.9 Note: 1 = Mean Minimum. 2 = Mean Maximum.

Aquaculture in the Kingdom of Saudi Arabia 259

The consumption of fresh and frozen fish in Saudi Arabia during the year 2007 was 170,121 tons, of which 23,314 tons, 37,090 tons and 14,375 tons accounted from the Red Sea, the Arabian Gulf and aquaculture production respectively. The fish production increased from 54,680 tons in 2000 to 75,341 tons in 2007 (MOA) and has reached the level of maximum sustainable yield. The present population of Saudi Arabia is about 22 million and the annual per capita fish consumption is 10.4 kg (8.3 kg in 2000). Fish consumption in Saudi Arabia is showing a rising trend in view of the value of fish as a health food especially as a source of omega fatty acids; which have been found to reduce the risk of cardiovascular diseases. It has been recognized that the exploitation of fishery resources from the Red Sea and Arabian Gulf alone are not enough to meet the existing and future demand for fish in Saudi Arabia. Aquaculture, which has a close relation to agriculture and animal husbandry in concept and practice, can play an important role in augmenting the fish supply in Saudi Arabia.

PRESENT STATUS AND DEVELOPMENT OF AQUACULTURE

Aquaculture was initiated three decades ago. The Saudi Arabian Ministry of Agriculture (MOA) contracted the Wight Fish Authority (WFA) of the United Kingdom (UK) to carryout the Fisheries Research Activities along the costal lines of both Arabian Gulf and the Red Sea. The Region-wise production details of fish and shrimp in the country is depicted in table 2. Several reports on the potential of marine fish farming in Saudi Arabia have been produced (Howard, 1977 a and b Howard et al., 1977; Vine et al., 1979). Summary of these reports is presented in table 3.

Table 2. Regional Fish/Shrimp Farming Production in the Kingdom of Saudi Arabia for the year 2007

No. of Fish Production No. of Shrimp Production Region Farms (tons) Farms (tons) Fresh Waters 46 3,606 0 0 Riyadh 21 1,916 0 0 Qasim 6 963 0 0 Mecca 15 627 0 0 Eastern province 2 81 0 0 Jouf 1 0 0 0 Hail 1 19 0 0 Tabuk 1 0 0 0 Coastal Waters 5 306 4 14,527 Mecca 1 9 1 12,109 Aseer 1 0 1 1,400 Tabuk 1 297 0 0 Medina 0 0 0 0 Jizan 2 0 2 1,006 Eastern province 0 0 0 0 Total Production 51 3,912.759 4 14,527.564

260 Feisal Bukhari

Table 3. Production of Farmed Fish by Species in the Kingdom of Saudi Arabia for the Year 2007

Region Carps Mullet Caviar Tilapia Cat fish Grouper Grouper Sea bass Sea bass Sturgeon Sturgeon Salt water Rabbit fish Mecca 0 1 0 4,633 4,636 0 0.09 0 0 Tabuk 0 0 12 0 280 15 0 0 0 Jizan 0 0 0 0 1,006 0 0 0 0 Eastern province 0 0 0 0 0 0 0 1 50 Qasim 1 45 0 0 0 0 0 0 0 Total 1 46 12 4,633 5,922 15 0.09 1 50 Production Medina, Aseer, Riyadh, Hail and Jouf Regions: No production.

Suitable sites for marine farming were identified, environmental parameters (temperature and salinity) evaluated and some preliminary observations on growth and salinity tolerance of three cichlid species, Oreochromis aureus, O. spilurus and Tilapia zillii, imported from Kenya, were made (Peacock, 1979; Osborne 1979). Fish fingerlings of O. spilurus showed satisfactory growth when cultured in floating cages. Fish culture project of king Abdul Aziz University for Science and Technology also established a tilapia and common carp hatchery in Riyadh during 1980. Since then, a substantial number of fingerlings were produced for distribution to prospective fish farmers playing a catalyst role in the development of fresh water aquaculture in Saudi Arabia. In the 1980's a number of fish culture projects were started. Most of them succeeded. Some of them failed mainly due to the misconception of the investors who thought aquaculture to be an easy way to make money and also due to the lack of trained personnel. In most cases the investors of these farms have used their own land, farm facilities and other operational inputs. The main turn-on factors for aquaculture development were identified to be the following: Availability of Land: Saudi Arabia is a vast country and wide tracts of land are available along both the coasts for mariculture. Some of the land within the agriculture belt was already moderately invested for the construction of small concrete tanks. These types of fish farms were usually integrated with agriculture to maximize the utilization of fresh water resources. The Department of Lands (MOA) leases out coastal lands cheaply for long term investment. Climate: Despite extreme climatic conditions in Saudi Arabia, a number of tropical and sub-tropical aquaculture species were successfully cultured. In view of the limited fresh water resources, mariculture has proven to be the potential area of investment with a wide range of seaside sites including hypersaline lagoons available for this purpose. Quality of Water: The water quality of both groundwater and sea water is suitable for aquaculture and appears to be pollution free. Aquaculture in the Kingdom of Saudi Arabia 261

Easy Credit: Agriculture banks provided interest-free loans to the farmers mainly for the machinery purchase and for drilling wells. Such loans were sanctioned on a 10-year repayment basis. Cheap Energy: Aquaculture in Saudi Arabia ranges from semi-intensive to intensive and requires a considerable amount of energy for water pumps, aeration and other purposes which is made available at a low cost. Subsidized Fish Feed: Feed is subsidized by the Government of Saudi Arabia and has been made available to farmers at a reasonable price. Marketing: There is a good demand for fish by both the Saudi's and the expatriates and the produce is locally consumed. Fish marketing infrastructure is also excellent.

Freshwater Aquaculture

Tilapia Species and Production Freshwater aquaculture in Saudi Arabia is based mostly on tilapia. There are about 14 tilapia production farms, with a total production exceeding 1,300 tons annually. Production systems: The production systems range from simple technology of stagnant waters (50%) to more intensive aquaculture practices (38.9%) and open water systems (11.1%) (Al-Owafeir M., et al 2007). Most of production facilities consist of concrete and fiberglass tanks varying in size from 1 to 200m³. Small tanks are used for spawning and larval rearing whereas; the large tanks/ponds are devoted mainly for grow-out. Fingerlings (2-10 g) are transferred to the larger facilities (Siddiqui, A. and Al-Harbi, A. 1997) where they grow and the fish reaching a size of 200-300g are continuously harvested and marketed. Tilapia reproduction in grow-out culture facilities is not monitored or controlled. Aeration is provided through out the culture period. Production varies from 5 to 25 kg/m³ (Siddiqui et al 1989) with a fish stocking density varying between 30 and 60 fingerlings/m² and it takes about 8 months for the fish to attain a marketable size (Al-Owafeir M., et al 2007). Fish Feeds: Commercial sinking fish feed with 34% and 39% dietary protein at a subsidized price (SR 800-1,400/ton) is available from a local feed company (Grain Silos/Flour Mills Organization) as well as private fish feed mills. The feed is available in powder, crumble and pellet forms. Manual feeding is common and the feeding rates and frequency of feeding vary with the size of fish. The feed conversion ratio ranges between 2 and 2.5. Marketing: Farmed tilapia weighing over 200 g is well received by certain ethnic expatriate groups. Saudi populations prefer local fish spices. Fresh tilapia, direct from the farm, are preferred. Tilapia sale price ranges between 11 and14 SR/kg, there are no seasonal price fluctuations. The retail price ranges between 6 and 20 SR/kg.

Common Carp Common carp, Cyprinus carpio, was introduced in to Saudi Arabia in 1980 from Taiwan. It was grown to maturity and spawned in small concrete tanks by providing a layer of nylon netting at the bottom of the tank and floating nylon netting at the water surface. Mature females and males, with an average weight of 1.5 kg, were released in between the two nettings and allowed to spawn naturally during the night. 262 Feisal Bukhari

Table 4. Fresh water Tilapia Farms and Production in Saudi Arabia (2007)

Farm Location Production (tons) Al-Sheeb Riyadh 300 Al-Rajhi Qasim 180 Al-Balla Qasim 150 Al-Alshaikh Riyadh 150 Al-Habib Riyadh 150 Al-Saadi Riyadh 75 Al-Ahmadi Qasim 70 Al-Kabir Qasim 50 Al-Zahrani Mecca 48 Al-Awaibidi Mecca 35 Baghanim Mecca 32 Al-Jadani Mecca 30 Al-Amoudi Mecca 24 Al-Tamimi Eastern Province 20 Total 1,314

The spawned fish were removed in the morning and eggs attached to the nylon netting were hatched in the fiberglass tanks with running water and aeration. Newly hatched larvae were reared on freshly hatched Artemia nauplii and rotifers for 4 weeks. Powdered artificial fish feed was given thereafter. Carp fingerlings (approx 2g) were stoked and reared in large concrete tanks. Fingerlings grown in this manner are supplied to fish farmers. However, carp is not commercially cultured in Saudi Arabia as it has poor market demand.

African Catfish The African catfish Clarias gariepinus, was introduced in 1986 from Egypt. Successful spawning of the catfish was achieved through induced breeding by giving an injection of carp pituitary and HCG. Semi-natural spawning was done by keeping one female and a male in fiberglass tank or by stripping the eggs from a female and squeezing the milt from the male. The eggs were hatched in a fiberglass tank in 24-36 hours. Larvae were normally reared on Artemia nauplii for the first week, thereafter gradually replaced by artificial fish feed (Siddiqui et al. 1992, 1993). African Catfish can withstand higher densities than tilapia under similar conditions, needs less water and can survive at very low dissolved oxygen levels. The potential of aquaculture of this species is good. However, the fish is yet to find way into the commercial aquaculture.

Freshwater Prawn Giant fresh water prawn, Macrobrachium rosenbergii, postlarvae and adults were imported from Taiwan during the fag end of 1990. Berried females were used for hatching and larval rearing from April 1991 onwards. Potentials of fresh water prawn monoculture, its Polyculture with tilapia and common carp have been investigated (Siddiqui and Al-Hinty, 1991). Natural live food production through the application of organic and inorganic fertilizers and the supplemental feeding has been practiced. Result's revealed that prawn monoculture is not profitable in comparison to tilapia aquaculture. However, it has great Aquaculture in the Kingdom of Saudi Arabia 263

aquaculture value in polyculture both in concrete tanks and earthen ponds (Siddiqui and Al- Hinty, 1991 and 1992).

Mariculture Saudi Arabia is rich in marine resources. In 1982 the Fish Farming Center (FFC) was established under an agreement between the Food and Agriculture Organization of the United Nations (FAO) and the Kingdom of Saudi Arabia (KSA), represented by the Ministry of Agriculture. FFC specializes in the development and application of aquaculture technology appropriate for the kingdom. Research and development activities on selected local species of fish and shrimp at FFC provides much needed information for successful aquaculture in KSA. There are 22 species of groupers and many other local marine fishes in the Red Sea. Studies are being carried out to choose and determine suitable marine species and to develop aquaculture techniques applicable to local conditions. In addition to the economic importance, some of the criteria for species selection are the attainment of maturity in confinement; readily spawn under captive conditions, high larval and fry survival and fast growth rates. Six local marine fishes studied include five species of groupers (hamoors), viz., Epinephelus malabaricus, E. fucoguttatus, E. polyphekadion, Plectropomus pessuliferus (taradi) and P. areolatus (najil). Groupers are high-priced and preferred in the Saudi market. Studies on the higher-priced Plectropomus sp. are in the early stages. The groupers have been naturally spawned under captive conditions without much difficulty at the FFC through proper maintenance and conditioning. Grow out to marketable sizes (> 500g) has also been shown to be economically feasible.

Rabbitfish Rabbitfish (sigan or saffy; Siganus rivulatus) is another important fish species which also has a high market demand. At the FFC, studies showed that S. rivulatus can be spawned naturally and artificially (Lchatowich et al 1984a), without the hormonal induction. High larval mortality however, is a major problem that needs to be addressed. The life cycle of S. rivulatus was completed and the seed became available for culture. This obliterated the need to collect juveniles from the Red Sea. The Rabbitfish fingerlings can reach marketable size in 6 months when reared at different (low and high) stocking densities in cages installed in the Red Sea (Lchatowich et al 1984b and Bukhari 2005). FFC also carried out fish pen-polyculture study with milkfish (Chanos chanos), mullet (Mugil cephalus) and tilapia (Oreochromis spilurus). Results were not very promising. Apart from poor survival there were difficulties associated with the harvesting of milkfish and mullet. However, tilapia showed encouraging results. Research priorities were fixed to investigate into aspects of potential alternate species for polyculture (Bukhari et al. 1986).

Table 5. Growth, survival and production of rabbit fish Siganus rivulatus in sea cages at different stocking densities

Stocking density Mean initial Mean final wt. Survival Production m −² wt. (g fish) (g fish) (%) (kg m −³) 80 2.0 108.0 96. 5 8.13 100 2.0 101.0 95.6 9.44 120 2.0 91.9 94.7 10.20 264 Feisal Bukhari

Tilapia Tilapia is known to have high resistance to adverse environmental conditions, including extremes of temperature and salinity. Tilapia culture is widely practiced throughout the kingdom spreading even to the coastal areas. FFC succeeded in developing and demonstrating aquaculture of O. spilurus in hyper-saline seawaters conditions along the kingdom's Red Sea coast. Various studies have been carried out on O. spilurus at the FFC during mid eighties of the last century. Results showed that the sex ratio of 1:4 gave more consistent fry production while, a 1:3 ratio also fared well. A six-week nursery trial revealed that the optimum fry survival and growth was the best at a stocking density of 13 per liter. A production trial in floating sea cages showed that a high density of 225 fish/m² yields the best production thus, recommended higher stocking densities for enhancing fish production (FFC 1987). Tilapia aquaculture studies were carried out in a concrete tank system, the "Baobab Tilapia Culture Facility" – a trademark of technique developed by Baobab Farm Ltd., Kenya. (FFC 1983). "Baobab Technique" is an intensive tank aquaculture technique for tilapia species which uses a hatchery specifically designed for mouth brooding tilapia species. The nursery and grow out systems were considered to be the best for tilapia production. Tilapia in the Baobab FFC showed very good growth (220-250g) and food conversion efficiency (1:1-1.5) after 9 months of tank culture with a production of 40 kg m−³ (FFC Operational Manual for Baobab systems 1991). Tilapia life cycle is completed in the closed, full strength saline seawater. O. spilurus brood stock and larvae were developed and established that could produce and grow in the Baobab salt water tanks, therefore fry acclimation in the arena was not necessarily any more.

Black Trigger Prawn The Fish Farming Center had started studies in the late 80's on tiger prawn by importing Penaeus monodon post larvae from Malaysia to test its culture viability in the kingdom. Since prawn is a brackish-water species and the average salinity of Red Sea is 40 ppt, acclimation to the high salinity of the full strength seawater is essential before it is reared in culture facilities. It was observed that prawn growth and survival were slow and low conservatively due to the high salinity of the Red Sea despite the lengthy periods of nursery acclimation. Also, it was observed that the tanks and ponds gave higher growth and survival for prawn (P. monodon) than in cages and pens (Bukhari et al. 1989) despite better water quality in the sea- based facilities compared to the land-based facilities.A poly-culture study involving P. monodon, rabbitfish (S. rivulatus) and mullet (Liza sp.) in tanks had shown a positive influence on prawn growth and survival rates. The addition of fish to shrimp tanks improved the water quality. It was observed that the presence of herbivorous fish stabilizes water quality and increases yields (Bukhari 2002). P. monodon had generally low survival (50%) and poor growth (24-27 g) in salt water ponds at FFC compared to a higher survival (70%) and growth (35-40 g) in south east Asian environments (Bukhari et al. 1989).

White Indian Shrimp Difficulty in the attainment of maturity of P. monodon in captivity and other species- related limitations made the FFC to look for a local shrimp spices to study as a culture model that might be advisable for aquaculture by the private sector. Aquaculture in the Kingdom of Saudi Arabia 265

The Indian White Shrimp Fenneropenaeus indicus, abundant in shallow lagoons of the southern part of the Red Sea coast with a depth of 1-2 m and with a peak of occurrence during April - November (Badawi and Cas, 1989) was found to be a potential alternative. Some juveniles were collected, grown and spawned in captivity for culture at FFC (Bukhari et al 1990). Larvae of F. indicus are easily obtained from ablated and un-ablated females (Bukhari et al 1991b). The earliest nursery stage for transfer to growout ponds at 43 ppt is PL25 (Bukhari et al 1997a). From hemolymph osmolality experiments it appears that the Red Sea strain of F. indicus is better acclimated to tolerate high salinities showing higher survival rates at salinities in excess of 35‰ (Bukhari et al 1997a) when compared to its Indian Ocean counter part. Microencapsulated artificial feeds to replace live feeds in F. indicus larval culture have been investigated. Results revealed that a 50% replacement is possible. It has been possible also to replace expensive local protein sources with cheaper local protein and to produce diets for the price of the cheapest imported feed (Bukhari et al 1997b). Density trials from 20- 80/m² for F. indicus in ponds at FFC resulted two production cycles of 180 days each per year (final harvest weight 15 to 28g), survival rate of 55-93%, feed conversion ratio (FCR) of 2-3 and a production ranging from 6 to 13 tons/ha/yr (Bukhari et al 1992 and 1993). Research conducted on shrimp species (Tiger prawn, Penaeus monodon and Indian white shrimp, F. indicus) has contributed greatly to the development of the commercial shrimp industry in the kingdom. FFC developed and demonstrated successful culture of the Indian white shrimp under hyper-saline conditions of the Red Sea. Production of P. indicus has been highly successful and present production at the FFC is from the 17th generation of domesticated broodstock. Another production trial was also carried out at the eastern side of the kingdom investigating on the influence of water exchange in tanks on P. monodon and F. indicus. Results indicated higher survival rates of 77.95% and 83.2% with 600 and 1200% water exchange, respectively for the tiger shrimp while, it was 69.8% and 77.1%, respectively for the white shrimp (Bukhari 1998). A comparative study was also conducted on the Saudi Arabian Gulf coast using two production facilities viz., rectangular cemented raceway tanks and circular earthen ponds with the tiger shrimp (P. monodon) and the white shrimp (F. indicus). Results revealed the possibility of obtaining two tiger shrimp crops of 4.5 tons/ha compared to one crop of 4.3 tons/ha in raceways. Estimated average pond production of F. indicus (April-Nov.) was 5.8 ton/hec/crop compared to 3.9 ton/ha in raceways (Bukhari 2000) (table 6).

Table 6. Average initial weight (g), final weight (g), survival rate (%) and production (tons/ha/yr) for the Indian white shrimp, F. indicus in earthen ponds at the Red Sea Coast of Saudi Arabia

Stocking Initial Weight Final Weight Survival rate Production density m−² (g) (g) (%) (tons/hec./yr.) 20-80 0.94-1.16 20-25 60-90 7-10

Grouper A study to investigate high density in grow-out culture facilities of the (Hamoor) Epinephelus polyphekadion; revealed the possibility of reaching marketable size of (500 g) 266 Feisal Bukhari during 38-44 weeks when 16 grammars fingerlings are used at Stocking density of 100 m −³ (FFC 2007). Continuous efforts at the Fish Farming Center's hatchery are in progress to improve the larval rearing and survival rates of P. areolatus and P. pessuliferus. Considerable success has been achieved with a 94% fertilization and hatching rate exceeding 68%.

Table 7. Average Weight (g) and Length (cm) for Tiger prawn, P. monodon and Indian White Shrimp, F. indicus in Rectangular Tanks and Earthen Ponds at the Arabian Gulf Coast of Saudi Arabia

Rectangular tanks Earthen ponds Weight Length Survival Weight Length Survival (g) (cm) (%) (g) (cm) (%) Tiger prawn 35.7 15.9 65.5 62.4 19.5 18.0 White shrimp 17.0 13.6 54.6 23.1 15.3 62.5

PRESENT AND FUTURE AQUACULTURE PROJECTS

Highlights of the kingdom's aquaculture situation are as follows:

• Freshwater fish farms (mostly tilapia) are scattered in the central, western and eastern inland areas, generally linked with agricultural farms; 2,900 tons of Oreochromis spilurus were produced by 40 farms. • Shrimp culture is considered as the main aquaculture activity, concentrated in the southern and south west regions were stable climate in common. More than 11,000 tons of shrimp was produced by 3 projects with a production area of 1,880 hectares. These projects are expected to be expanded to 7,600 hectares and produce about 40,000 tons. It is also expected that about 10,000 tons will be produced from 3 new projects under construction. Also, 70 shrimp farming projects are in the pipeline. • On going Auxiliary Activities includes 4 fish feed plants, 2 of which are expected to export about 10% of high-quality feed to neighboring countries. • A leading company in the south has established a hands-on training institute in aquaculture, equipped with various diagnostic laboratories and a processing plant that has a production capacity of more than 80 tons/day. • Another processing plant is operating in the east. Another company in the east has an Inspection, Diagnosis, Analyses, and Consultation facilities.

The MOA is working on the establishment of the legal framework to regulate the aquaculture industry. The kingdom is working for establishment of aquaculture projects that implement environment-friendly, responsible and sustainable culture systems. One of the objectives is to improve production of safe products that are suitable to global market requirements. The Quality Management Systems (QMS) is followed by leading farms. They follow regulations and the FAO Code of Conduct, practice GAP/GMP and SOP (documentation at various production stages), HACCP/SQF (implementation and recommendation of Aquaculture in the Kingdom of Saudi Arabia 267

certification by the SGS for hatchery, farms, feed mill and processing plant), obtained ISO Certification (ISO 9000-2001; working to obtain ISO 14000; ISO certification allowed the export of shrimp to Japan, USA an EU), and have QAI Specialized Laboratory (analyzes and monitors the production processes and the environment). The kingdom will benefit considerably by establishing the aquaculture industry. For instance:

− It is able to effectively utilize its natural resources that would have otherwise remained idle, particularly the large tracts of coastal flats; − It generates secondary business or income and job opportunities for local people. − It promotes socio-economic development of coastal areas that encourages local and other people to stay and populate, which inturn promotes border security. − It reduces the gap between local production and consumption. − It improves the country's trade balance through aquaculture products’ exports. − It enhances scientific awareness through aquaculture technology transfer and adoption.

COMMERCIAL MARINE FARMS IN SAUDI ARABIA

National Prawn Company (NPC)

National Prawn Company (NPC) is one of the world’s largest fully integrated desert costal aquaculture project located south of Jeddah, Saudi Arabia. It was established after over three decades of dedicated RandD at a cost of more than US$350 million to catch-up with the booming global seafood market and this company marked the beginning of coastal aquaculture in Saudi Arabia.

The technology development and adoption includes selection of site and species, engineering and hydro dynamic designing, preparation plans and execution of earth work to facilitate mechanical harvesting, formulation of diets for high saline and winter aquaculture, etc. that were achieved by various level of RandD programmes. All the efforts were aimed at an annual production of 10,000 to 15,000 tons. The company poised to produce over 30,000 268 Feisal Bukhari tons annually from 16 more farms after the completion of its ongoing second phase development. The completed Phase – I Project is fully integrated with its own domestication units, 2 Naupli production units, 3 Larval rearing units, 11 farms with the production capacity of 12,500 MT/yr, 120 MT Production capacity of state of the art modern equipped automated Processing plant by producing various product mixes, 50000 MT/yr production feed mill, 21.4 MW Power Plant, Desalination RO Plant with a production of 1100 m3 per day and fully equipped supporting units.

The shrimp farm stocking material is obtained from locally domesticated native brood stock, reared under high bio-security regulations. Grow out shrimps are fed by in-house manufactured high saline feed through mechanical feeding and marketable shrimp is mechanically harvested, marketed or processed immediately after the harvest based on market requirement.

It has its own well equipped Central Laboratory and an organized QA system in place with regularly updated measures of standards and Bio-Security controls. An established R and D department with a team of qualified researchers works on domestication, feed formulation, Bio-saline agriculture project and other projects.

Aquaculture in the Kingdom of Saudi Arabia 269

The Intake Pump Station has been designed to supply water at a 90 m3/sec rate through a man made intake canal of 35 km. On the other hand the Discharge Pump Station has been designed to push a flow of 90 m3/sec from a drainage canal of 38 km. Each farm has been designed to release the drainage water through its own Effluent Treatment Plant (ETP) with a sedimentation basin in an effort to reduce the farm effluents and to protect the aquatic ecosystem.

BaaN ERP is being implemented in NPC and covers it’s Financial and Management functions, Warehouse and Distribution, Purchasing and Sales, Production and Processing. By end on providing the Business Performance Indicators through the Executive Information Systems (EIS) to enable the top management for critical decision making. All MPC production units of Hatcheries, Grow out farms, Processing Plants and Feed Mills are covered 270 Feisal Bukhari under the certification of ISO 14001:2004 and HACCP Standards. Besides Processing Plant facilities are complaint with EU standard and certified for the same.

The Company presently exports around 10,000 tones of shrimp in different size groups to 30 countries based on their requirements by every year. Besides the frozen products, fresh shrimps are exported as well to certain countries including Turkey and Italy etc. NPC has recently commenced the construction of the second phase of the project’s with 16 farms with the production capacity of 17500 MT/Yr, which will significantly increase its annual production to more than 30,000 tones of premium quality shrimp. This is predicted to make NPC the single largest supplier of shrimp in the world. The multi million dollar venture is also envisioned to be a global leader in environmentally friendly aquaculture shrimp production, boasting cutting-edge farming technologies and techniques as well as stringent quality standards. Besides shrimps, fish culture projects and Marine Agriculture Project by producing mass commercial phytoplankton facilities are on the developmental stages and scheduled to take off by 2008. Along that Bio-Technology Project of Chitin and Glucosamine production from the shrimp head meal is in pipe line. NPCs workforce comprises of over 2000 employees from nearly 27 countries, all of them working wholeheartedly towards taking the company to greater heights. Some of these employees are specialists in their respective fields.

Aquaculture in the Kingdom of Saudi Arabia 271

Yet NPC understands the need to keep them updated on their knowledge and skills and hence arranges for internal and external courses under the auspices of its in house Training Center which also contributes a lot to the Saudization efforts of the government, by collaborating with King Abdul Azaiz University. Fresh, out-of-educational institutions, Saudi nationals are provided with on-the-job training and courses in English, so that they are ready to take up any job which suit their careers. NPC provides its employees with furnished accommodation, recreation facilities like indoor and outdoor sports, super market, laundry, centralized dining halls, Clinic with 24 hours medical care, cultural centre, library, school facility, and a central mosque at the Township accommodation area. Over a 60 km stretch of the constructed 160 km of road is asphalted.

Saudi Fisheries Co. (SFC) Shrimp Farm

SFC started investing in Aquaculture from 1992 and implemented its project in 1995 with a shrimp farm located on the southern Red Sea coast at Al-Hureida covering a farm area of 10 sq. km. housing 108 circular rearing ponds of 1 hectare each.

The Shrimp Farm of Saudi Fisheries Company.

Al-Faris Farm for Sturgeon Fish and Caviar Production

Al-Faris farm (Caviar Court) produces high-quality "Osietra Malossol" grade caviar of the sturgeon species Acipenser baerii and their crossbreeds.

272 Feisal Bukhari

Al-Faris farm for sturgeon fish and caviar production.

Sturgeon grows in facilities designed and built in accordance with the closed circuit recirculation technology. Self-sufficient indoor units are equipped with sophisticated water treatment hardware. The water treatment includes mechanical separation, biological filtration, aeration and disinfection. This approach guarantees complete isolation from harmful environmental factors such as pollution and infections.

Water treatment plant of the Al-Faris Farm. Aquaculture in the Kingdom of Saudi Arabia 273

CONCLUSION

The kingdom still has tremendous potential for coastal as well as inland aquaculture activities. Survey conducted by the country's Department of Aquaculture has recognized the availability of many suitable coastal areas for marine farming operations. The kingdom's natural resources (highly suitable environment with unpolluted water, favorable climate, large areas of suitable land, no mangrove destruction) and well-established infrastructure (good road networks, airports and seaports), availability of established technology and the supportive Government policies (MOA and other related government agencies; e.g; long term lease of land at work permits) are responsible for the success of aquaculture in the kingdom. Saudi Arabia has plans to pursue aquaculture of other local species of marine fish, algae, seaweeds and mollusks. At present, the kingdom is in the process of establishing the legal framework to regulate the aquaculture industry, taking in to consideration the sustainability of aquaculture projects that are environment-friendly and socio-economic and technical viability.

REFERENCES

Al-Owafeir, M., Tharwat, A. and Belal, I. E. (2007). Tilapia Aquaculture in the Kingdom of Saudi Arabia: Field Study. Saudi Journal of Biological Sciences. 14 (1), 25-34. Bukhari, F.A., 2002. Cultured Tiger Prawn Penaeus monodon through polyculture with Rabbitfish Siganus rivulatus or Mullet liza sp. in Red Sea water. Egypt. J. of Appl. Sci., 17 (9), 31-38. Bukhari, F.A., (2000). Comparison Production of tiger shrimp Penaeus monodon and White shrimp P. indicus in cemented raceway tanks and earthen ponds, at the Arabian Gulf. Arab Gulf J. Scient. Res., 18 (1), 54-63. Bukhari, F.A., (1998). The influence of Water Exchange Rate on the Production of Penaeus monodon (Fabricius) and P. indicus (Milne Edards) in Saudi Arabia. Arab Gulf J. Scient. Res., 16 Pp. 415-430. Bukhari, F.A., D.A., Jones and A.J. Salama (1997). Development of nursery feeds for White shrimp Penaeus indicus cultured in Saudi Arabia. Journal of King Abdul Aziz University Marine Sciences, 9, 91-99. Bukhari, F.A., D.A., Jones and A.J. Salama (1997). Optimal salinities for the culture of White shrimp Penaeus indicus from the Red Sea. Journal of King Abdul Aziz University Marine Sciences, 8, 137-147. Bukhari, F.A., D.A., Jones and A.J. Salama. (1993). The potential for the culture of White shrimp Penaeus indicus in high saline ponds on the Saudi Arabian coast of the Red Sea. European Aquaculture Soc. Spec. Pub. No.19, 117. Bukhari, F.A., S., Mannewwong, S., Al-Thobaiti, M.Y., Seth and M., Carlos.(1991). Spawning, hatching and larval rearing of the White shrimp Penaeus indicus at the Fish Farming Center, Saudi Arabian Agriculture Magazine 4th ed. 22, 39-49. Bukhari, F.A., A., Al-Suhame and M., Carlos. 1991. Growth and survival of Penaeus indicus in different salinities. Saudi Arabian Agriculture Magazine 1st ed. 21, 23-27. 274 Feisal Bukhari

Bukhari, F.A., (1981). Aquaculture activities at the fisheries department. the Saudi Arabian Agriculture Magazine 4th ed. 12, 20-23. Howad, K., (1977). A preliminary report on the prospects for marine fish farming on the Gulf Cost of Saudi Arabia. MAW and WFA Rep. No. 11, 9 p. Howard K., M. Amousi and P. Vine (1977). Prospects of marine farming in Saidi Arabia. An examination of the hydrographic parameters in summer time to assess the suitablility of Rabigh coast for marine farming. MAW and WFA Rep. No. 20, 14 p. Osborne, T.S., (1979). Some aspects of the salinity tolerance and subsequent growth of three tilapia species, Sarotherodon aureus, S. spilurus and Tilapia zillii. MAW and WFA Rep. No. 46, 16 p. P. White and F.A. Bukhari. (1990). Survey of potential aquaculture sites in the Jazan area. Tech. Rep. Fish Farming Center, Jeddah, Saudi Arabia. Peacock, N. A., (1979). The suitability of tilapia species for marine aquaculture. MAW and WFA Rep. No. 48, 12 p. Siddiqui, A. and Al-Harbi, A. (1997). Effects of sex ratio stocking density and age of hybrid tilapia on seed production in concrete tanks in Saudi Arabia. Aquaculture International, 5, 207-216. Siddiqui, A. Q., A. R. Al Najada and H. M. Al Hinty, (1993). Growth, survival and production of hybrid tilapia (Oreochromus niloticus × O. aureus), common carp (Cyprinus carpio) and African catfish, Clarias gariepinus (Burchell 1822) in mono-and polyculture systems during winter in the central region of Saudi Arabia. Prog. Fish-Cult. 55, 57-59. Siddiqui, A. Q., and H. M. Al Hinty, (1992). Feasibility study of freshwater prawn, Macobrachium rosenbergii, culture in Saudi Arabia. (KACST Project No. AR-1164) Third Progress Report, 55p. Siddiqui, A. Q., and H. M. Al Hinty, (1991). Feasibility study of freshwater prawn, Macobrachium rosenbergii, culture in Saudi Arabia. (KACST Project No. AR-1164) Second Progress Report, 22p. Siddiqui A., Howlader, M. and Adam A., (1989). Culture of Nile tilapia Oreochromis niloticus (L) at three stocking densities in outdoor concrete tanks using drainage water. Aquacult. Fish. Manage., 20, 49-57. Vine, P. N., N. Peacock, N. A. and T. S. Osborne, (1979). Studies of the aquaculture potential of Saudi Arabia MAW and WFA Rep. No. 29, 17 p.

Chapter 13

AQUACULTURE IN TURKEY – STATUS AND NEEDS

Hayri Deniz∗ Aquaculture Department, General Directorate of Agricultural Production and Development, Ministry of Agriculture and Rural Affairs, Ankara, Turkey

ABSTRACT

The geographic and climatic variations as well as the abundance of marine and inland waters offer a wide variety of production types on different species in aquaculture in Turkey and because of this reason Turkish aquaculture is expanding very rapidly. Aquaculture, being a very young sector, represents 18% (139.873 mt) of total fish production in Turkey. Due to developments in the sector, Turkey soon became the third fastest growing aquaculture sector in the world. At the same time, Turkey is the 5th largest aquaculture producer in Europe and the 3rd largest (when shellfish production is excluded). It is also the 2nd largest producer in Europe of sea-bass, sea-bream and rainbow trout. Thus, Aquaculture is playing an increasingly important role in the Turkish economy, as fishery products are the only products of animal origin that can be exported to the EU. Turkey has excellent growing conditions and has the potential to expand production substantially. However, the current distribution of sea farms, most of them located in the Aegean region in enclosed bays or coastal waters where they compete with other activities is considered a constraint and the main problem for the future expansion of the sector. Additionally, there are several other factors affecting the development of the aquaculture industry, such as the complex and lengthy licensing procedures, short site leasing period, the changing aquaculture regulation framework in Turkey, the lack of a long term planning policy, the adaptation to the EU framework on environmental issues, the dependency on carnivorous species, the role of the media in the consumer perception of aquaculture and the lack of reliable data among others. However, the increasing fish consumption particularly in the domestic market is the main driving force for the development of aquaculture. The market potential for aquaculture products makes this sector one of the most attractive sectors for investment. There is a great possibility of

∗ E-mail: [email protected] & [email protected]

276 Hayri Deniz

cooperation with other Mediterranean countries in various fields such as studies in technological innovation, new potential species, economic performance of the industry and prior to setting up producers organizations, technical assistance to improve poor growth performance of some species, or the design, supply and installation of offshore fish farms; production management for small fish farms, offshore facilities and pilot plants for new species, insurance issues, market studies, feasibility plans for new zones and training on marketing, promotion and quality control.

INTRODUCTION

Turkey is a peninsula with wide selection of lakes, dam lakes, ponds, reservoirs, rivers and springs. This diversity in water masses presents a major potential for aquaculture (Figure 1 and 2). With 8,333 km of coastal line and 177,714 km of rivers, the marine and inland water sources suitable for aquaculture are approximately 26 million ha (Table 1 and 2). It is known that there are 247 species in the Black Sea, 200 in the Sea of Marmara, 300 in the Aegean Sea and 500 in the Mediterranean. However, only 9 species of commercial interest represent almost the 60% of the total Turkish production (DENIZ, 2001). Turkey’s inland water resources are unevenly distributed throughout the country. The mean annual surface runoff of Turkey’s 26 river basins is 186 billion m3, of which half is considered technically and economically exploitable. Turkey produces approximately 0.6% of the total world fishery production. Out of 225 countries, Turkey is ranked 31st in marine fisheries and 30th in aquaculture production.

Table 1. Sea Resources in Turkey (Source: MARA)

Coastlines Surface Area Marine Resources (km) (ha) Mediterranean, Aegean Sea, Marmara Sea, and Black Sea 7,144 23,475,000

Istanbul and Dardanelles 1,189 1,133,200

Total 8,333 24,607,200

Table 2. Freshwater Resources in Turkey (Source: MARA)

Freshwater Resources No of Resources Surface Area (ha) Length (km)

Natural Lakes 200 900,118 - Dam Lakes 159 342,377 - Ponds 750 15,500 -

Rivers 33 - 177,714

Total 1,142 1,261,995 177,714 Aquaculture in Turkey 277

Figure 1. Turkey view from the Space (Source: Own elaboration).

Figure 2. Inland water basins in Turkey (Source: MARA).

Official figures indicate that total fishery production in 2007 was 772,323 mt (Table 3, 4, and 5), comprising marine fisheries 76%, aquaculture 18%, and inland fisheries 6% (DENIZ and KARASU BENLI, 2008). Contribution of aquaculture was 18% as a volume in total fisheries production, although, 39% as a value in 2007 (Fig. 3 and 4).

Table 3. Fisheries production in mt in Turkey during 2003 – 2007. (Source: TURKSTAT)

Source 2003 2004 2005 2006 2007 Marine Fishery 463,074 504,987 380,381 488,966 589,129 Inland fishery 44,698 45,585 46,115 44,082 43,321 Aquaculture 79,943 94,010 118,277 128,943 139,873 Total 587,715 644,582 544,773 661,911 772,323 278 Hayri Deniz

Table 4. Landings of key commercial species in mt during 2003 – 2007. (Source: TURKSTAT)

Species/year 2003 2004 2005 2006 2007 Anchovy 295,000 340,000 138,569 270,000 385,000 Horse Mackerel 28,000 27,405 13,540 14,117 22,991 Pilchard 12,000 12,883 20,656 15,586 20,941 Atlantic Bonito 6,000 5,701 70,797 29,690 5,965 Whiting 8,000 8,205 8,309 9,112 12,940 Grey mullet 11,000 12,424 10,560 8,915 8,291 Blue fish 22,000 19,901 18,357 8,399 6,858 European hake 7,500 4,380 4,100 3,460 3,337 Total 463,074 504,897 380,381 488,966 589,129

Turkish aquaculture which started with one farm in 1971 has rapidly developed into 1,715 farms in 2008 with governmental support and technical developments. Currently, there are 1,365 inland fish farms with 88,520 mt capacity and 350 marine farms with 110,840 mt capacity (Table 6). The Euphrates and the Tigris river systems which are within the GAP Region consist of 2,235 km of rivers, 6,481 hectares of natural lakes, small lakes and approximately 129,987 ha of dam lakes, the construction of which has been completed by DSI and opened for operation, are suitable for aquaculture.

Table 5. Fisheries production in Turkey in the past decade (mt) (Source: MARA, 2008)

Total Total Fisheries % of Total Fisheries Year Inland Marine Aquaculture Production Production 1998 33,290 23,410 56,700 543,900 10.42 1999 37,770 25,230 63,000 636,824 9.89 2000 43,385 35,646 79,031 582,376 13.57 2001 37,514 29,730 67,244 594,977 11.30 2002 34,297 26,868 61,165 627,847 9.74 2003 40,217 39,726 79,943 587,715 13.60 2004 44,115 49,895 94,010 644,492 14.59 2005 48,604 69,673 118,277 544,773 21.71 2006 56,694 72.249 128.943 661.991 19.47 2007 59,033 80,840 139,873 772,323 18.11

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Figure 3. Contribution of Turkish fisheries production in 2007 (volume, mt) (Source: TURKSTAT).

Figure 4. Contribution of Turkish fisheries production in 2007 (value, million €) (Source: TURKSTAT).

There is increasing need for the development of aquaculture as natural resources. Several natural water resources make Turkey an ideal country for aquaculture development (GOZGOZOGLU, 2002). Turkey has a great potential for aquaculture and fisheries. A wide diversity of aquatic species can be farmed in fresh, brackish or salt water using a variety of production systems. Aquaculture in Turkey is a relatively young industry. It started with rainbow trout culture in the early 1970s and little happened in terms of sea farming until 1985 when sea bream and sea bass culture started in the Aegean Sea. Today both freshwater and sea farming play an increasingly important role in the production of fisheries products. In 2000 its share of total fisheries production was around 14% by volume and 28% by value. In 2007, aquaculture was contributing around 18% by volume and 39% by value.

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Table 6. Number of farms by species and sub-sector in 2008. (Source: MARA-DGAPD Aquaculture Department)

Species No. of farms Total capacity (mt/year) Inland Trout 1,342 85,797 Common carp 42 2,045 Spirulina 5 395 Other 9 674 Sub-total 1,398 88,520 Marine Sea bass, sea bream 305 79,694 Trout 7 7,044 Trout + sea bass 11 5,427 Sea bream + sea bass + new 11 8,399 species Blue fin tuna 9 8,140 Mussel 3 1,625 Other 4 1,185 Sub-total 350 110,840 Total 1748 199,360

The main developments took place during the 1990s with the rapid increase in sea bass and sea bream production, the development of rainbow trout, Atlantic Salmon and sea bass farming in the Black Sea, kuruma shrimp on the Mediterranean coast, mussel in the northern Aegean and Sea of Marmara, and more recently the development of turbot culture in the Black Sea (Figures 5 and 6). The sector has developed to such an extent that Turkey is currently the third largest finfish aquaculture producer in the World and the second largest producer of both sea bass and sea bream and of rainbow trout. Aquaculture production declined during the 2000-2002 because of economical crises, after then was increased ordinarily up to now. Before 2003, marine aquaculture production was less than the inland aquaculture production. After 2003, growth rate of mariculture operations was superior to that of inland aquaculture (Figure 7). Aquaculture is an important economic activity in the coastal and rural areas of many countries. It offers opportunities to alleviate poverty, creates employment, helps community development, reduces overexploitation of natural aquatic resources, and contributes to enhancing food security. For example it is estimated that the aquaculture sector in Turkey provides employment for around 25,000 people. Due to the increasing worldwide demand for aquatic products, aquaculture is one of the most important and fastest growing sectors, not only within fisheries and but also within the food production sector.

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Figure 5. Contribution of aquaculture production by regions (volume, mt) (Source: TURKSTAT)

Figure 6. Contribution of regions in Turkish aquaculture by value (million €) (Source: TURKSTAT).

Turkey’s population is increasing at a rate of 1.5% per annum, and per capita income is also increasing in parallel with the economic development and attempts at integration with the EU. Current per capita fish consumption is very low compared to many European countries, but it is expected that all these development will lead to increases in domestic fish consumption. In fact there are some indicators that this is happening already. On the other hand, wild fish stocks are already under pressure from over-fishing, environmental degradation and pollution. Annual fish consumption per capita in the world is about 16 kg. However, the fish consumption in Turkey is around 8 kg. As the annual per capital fish consumption of EU countries is 25 kg, the consumption in Turkey needs to be doubled to reach world average and tripled to reach EU consumption level (DENIZ, 2008). Being the only animal product exported into EU countries in Turkey, the majority of the fish production 282 Hayri Deniz consists of sea bass and sea bream raised in marine cages. Turkey, with a capacity of 25% of the EU sea bass market, is the third fastest growing country in the world in aquaculture.

Figure 7. Growth trends of total aquaculture, mariculture and inland aquaculture in 2000-2007 (mt) (Source: TURKSTAT).

AQUACULTURE IN TURKEY

It is well known that aquaculture is one of the fastest growing food production activities in the world, a trend that is certainly true in Turkey. Aquaculture in Turkey has grown considerably over the past 10 years to keep pace with consumer demand for fresh, high quality fish. Demand for seafood in domestic market alone is expected to increase considering low per capita of 7-8 kg, which is very low for a country like Turkey. The first aquaculture practices in Turkey initiated in the inland waters were during the 1970s for trout production and in 1985 for marine fish production. Due to the late commencement of aquaculture practices compared to other countries and to unconscious practices during its initiation years as well as inadequate follow up of relevant technological development, aquaculture in Turkey has relatively been underdeveloped. However, with the initiation of academic education related to aquaculture in 1980s and the cooperation between private sector and academic communities to realize projects on the issue has enabled aquaculture in Turkey to remarkably increase within a short period of time. The first sea bream and sea bass hatchery and cage systems in Turkey were established in 1985 in the Aegean Sea (OKUMUS and DENIZ, 2007). During the early 1990s Atlantic salmon and rainbow trout mariculture in the Black Sea has attracted considerable attention and efforts, but trials for salmon farming had to be Aquaculture in Turkey 283

terminated due to high water temperatures during summer. There were some attempts for kuruma shrimp on the Mediterranean coast during the mid 1990s. Initiative of bluefin tuna farming or fattening in the Mediterranean and Aegean Sea was the main development at the beginning of the new millennium. Lack of shellfish production has been a limiting issue for diversity of Turkish aquaculture; however mussel farming has recently been initiated in the Aegean Sea. The sector has developed to such an extent that Turkey is currently the third largest farmed finfish producer in Europe (after Norway) and the second largest producer of both sea bass and sea bream (after Greece) and of rainbow trout. Production figures in the last 5 years show that Turkey is among the first 12 countries with the fastest developing aquaculture sector. The rising aquaculture sector in Turkey that has recently began to develop, ranks among the sectors having a promising future (Figures 8 and 9). The aquaculture sector is divided into various branches. One of the main branches is trout farming which exists in almost each province of Turkey. Additionally, sea bass and sea bream culture which is carried out in provinces located in Aegean Sea coast; particularly in Mugla Province has also gradually developed. Furthermore, it is possible to find many initiatives in Turkey on tuna culture which has started accelerating and became widespread among European countries after 2000.

Figure 8. Distribution of aquaculture productions by species in 2007 (volume) (Source: TURKSTAT).

Figure 9. Distribution of aquaculture productions by species in 2007 (value) (Source: TURKSTAT). 284 Hayri Deniz

Some of these initiatives have succeeded and started production as soon as they have completed building their facilities in various places. In order to keep up with such a rapid development, existing fodder companies and fish net factories have renewed their technologies and have proceeded in this sector. In addition, the number of hatcheries and firms selling material and equipments for aquaculture purposes has increased, and new consulting companies have been established. Thus, foreign companies, seeing Turkey as an open market have started to make investments. The industry has developed to such an extent that Turkey is currently the third largest farmed finfish producer in Europe and the second largest producer of both sea bass and sea bream and of rainbow trout. The production figures of the last 5 years show that Turkey is among the first 10 countries with the fastest developing aquaculture sector. Its rapid development has been driven by various factors including relatively high demand for fish, availability of sheltered sites and good water quality, government supports, until recently loose or flexible regulations, high private sector interest for aquaculture investment, rapid development of specific marine hatchery technology and low labor cost. Currently there are 1,715 fish farms with total license capacity of 199,360 mt/y. More than half (56%) of this capacity is held by marine farms, and the rest is by freshwater farms. This also reflects current production share of 58% marine and 42% freshwater. Twenty-one percent of marine cage farms are found in offshore sites and holds 60% of total marine cage capacity. Considerable part of the farms is small to medium-size family operations. For example, 42% of the marine farms have capacity of less than 50 tons and 18% have over 500 mt. There are 20 marine hatcheries producing 330 million fry annually (MARA, 2008). One of the typical characteristics of aquaculture in Turkey is that it is mostly (96.57%) based on intensive and semi-intensive systems of carnivorous fish species production (Table 7). Rainbow trout ranks the first (44.72%) followed by seabass (29.79%), and sea bream (22.07%) (EUROFISH, 2008). There are number of marine farms (350), mostly cage farms and some ponds, which have completed license and permit issues. They have a total capacity of 110,840 mt/y. The major species cultured in marine waters are, sea bass (30% of total aquaculture production), sea bream (23%), rainbow trout (2%) and new Mediterranean species (2%). Sea bass and sea bream are responsible for the raise in production figures. In contrast, shellfish production is almost stable with annual production rates around 1500-2000 mt/year. Considering the capture-based aquaculture, there are 13 tuna-fattening farms (seven companies). Unfortunately, the socio-economic impact of aquaculture is greatly ignored and there are no reliable figures on this issue. It has been estimated that aquaculture provides 25,000 employment opportunities. However, in some particular jobs, especially aquaculture engineers, technicians and workers who are employed at production sites and hatcheries are working under very hard conditions. In recent years, fish production through aquaculture has increased. Competition between fishermen dealing with aquaculture in trout, sea bass and sea bream production has led the sector in seeking new fish species. Black Sea turbot, on the other hand, is one of the species with high market value. The culture of fish species has been practiced in the recent years to diversify aquaculture production in Turkey since the market of the main three species, sea bass, sea bream and trout, became more competitive. Therefore, Black Sea turbot has a great potential not only for aquaculture but also for the market (Table 8). Aquaculture in Turkey 285

Site selection is an important factor for the aquaculture sector, affecting general and farm level management both in inland and marine aquaculture. In order to make proper site selection some points need to be taken into account: type of water, temperature-salinity range, areas of ground and surface and water depth, type of ground, tidal range, elevation and distance from the sea, distance from land, nature of seabed, type of pumping system, coastal topography, shelter, access, services, local infrastructure and hazards.

Table 7. Marine aquaculture farms by production systems in 2008. (Source: MARA)

System No of farm Capacity (mt/y) Cages 238 100,834 Land-based (ponds) 108 3,581 Rafts/long-lines 3 1,625 Mobile (ship) 1 4,800 Total 350 110,840

Table 8. Mariculture production by species for 2003 – 2007 (Source: TURKSTAT)

Annual production (mt) Species 2003 2004 2005 2006 2007 Sea bass (Dicentrarchus labrax) 20,982 26,297 37,290 38,408 41,900 Sea bream (Sparus auratus) 16,735 20,435 27,634 28,463 33,500 Trout (Oncorhynchus mykiss) 1,194 1,650 1,249 1,633 2,740 Mussel (Mytilus galloprovincialis) 815 1,513 1,500 1,545 1,100 Others - - 2 000 2,200 1,600 Total 39,726 49,985 69,673 72,249 80,840

All of these parameters limit the availability of suitable zones for aquaculture. Aquaculture is an activity in conflict with a number of other activities because of competition for suitable areas with other sectors such as: tourism, environmentally protected areas, areas for culture and archaeology, navigation routes and harbors, recreation, marinas and resorts, and military installations. In the beginning, marine farms were set up in the protected shallow bays with little awareness of their environmental impact and technological and financial insufficiencies. As a result of this, they caused organic pollution and negative visual impact, which resulted in conflicts between aquaculture operators and other users, mainly in the tourism industry. These conflicts have caused great harm to the aquaculture industry. In order to prevent such conflicts and minimize environmental impacts, solutions with offshore mariculture systems and eco-friendly technologies are given priority. In addition, integrated coastal zone management (ICZM) models are being developed and implemented. The MARA has stated that the aquaculture production will be increased to 250,000 tons in 2020-2025 compared to the level of 139,000 tons in 2007 (AKBULUT, 2004). The province of Mugla ranks first (58,987 tons) in the production of aquaculture species being the first producer of trout (18,847 tons), seabass (27,979 tons) and sea bream (20,116 tons). After 286 Hayri Deniz

Mugla, Izmir is the second largest province in terms of production with 17,569 tons. These two provinces represent 60% of the total aquaculture production in Turkey.

Aquaculture Production Trends

According to 2007 statistics, the total Turkey production of fishery was 772,000 mt. Aquaculture contribution was 139,873 mt, where 59,000 mt were produced in inland waters and 81,000 mt were farmed in marine environments. Aquaculture in Turkey started with carp and trout farming in the 1970s and developed with gilthead sea bream/sea bass farming in the Aegean and Mediterranean seas in the mid-1980s, followed by cage culture of trout in the Black Sea during the 1990s and more recently tuna rearing in the Aegean Sea and the Mediterranean Sea in the early 2000s. Aquaculture is one of the fastest growing industries in Turkey having grown in volume by over 20% for the past 10 years. During the 1990s production quantities of the 3 major species, rainbow trout, sea bass and sea bream increased rapidly until 2000, followed by a decline during the subsequent two years due to serious general economic crisis in the country in general (Table 9).

Table 9. Aquaculture of commercially important species: 2000-2007 (mt). (Source: MARA)

Species 2003 2004 2005 2006 2007 Trout (inland water) 39,674 43,432 48,033 56,026 58,433 Carp (inland water) 543 683 571 668 600 Trout (marine water) 1,194 1,650 1,249 1,633 2,740 Sea bream 16,735 20,435 27,634 28,463 33,500 Sea bass 20,982 26,297 37,290 38,408 41,900 Mussel 815 1,513 1,500 1,545 1,100 Others - - 2,000 2,200 1,600 TOTAL 79,943 94,010 118,277 128,943 139,873

The most important farmed species are trout, sea bream, and sea bass; other species which are also farmed are bluefin tuna, molluscs, clam, carp, and eel. The VAT created by aquaculture sector in 2007 was approximately 1,641 million TL out of which 68% was achieved through fisheries and 32% through aquaculture (EUROFISH, 2008). The limited species diversity is illustrated in table 8, where 3 species clearly dominate, all of which are intensively cultured carnivorous species and are essentially luxury food items. The extensive and/or polyculture of other freshwater species such as cyprinids and also molluscs, crustacean and aquatic plant culture is very limited. Sea bream grow from 2-5 g to portion size in 11-12 months, while sea bass needs 18-26 months. The Feed Conversion Ratio (FCR) is around 1.7 for sea bream and 2.2 for sea bass. Trout are mostly cultured in concrete raceways and circular ponds. It may take 12 to 24 months to grow rainbow trout to a portion size of 200-250 g in traditional raceways; but it may be as short as 2-3 months in cages, particularly in marine cages in the Black Sea. Aquaculture in Turkey 287

It is also possible to produce large trout in cages. In the Black sea region rainbow trout is grown in land based farms or freshwater cages during summer and transferred to sea cages in November. They can be grown until the end of May and harvested before the critically high summer temperatures. Trout sold for the domestic market is mainly marketed as fresh and whole portion size, while rainbow trout produced in marine cages in the Black Sea is marketed as “Black Sea Salmon” at a size of 0.7-3.0 kg. Therefore, trout farming in cages presents an opportunity for development in the Black Sea region (EMRE and OKUMUS and MALTAS, 2007) (Figure 10 and 11). The aquaculture sector currently supports a total of 1,748 farms: 1,398 inland and 350 marine (Table 10, Table 11). More than two-thirds of these are small rainbow trout farms, while sea bass and sea bream farms comprise 17%. One of the major characteristics of Turkish aquaculture sector is the large number of small farms producing less than 10 mt per year. Many of these farms are small-scale family-operated and medium-sized, owner-operated farms. Indeed the aquaculture business model in Turkey varies from small family farms with multiple income sources to limited partnerships or corporations. The annual production capacity of the sea farms varies between 50-3,500 mt/year, while in freshwater farms it is generally much lower, ranging between 3-1,000 mt/year (Figures 12, 13 and 14).

Figure 10. Kent trout farm in Kayseri (Source: Kent Alabalık Inc.).

According to the Aquaculture Department of MARA-DGAPD there are currently 381 applications (64,860 mt/y) for new farms or for increasing the capacity of existing farms. Freshwater aquaculture production capacity increased by less than 2% during 2003-2004, but in 2007-2008 it increased by 18% (in terms of number of farms) and 55% in production capacity. The development of marine aquaculture has been significantly slower as the number of farms and total capacity has increased by 8% and 10%, respectively in 2007-2008.

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Figure 11. Trout farm in the Black Sea (Source: Own elaboration).

Table 10. Evaluation of marine fish farms according to size in 2008. (Source: MARA, 2008)

Size of farm Number of % of the Total Capacity % of the (mt) farms sub-sector (mt/y) sub-sector <50 146 42,00 3,972 4,00 51-100 59 17,00 5,245 5,00 101-250 50 14,00 8,905 8,00 251-500 30 9,00 12.667 11,00 501-1000 47 13,00 41,391 37,00 >1000 18 5,00 38,660 35,00 TOTAL 350 100 110,840 100

Table 11. Evaluation of inland fish farms according to size in 2008

Size of farm Number of % of the sub- Total Capacity % of the (mt) farms sector (mt/y) sub-sector <10 607 44,47 3,513 3,97 11-20 192 14,7 3,175 4,59 21-40 296 21,68 8,189 9,25 41-50 44 3,22 2,149 2,43 51-100 82 6,01 7,258 8,20 101-150 26 1,90 3,503 3,96 151-200 19 1,39 3,680 4,16 201-250 23 1,68 5,610 6,34 201-500 33 2,42 12,849 14,52 501-1000 41 3,00 33,694 38,06 TOTAL 1,398 100 88,520 100 Source: MARA, 2008.

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Inland aquaculture started in early 1970s and developed at a steady pace until the 1990s. During the nineties there were rapid developments in terms of production volumes and production systems. This development lasted until the economic crisis during 2001-2002 which hit the sector badly. After the crisis the sector recovered rapidly with the help of production subsidies. In inland farming the province of Trabzon ranks the first with 65 farms.

Figure 12. Kılıc sea bass and sea bream farm in Mugla (Source: Kılıç Holding).

Figure 13. Land-based sea bream and sea bass farm in Mugla (Source: Own elaboration). 290 Hayri Deniz

Figure 14. Aqua-Dem bluefin tuna farm in Izmir. (Source: Own elaboration).

The provinces of Ordu, Sivas, Mugla, Samsun, Sakarya and Rize rank second with 20-30 farms each. The province of Mugla leads in terms of volume of inland fish farming with a production of almost 11,000 tons/year followed by Kayseri with 4,000 tons in 2007. Trout farming in Turkey refers to Oncorhynchus mykiss, commonly called rainbow trout due to a red-colored stripe from the gills to the tail along the lateral line. It is essential to make the difference between large trout and portion trout. Large trout also commonly named salmon trout is raised in floating cages in the Black Sea, while portion size trout is farmed in all regions of the country, from hatching to commercial size, in a freshwater environment (FISHE, 2000). Farmed fish productions have been increasing rapidly and regularly, but captured fish productions have been decreasing or more or less standing firm for three major species because of over fishing and pollutions. On the other hand, most of wild sea bass, sea bream and trout is sold to restaurants or hotels without statistical compilation. There are 20 active marine hatcheries producing around 250 million sea bass and sea bream fry annually. These hatcheries are modern, employing automated water quality control and feeding systems and producing out of season fry. There have been shortages in sea bream fry supply in recent years and sea bream fry imports (25 million fry) have been permitted during the 2007 production. Some hatcheries also export sea bass and sea bream fry. The leading company in Turkey has three hatcheries and total annual capacity of 200 million sea bass and sea bream fry (Figure 15). Three other operators each have two hatcheries and between them produce 130 million fry. The total production target of these hatcheries for the 2007 was around 332 million fry. Half of these marine hatcheries have also attempted to produce other new Mediterranean species. There are 120 licensed trout hatcheries producing around 250 million fry annually. Although based on the current trout production of around 50,000 mt, the estimated trout fry demand is close to 300 million (Figure 16). Aquaculture in Turkey 291

Figure 15. Kılıç sea bass and sea bream hatchery in Aydın (Source: Kılıç Holding).

This is because most of the trout farms have small hatcheries or hatching systems to produce their own eggs only. However, some big trout producers import eyed eggs, mostly from the USA. Many of the trout hatcheries are old and in need of modernization and upgrading. These hatcheries only operate seasonally and have incurred heavy losses due to pathogens and water quality fluctuations. This is a major issue that the government should be addressing through the establishment of regional brood stock management and hatchery units (EU ACQUIS TURKEY, 2007). Live fish import and export permits are issued by MARA (DG for Protection and Control in consultation with DG General for Production and Development). Health certificates are required to protect against major pathogens and products which arrive at designated airports or ports.

Figure 16. Gümüşdoğa trout farm in Mugla. (Source: MARA).

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Structure of the Aquaculture Sector

Production from marine aquaculture totaled 80,840 mt (59%), whilst freshwater aquaculture production was 59,033mt (41%) in 2007. Freshwater production is carried out either in land-based units extracting water from rivers (the major type of production unit), or in cages set in lakes and hydro-electric or irrigation dams. In contrast, marine aquaculture production mostly depends on cage farming. There are 108 land based sea farms and 242 sea cage farms. Marine aquaculture in Turkey (92% of sea farms) is located primarily on the Aegean coast where geographical and hydrographical conditions suit the species cultured (Figure 17).

Figure 17. Geographical distribution of Aquaculture production by provinces 2007 (Source: EUROFISH).

There are only 12 farms on each of the Mediterranean and the Black Sea coasts. Along the Aegean coast 63% of the total marine fish farms are situated in the province of Mugla, 23% in Izmir and 5% in Aydin. Thus, site availability for cages is a major constraint for further development in the Aegean Sea, whilst in the Black Sea high summer temperatures for trout and low winter temperatures for sea bass and a general lack of sheltered areas are the main limitations. The province of Mugla ranks first (65,763 mt) in the production of aquaculture species being the first producer of trout (12,268 mt), sea bass (29,221 mt) and sea bream (24,259 mt). After Mugla, Izmir is the second largest province in terms of production with 19,665 mt. These two provinces represent the 60% of the total aquaculture production in Turkey (Figures 18 and 19).

Aquaculture in Turkey 293

Figure 18. Distribution of marine fish farms by regions as a number. (Source: MARA).

Figure 19. Distribution of marine fish farms by regions as a capacity. (Source: MARA).

Three main production systems are employed in Turkey: concrete raceways, floating cages and ponds. Raceways are used mainly for trout production, floating cages for sea bass, sea bream, trout and tuna, whilst ponds are used mainly for carp and sea bass (Figure 20). Concrete circular ponds are also employed for trout production. Fiberglass tanks are mostly preferred in hatcheries and juvenile production. There is only one farm using a closed recirculated aquaculture system. Mussels are cultured on ropes suspended from floating rafts. The cages used are mostly circular, made from High Density Polyethylene (HDPE), with diameters (ø) ranging from 12 to 66 m. Sea bass/sea bream farms are using ø 16-30 m, while trout producers use cages smaller than ø 20 m, and the tuna farmers prefer over ø 50m. Small wooden cages are only used in trout production in inland waters. Currently there are around 171 freshwater cage farms with a total capacity of 25,350 mt per year (Figure 21).

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Figure 20. Distribution of marine fish farms regarding the culture systems (number). (Source: MARA).

Figure 21. Distribution of marine fish farms regarding the culture systems (capacity, mt). (Source: MARA).

Recently, big companies have started to established standard offshore sea bass/sea bream production systems with an annual capacity of 2,000 mt consisting of 18 cages of ø30 m and automated feeding systems. Turkish aquaculture has limited species diversity. Currently only the following species are cultured commercially: Rainbow trout (Oncorhynchus mykiss); Sea bass (Dicentrarchus labrax); Sea bream (Sparus aurata); Carp (Cyprinus carpio); Blue-fin tuna (Thunnus thynnus) and Mediterranean mussel (Mytilus galloprovinciialis).

Diversification of Cultured Species

There are many major new or alternative Mediterranean species cultured in experimental or pilot scales such as common dentex (Dentex dentex), common sea-bream (Pagrus pagrus), common pandora (Pagellus erythrinus), sharpsnout sea-bream (Puntazzo puntazzo), white grouper (Epinephelus aeneus), shi drum (Umbrina cirrosa), striped sea bream (Lithognathus mormmyrus), meagre (Argyyrosomus regius), greater amberjack (Seriola dumerili), brown Aquaculture in Turkey 295

meagre (Sciena umbra), white sea-bream (Diplodus sargus), two-banded sea-bream (Diplodus vulgaris).

• Common dentex (Dentex dentex) This is the first Sparid species farmed experimentally since 2002, and the first larviculture production was carried out by Akuvatur (SAKA and TUNCER and FIRAT and UCAL, 2007). In the last 3 years, 150 tons of Common dentex have been coming out to the markets from Akuvatur. There are still some problems from the larval to end of the on- growing stage. Selection of broodstock from wild stocks is not possible during the spawning period and breeders are very sensitive to manipulation (Figure 22).

Figure 22. Cultured common dentex (Dentex dentex) (Source: Akuvatur Aquaculture Inc.).

• Sharpsnout Sea Bream (Puntazzo puntazzo) Recently, this species has become one of the most interesting candidates for new species in Turkish aquaculture operations. Two companies, Pınar Marine Product Inc. and Akuvatur Marine Product Inc., have been involved in the production of sharpsnout (Figure 23). Over the past 3 years Akuvatur has produced about 30 tons of sharpsnout Sea Bream.

Figure 23. Cultured Sharpsnout Sea Bream (Puntazzo puntazzo) (Source: Akuvatur Aquaculture Inc.).

• Striped Sea Bream (Lithognathus mormmyrus) This species is also a new candidate fish for aquaculture in Turkey. Pinar Marine Product is producing Striped Sea Bream. After 24 months of growth the fish reaches 200-250 g weight. The achieved survival rate is 90%.

• Brown meagre (Sciena umbra) 296 Hayri Deniz

Meagre is not a widely known species, and it therefore does not demand high prices in the domestic market. With respect to the export laws, the provenance certificate and the bureaucratic process is the main problem for producers and enterprises. Over the past 3 years Akuvatur has produced about 5 tons of brown meagre (Figure 24).

Figure 24. New cultured brown meagre (Sciena umbra) (Source: Akuvatur Aquaculture Inc.).

In addition to the species mentioned above, there are other candidate species that are being developed in Turkey such as common sea bream (Pagrus pagrus) (Figure 25), blue spotted sea bream (Pagrus caeruleostictus) (Figure 26), red shi drum (Umbrina cirrosa) (Figure 27), white grouper (Epinephelus aenaus) and leer fish (Lichia amia). Furthermore, extensive farming of oyster (Ostrea edulis), clam (Tapes decussatus) and warty venus (Venus verrucosa) is conducted in a few lagoons in Marmara Region. Production of tilapia fish has been going on for a long time at Çukurova University in Adana, although that they are not included in the aquaculture records (BASCINAR, 2004).

Figure 25. New cultured common sea bream (Pagrus pagrus) (Source: Akuvatur Aquaculture Ltd.). Aquaculture in Turkey 297

Figure 26. New cultured blue spotted sea bream (Pagrus caeruleostictus) (Source: Akuvatur Aquaculture Inc.).

Figure 27. New cultured shi drum (Umbrina cirrosa) (Source: Akuvatur Aquaculture Inc.).

Figure 28. Black Sea turbot (Psetta maxima) (Source: SUMEA).

Efforts are being made to develop the commercial production of species new to the Black Sea as well. The target species are turbot (Psetta maxima) (Figure 28), sturgeons (Acipenser spp.) and native sea going trout (Salmo trutta). Considerable progress has been achieved in the hatchery phase for turbot, but there is a need for considerable investment for on-growing. The Government of Turkey has set a target to promote aquaculture industry, including the development of culture techniques for new species in the 8th national Development Plan 298 Hayri Deniz

(2001-2005). Black Sea Turbot was identified as the top priority species. To achieve the Plan, the Government of Turkey requested a series of technical cooperation with the Government of Japan (JICA, 2008). A Technical Cooperation Project on Developing a Roadmap for Turkish Marine Aquaculture Site Selection and Zoning Using an Ecosystem Approach to Management was submitted to the FAO by MARA and it was accepted by FAO and completed in 2008. In addition, a technical cooperation project on the conservation, restocking and developing commercial aquaculture of sturgeon was submitted to the FAO in 2005. This project was accepted by FAO in 2008 and it will be completed in 22 months. In the inland aquaculture sector, some alternative salmonid species (such as brown and brook trout) are being reared as an alternative species alongside rainbow trout.

Aquaculture Regulation

Article 13 of the Law states that those who wish to farm aquatic species for commercial purposes are obliged to apply to MARA by informing the Ministry about the location, characteristics and management of the facilities, and submit the enterprise’s project and plans. Permission is issued by MARA if there are no adverse effects in terms of public health, the national economy, navigation or science and technology. The provisions of the last paragraph of Article 4 of the Fisheries Law 1380 are also applicable for production units to be established in the sea and inland waters. According to Article 13 of the Fisheries Law, the procedures and principles related to aquaculture are determined by the Aquaculture Regulation, which was issued in 2004. This regulation was amended in 2007, and it sets out rules for the following issues (GOZGOZOGLU, 2007):

• Site selection for inland and marine farms. • Application and evaluation procedures for fish farming licenses. • Approving the projects and issuing licenses. • Improving production capacity, species etc, cancellation (closing down farms), site changes and sales. • Other aquaculture activities (tuna fattening, organic farming, etc.). • Importing brood fish, eggs and fry. • Compulsory technical staff employment. • Fish health management. • Environmental impacts and protection. • Monitoring and control of farming activities. • Fish welfare.

MARA has 4 main DGs and staff compliment of about 40,000 in all branches. The DG of Agricultural Production and Development is the one responsible for all aquaculture activities. All aquaculture producers must have an aquaculture license of registration from the DGAPD Department of Aquaculture. The details of the application, issuing and cancellation of the aquaculture license are described in the Aquaculture Regulation, 2004. This Regulation was amended in 2007 by adding fish welfare issue. Aquaculture in Turkey 299

Site Selection and Licensing of Farms

Entrepreneurs or applicants need to submit their applications either to central offices (Aquaculture Department of DGAPD in Ankara) or Provincial Directorates of MARA with all the relevant supporting documentation. For example, an application with detailed information on the species, capacity, the production system along with a map of the area (1/25,000 scale) has to be submitted. Applications for on-growing farms and hatcheries up to two million fry/year capacity of the following species: trout, carp, sea bass and sea bream can be submitted to the Provincial Directorates. Whereas, applicants for other on-growing species (namely turbot, sturgeon, eel, algae, molluscs and crustacean species) and trout, carp and sea bass/sea bream hatcheries with a annual capacity of more than two million have to apply directly to the Aquaculture Department in Ankara. A team of experts from the central or provincial office then visits the site and prepares a preliminary survey report. If the report is positive, a preliminary license is issued for 8 months which can be extended for up to 4 months. Supporting documentations submitted for the preliminary license must include an application letter, site map, the preliminary survey report and a water quality report.

Environmental Impact Assessment and Monitoring

The entrepreneur can prepare the full project documentation, which includes a farm or a hatchery design and a feasibility report and an environmental impact assessment (EIA) report. Approval is also needed from other related institutions depending on the nature of the project (e.g., Ministry of Environment and Forestry, Ministry of Health, Maritime Affairs, Department of Transport, State Hydraulic Works, Ministry of Culture and Tourism). If the project is approved, the license (Fish Farming Document) is issued along with a ‘Producer Certificate’. This process usually takes about 1 year. The rental contract period for marine cage sites is granted for a maximum of 15 years which can be terminated earlier by the government. According to the Aquaculture Regulation (2004) all the hatcheries have to employ technical staff (graduates from related departments of universities) and one of them should be assigned as a Technical Manager. The minimum compulsory employment for on- growing farms depends on the production capacity of farms (Table 12).

Table 12. Fish Farm Technical Staff Requirements

Capacity (mt/year) Technical staff 50-249 1 250-499 2 500-749 3 750-999 4 > 1000 mt 5 Source: MARA.

According to current EIA legislation those fish farms with annual capacity of less than 30 mt do not require an EIA. Some fish farms which have between 30-1,000 mt annual 300 Hayri Deniz capacities may require EIA and this is determined by EIA commissions in each province. Farms must submit an EIA report if they produce over 1,000 mt per annum. There are 12 farmer unions (9 for freshwater fish farming and 3 for marine fish farming), 6 aquaculture associations and one Fisheries and Aquaculture Federation based in Izmir.

Conflicts between Other Coastal Sectors

The diversity of interests in coastal areas, and the complex mosaic of rights and economic activities, renders these conflicts as the greatest challenges to management. Coastal areas exhibit all those characters that make natural resource conflicts especially difficult to manage: high levels of scientific uncertainty, multiple interests, high economic stakes, complex spatial issues such as transnational impact, overlapping institutional responsibilities and the management constraints associated with common property resources. All these in practice hamper sustainable development of marine aquaculture. Some of the project outputs shall contribute to minimizing these conflicts. There has been steady growth in the economic significance and impact of aquaculture related activities in Aegean and Mediterranean coastal areas of Turkey. The aquaculture had a significant impact on the area, providing new employment opportunities and income into the local economy. It also provides relatively inexpensive bass and bream into national market.

Effect of New Environmental Law

However, after amendment in Environmental Law and related Notification issues, most of the current cage farms (approximately 85%) face either risk of closing down or have to move offshore areas. This would cause serious socio-economic consequences including sharp drop in production and more than 5000 job losses. Turkey had similar experience in the past when farms were forced to move urgently somewhere in inshore areas. Today same farms are facing the same problem. The project will help to secure sustainability of the offshore farms. Large finfish farming companies tend to lease suitable offshore sites, while small farms are having difficulties leasing sites and moving offshore. The project will develop ways of bringing small farms together and leasing them common sites which will help the small farms to survive. Currently, various companies exhibit the tendency of increasing production capacity. Although such tendency is not possible to do in inshore waters, moving offshore will provide a better opportunity to achieve this objective. The advantages of this approach is to increase the stocking density, while decreasing the on-growing duration and the incidences of disease outbreaks. Conflicting issues between ministries/institutions and legislation create problems in getting fish farming licenses and management of the sector. FAO TCP on “Developing a Roadmap for Turkish Marine Aquaculture Site Selection and Zoning Using an Ecosystem Approach to Management” was carried out jointly by FAO and MARA in 2008. The project main outputs were as follows:

Aquaculture in Turkey 301

• To train marine aquaculture farmers in the application of commonly agreed upon site selection criteria and identification of relocation options, using the ecosystem approach to mariculture management. • To prepare a draft pilot zoning plan for mariculture zones with short, medium and long term options for present and future marine aquaculture enterprises in support of a sustainable sector development. • To develop a road map of actions to define mariculture areas and to move farming to offshore and open sea areas. • To hold a stakeholders workshop to increase awareness and social acceptability of stakeholders active in the coastal marine environment, on the rightful place of mariculture within this environment. • To prepare draft advocacy brochures to be posted in places of marine aquaculture within the coastal environment and other leaflets as required in the process (Figure 29). • To write a project proposal for developing sound mariculture site location and management built in a multi-stakeholder environment using participatory approaches suitable for funding as UTF or other funding mechanisms.

The TUBITAK project on “Environmental Impact of Marine Cage Fish Farms on the Marine Ecosystem” has been carried out jointly by MARA, MEF, TUBITAK, SUFED and universities. This project outputs will also address environmental issues.

Figure 29. Advocacy brochures on importance of marine aquaculture (Source: MARA). 302 Hayri Deniz

Development of Turkish Aquaculture

There are many reasons to encourage the future development of the Turkish aquaculture sector:

• Consumption of fishery products in Turkey reached 8.20 kg per capita per year (kg/c/y) in 2007, whereas in 1996 the consumption rate was about 7.60 kg/c/y. This corresponds to an increase of about 1.5 kg/c/y over 10 years which is combined with the growth in population of 10 million inhabitants over the same period amounts to a total additional 120,000 mt consumed in Turkey in 2007. Due to the size of the Turkish population, any slight increase in domestic consumption will substantially impact the volumes of fish products consumed on the domestic market. The additional volume consumed on the domestic market nearly matches the total Turkish aquaculture production of 139,873 mt in 2007. • The production of seafood has become a strategic sector for Turkey since Turkey cannot export any other product of animal origin to the EU other than fishery products. The high external demand, especially from Italy, Spain and Greece has acted as the driving force for the Turkish aquaculture sector. • The low cost of labor is a comparative advantage for the Turkish industry and contributes to its profitability. Workforce in Turkey is cheaper than in other competing Mediterranean producer’s countries with an average monthly salary of 250 € for a skilled worker. • The industry imports raw materials paid for in US Dollars but exports final production in Euro, increasing profitability because of the current depreciation rates of the Dollar. • Payment terms and conditions are favorable for the producers. The average payment period to suppliers is between 12-18 months. There is no regulation concerning the payment conditions, and as reported this is the way the industry is used to work. • Government subsidies to aquaculture including subsidized energy supplies have contradictory effects. Government facilities, as the policies applied by the Agricultural Bank are really convenient for the development of the industry: a) Credits for fry, feed, staff, maintenance, etc are given for an 18 months period maximum. b) Credits for cages, ponds, hatcheries, systems upgrade, change to recirculation systems, equipment, etc are given for a maximum payoff period of 5 years. c) For a credit less than 130,000 € an 8.75% interest rate applies. For a credit over this amount the interest rate is a 17.5%. These interest rates could be changed by the bank. As reported by the bank representatives the unpaid rate of credits is only 3%. d) Governmental planning has thus resulted in a one-sided support to stimulate production growth without other regulatory measures. Large production increases and low prices especially on the domestic market have brought the Turkish aquaculture industry to an unstable situation. • Other factors that are reported to influence the development of Turkish aquaculture are the faster growth rates of marine species in Turkish waters compared with Greece Aquaculture in Turkey 303

or Italy, the non-compulsory insurances and the development of technical equipment especially in inland aquaculture.

General View

The potential for development of the Turkish aquaculture industry will likely be stimulated by the continued population growth which is expected to reach 76 million in 2010. This growth will lead to additional demand either at the present or higher rates per capita consumption. Some producers state that they have no surplus for export because all production quantities go to fill the domestic demand especially for trout (EUROFISH, 2008). At the same time, it can be seen that Turkish aquaculture products are beginning to be exported to new markets such as USA, Canada and the Middle-East. Vertical integration is another trend influencing the sector. The industry is increasingly moving towards integration of production and processing facilities in order to optimize the value of the production. At the same time, the sector is undergoing a process of concentration on fewer and larger units, indicating the maturity stage which the industry has achieved. As an example of this, one company accounts for 50% of the total Turkish production of fry, whereas, in marine aquaculture, 20% of the producers account for 80% of the production. However, the aquaculture sector in Turkey in general is not well structured despite the high level of manpower and technology and the scale of the industry. Marine aquaculture facilities vary from small units that are not highly competitive in the sector to full-blown industrial ventures that compete in the global market. From the point of view of some stakeholders the Small and Medium Enterprises (SMEs) should learn to work together and control the costs as some SMEs are already doing. But working in partnership does not seem to agree with the tradition of the Turkish mentality, and generally SMEs tend to work without advanced planning and to produce without looking at the market.

FUTURE DEVELOPMENT CHALLENGES

One of the major challenges facing Turkish aquaculture today is the strong media and public opinion opposing marine cage culture. The issue is directly related to the competition for resource utilization and less with environmental impact or sustainable utilization of coastal areas, since it is claimed that other activities such as the tourism and recreational industry also have a negative environmental impact on coastal zones. As a consequence of this conflict marine cages are forced to move offshore. This new scenario is going to affect negatively mainly the SMEs as many of them cannot afford investments and costs in changing the production system. But at the same time this new scenario opens new opportunities for increasing production and investments using new technologies. Another challenge is the human and industrial pollution of coastal zones, which are seen by the aquaculture sector as a threat for its development. Climate change is seen as a potential challenge as environmental conditions varies widely between species and also between life stages of individual species. 304 Hayri Deniz

In general environmental conditions are seen as a major challenge for the development of the industry. The cost to treat potential diseases can have a big impact on the profit margin of the industry. The industry clearly sees this issue as a challenge in connection with the cost efficiency performance of the activity. Turkish Government gives countdown to foreign investments. There are some Greek, Norwegian companies such as Nereus, Selonda, Helenix and Fjord Marine.

Framework for Regulation and Planning

Economic growth in Turkey during the last years has favored most sectors including the aquaculture industry. From 2003 to 2007 direct foreign investment in Turkey has increased rapidly. However, aquaculture stakeholders, generally, have a negative assessment, even if the government is supporting the industry financially. The complaints concern the lack of communication and coordination among authorities and with the industry as well as the need for integration and harmonization of related policies and regulations. The institutional structure of MARA is not considered as suitable for the industry. One of the most common complaints is that there is no single unit with full competence for aquaculture issues. This structural deficiency is considered as being damaging for the industry due to the bad coordination of procedures among the different bodies involved in the industry. Site selection for marine aquaculture is one of the main problems. According to the Aquaculture Regulation requirements for the distance between cage farms have to take the following criteria into account:

• projected annual production capacity (minimum annual production capacities for a cage farm is currently 250 mt/y); • water depth and current speed; • on offshore, open coast and outside the enclosed bays and gulfs, cage sites should have minimum 40 m water depth and have an EIA.

According to current 2003 EIA legislation those farms with annual capacity of less than 30 mt do not require an EIA. Farms having annual capacities between 30 and 1000 mt may require EIA and which is up to the province EIA commissions to decide. Farms aiming to produce over 1000 mt per year must submit an EIA report (MEF, 2007). In 2006 the Ministry of Environment and Forestry amended the Environmental Law to exclude marine cages from environmentally sensitive areas, enclosed bays and near shore areas. The amendment of the law and the implementing regulation was issued with no previous consultation with the stakeholders. The definitions in these legislations were considered too vague and the time limit given to farmers to move to new sites was short and unrealistic. This current situation has led the industry to a state of waiting for the final decision in order to start moving in the right direction. Due to frequent changes in the legislation it is reported that some companies had to move cages 3 or 4 times during 9 years upsetting production schemes and affecting production and sales results.

Aquaculture in Turkey 305

Research, Development and Innovation

There are 4 MARA Research Institutes (Trabzon Central Fisheries Research Institute, Mediterranean Fisheries Research, Production and Training Institute, Egirdir Fisheries Research Institute and Elazıg Fisheries Research Institute). There are 13 Fisheries Faculties and 5 Departments at the Agriculture Faculties providing undergraduate and graduate education in fisheries and aquatic sciences. The State Planning Organization (SPO) has supported comprehensive national projects in various fields but stopped their direct funding in 2006 by transferring funds to TUBITAK. TUBITAK is a scientific planning forum that helps to organize and support research activities. Fisheries research projects carried out in Turkey are generally funded primarily by the government (partly by MARA), TUBITAK or from the researching institutions' budget. Turkey has significant know-how and research capacity in aquaculture related areas but this is not well organized. Aquaculture RandD activities are mainly performed by various Fisheries Faculties. MARA research institutes have the capacity to perform aquaculture research or collaborate with other institutions in collaborative research programmes. Each year, 600 students graduate from these faculties, but the numbers employed by the sector are very limited, mainly in marine aquaculture. Faculties conduct aquaculture program studies as MSc and PhD thesis providing finance either from universities’ research funds or from TUBITAK. Currently, neither MARA nor the private sector is directly supporting university studies, which are mostly limited in duration (to that of MSc or PhD studies) and intended only for publication in scientific journals (Figure 30). The Turkish Journal of Fisheries and Aquatic Sciences (TrJFAS) is a refereed academic journal which is published by Central Fisheries Research Institute of Turkey and Japan International Cooperation Agency (JICA). It is published biannually (April and November) in English. It aims to address research and needs of all working and studying personnel within the many varied areas of fisheries and aquatic sciences. The Journal publishes English language original research papers, critical review articles, short communications and technical notes on applied or scientific research relevant to freshwater, brackish and marine environments. The Turkish Journal of Fisheries and Aquatic Sciences has been accepted to "SCIENCE CITATION INDEX in 2008.

Figure 30. An international and national journal has been published by MARA.

306 Hayri Deniz

MARA organizes its own RandD activities through the Directorate General for Agricultural Research (DGAR) and fisheries research institutes. Dissemination and extension services are the weakest link of the R and D activities. There is also a lack of partnership between stakeholders, producer associations and public institutions, which is considered as the major constraints for development of an environmentally sound and economically viable aquaculture sector. Few private processing companies have the resources for innovation, preferring instead to mimic successful applications elsewhere. Within the catching sector, there is limited finance availability for new investments that may even prove to be more efficient such as for example to test a new vessel design or test the potential of using fish aggregating devices. The situation is different in more prosperous sectors, most notably aquaculture and BFT ranching. However, potential investors still need to be convinced of the long term sustainability of the business, especially in the context of falling international prices, increased competition for sea areas from alternative users and increased pressure from the environmental lobby. On this basis there would appear to be a strong case for development of public sector funding of research activities with the objective of increasing the public benefit from sustainable usage of marine and fresh water resources. Research, Development and Innovation will be needed for the infrastructure development in moving marine cages offshore. The impact on the industry will be costly if the cages have to be moved offshore. The regional impact of such an operation has not yet been assessed. Difficulties of the Licensing Procedure

To apply for a production license is a long and tedious procedure. It may take around two years to obtain the final permission to establish an aquaculture facility. There are many institutions involved in the procedure of getting a license including: MARA, Ministry of Environment and Forestry, Ministry of Culture and Tourism, Ministry of Public Work and Settlement, Ministry of Interior, Under-secretariat for Maritime Affairs, and State Planning Organization. Furthermore, licenses have a validity duration between 10 and 15 years which is not considered long enough for an industry that works with long term plans. In inland aquaculture, the 10-15 years license period is considered inadequate. The price for water is high for an average inland farm facility, which has to pay €24,000 per year to obtain a 1,000 l/second flow of water. The stakeholders feel that the legislation was not made taking into consideration the requirements of the producers. The demand for drinkable water is expected to grow in the coming years following the population growth. Some companies are now facing water scarcity since the government is directing water supplies, mainly in the cities, for human consumption.

EU Harmonization

Twinning projects with the EU have been reported as highly beneficial for the industry. Since 2002 the EU has developed 66 twinning projects with Turkey in different economic areas. The TR-03-AG-01 (Alignment on EU Acquis in terms of fishery policy) Twinning Project is financed by the Pre-accession Program which aims to assist Turkey in meeting the criteria for EU membership through bilateral co-operation projects focusing on the transfer, implementation and enforcement of European legislation. The Fisheries Twinning Program Aquaculture in Turkey 307

supports Turkey’s legal and institutional alignment to the EU acquis in terms of fisheries policy. The overall objective of this project is to enhance the sustainable contribution of the fisheries sector to the national economy and prepare the sector for Turkey’s accession to the European Union.

Integrated Coastal Management (ICM)

Tourism is the main sector conflicting with the development of marine aquaculture especially on the Aegean coast and in particular on in the provinces of Mugla, Aydin and Izmir. Currently, around 90% of the existing 242 sea cage farms are located on the coasts of these 3 provinces and the great majorities (65%) are found on the coast of Mugla, near Bodrum, Fethiye, Marmaris and Datca. These provinces are also the heart of tourism sector, and important for nature conservation, historical and cultural areas. Aquaculture, tourism and recreation all require similar standards of water and environmental quality and the arising conflicts of interest are inevitable. In Turkey tourism is generally associated with hotels and second home areas which are reportedly many of them are only occupied during one month in the summer. Conflicts with aquaculture are also associated with the infrastructure that is directly related to the operations of the aquaculture sites. Recreational activities create conflicts of interest with yachts and pleasure boats, divers, windsurfers, swimmers and recreational fishery. Many hold the view that the problems and conflicts with aquaculture can be resolved by revising the public support schemes for aquaculture development in the critical areas involving all the stakeholders and improving communication between the MARA, MEF, Ministry of Culture and Tourism, and Undersecretariat for Maritime Affairs, the Authority for Protected Areas and all the authorities potentially involved in developing Coastal Management Plans integrating aquaculture as one of the activities in the areas.

Coherence of Government Programs-Necessity of Additional Program

The aquaculture industry considers that the government should give priority to support the marketing of aquaculture products in order to increase internal demand, and exports by supporting the creation of a Turkish brand. Support for the development of organic aquaculture should also be considered as a priority. Fish health research is among the topics to be given priority as cases of mass mortality in some fish farms are reported. It seems particularly necessary to work on disease control in order to avoid situations, which give a bad image to the industry. Food safety issues have been reported as an obstacle for the growing consumption of aquaculture products in Turkey. Consumers are reluctant to buy fish products especially in summer, because the cold chain is not sufficiently established along the trade chain. Most of the fishery products are sold in open markets on the street, and consumers are skeptical about the hygiene conditions at which these products are sold. New species are considered to hold a good potential for Turkish aquaculture. The programs to develop the commercial production of new species not only in the Aegean or in the Mediterranean but in the Black Sea as well would be welcomed by the industry. Among 308 Hayri Deniz the potential new species are turbot, sturgeons and native sea going trout. Considerable progress has been achieved in some of these species but the commercial stage is still far away. In terms of infrastructure development, industry representatives attach importance to the establishment of new storage facilities, processing facilities, piers and slipways. In inland aquaculture, availability of fish fry is considered as priority for public support following scarcity especially of trout fry.

Public Awareness

To improve the public perception of aquaculture products, the industry believes that there should be a promotion campaign on the health benefits associated with farmed products. However, some companies have reported the perception of a bad image of the aquaculture products among the consumers. The stakeholders are aware that the visual impact of the marine aquaculture activities is one of the main arguments used by the tourism industry against the aquaculture sector. Therefore, one of the concerns is to help improving the image of the industry by making the farms less obtrusive and to maintain the attractiveness of the environment. Furthermore, it is considered necessary to explain the real environmental impacts in order to demonstrate the sustainability of the activity. Producers also believe that food safety and especially traceability must be improved. As a general comment producers doubt that all the links of the trade chain are sufficiently committed to food safety and quality. Visual impacts, water impact and nutrient discharges are the most important environmental concerns for the aquaculture sector. All these issues which are rapidly exploited by the media, are affecting the image of the industry. As reported during many interviews, the information provided by the media lack scientific accuracy and there are those who suspect that this type of information is controlled by the tourist industry. One of the most powerful holdings in Turkey controls 65% of the Turkish media and has large real estate investments. It has been referred to as one of the main players in the stream of information aiming at eliminating the aquaculture industry from tourist areas.

Interactions between Aquaculture and Other Coastal Sectors

The traditional impacts of bio-chemical pollution, organic pollution and eutrophication or habitat modifications are not seen as a problem by the aquaculture industry from the point of view that these problems have been solved. Waste management would need more attention by the industry, as minimization of waste is not seen as a priority. The three Rs (Reuse, Recycling and Recovery) are not practiced in Turkish aquaculture also because there is not a complementary industry supporting these activities. Only large corporations exploit organic waste to produce pet food and there are pilot projects to make fertilizers from organic waste.

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Market Aspects in Aquaculture Products in Turkey

Essential aspects of the market as structure, competition, growth, analysis of demand, analysis of competitiveness, prices at the different stages on the trade chain, legal factors and requirements, market demands, market drivers, etc, were unknown elements both in terms of the domestic or the export markets. Lack of market information is seen as one of the main constraints for the aquaculture market development. On the domestic market low per capita consumption is the main problem. This situation could be overcome using promotion activities. The sources of information of the state on aquaculture industry and markets are the suppliers, trade fairs and some internet sites. The “Turkish Aquaculture and Fisheries Magazine” published by SUFED, “Yunus-Dolphin” published by SUMEA, “Aqua Culture” published by Mugla Fish Farmer Association, and “Fisheries” published by Aquaculture Engineer Association are seen as good information on the state of play of the industry. An important challenge facing the aquaculture and fisheries industry alike is to improve the distribution chain especially in the central part of Turkey, which would contribute substantially to gain consumer confidence for fishery products in general. In order to avoid taxes, the wholesale chain sales are not declared, resulting in poor statistical reporting and insufficient knowledge of the trade chain. Therefore the industry is demanding more controls on sales in order to predict future situations and to adopt production strategies according to the market demands. Concerning the strategy to increase exports of Turkish aquaculture products, the industry believes that the best option is to increase the value of the production focusing on the quality of the exported products instead of the quantity. The industry is starting to export to new markets. USA, Canada and especially Russia have been reported to represent excellent opportunities. However, the price of aquaculture products for Middle East countries is considered too high. Aquaculture industry in Turkey is also aiming at producing more processed products but it is necessary to upgrade the processing technology also to be able to comply with the EU legislation and to meet its stringent requirements on food safety and hygiene.

Consumer Aspects Regarding Aquaculture Products in Turkey

Annual per capita fish consumption is low in Turkey. Availability of fisheries products and dietary traditions appear to be the main factors limiting the consumption of fish. In order to increase consumption of seafood products on the domestic market the aquaculture sector believes in the need for consumer information and education. Promotional campaigns are seen as a real necessity for the industry. These campaigns should benefit consumers by providing them better information about the fish products they buy. Labeling with information of the commercial names, production method and origins should help ensuring that consumers are not misled, as for example when fishmongers sell most of the aquaculture products as wild catch. Particularly, fish larger than 600 g are reported as being commonly sold as wild caught since most people do not know where the fish is coming from. The marine aquaculture industry doubts the influence of tourism as potential market for aquaculture products mainly for two reasons: tourists visiting Turkey come with a medium- low purchasing power and prefer to go for cheaper options other than fish, especially in 310 Hayri Deniz tourist areas where prices are higher. The hotel trade industry believes that prices of aquaculture products are too high and they do not offer aquaculture species on a general basis to their clients. Tourism in Turkey is quite seasonal, where tourists come mainly in the summer time. Their fish product consumption should therefore be concentrated only on these months but the aquaculture industry has not recorded any special pattern regarding higher sales during the summer season. The potential impact of increased tourist consumption in the summer months on sales of aquaculture products should be easy to see, since the catching sector has a traditionally low production patterns during the summer, leaving the aquaculture sector as the only potential supply source for an increased demand for seafood (EUROFISH, 2008).

MARKETING

As described in detail above, official figures indicate that total fishery production was 772,323 mt in 2007, of which marine fisheries represent 67%, aquaculture 18%, inland fisheries 6% and the remaining 9% from other marine organisms. Pelagic species dominate marine landings and 60-70% of the total landings (by volume) are anchovy. Marine fish landings can be broadly categorized by their distribution through the following marketing channels:

a) Fish shipped directly to a fish market for an auction sale in the name of the boat. b) Fish sold directly on a boat to a local or distant commission agent. c) Fish shipped directly to a processing plant. d) Fish shipped to a cold store in the name of the boat.

The highest quantity of fish, primarily anchovy, is caught along the East Black Sea coast. Although large amounts of fresh anchovy are distributed to major markets nationwide, losses are high due to poor handling, packing and transport. With sustained large catches, many vessels therefore prefer to sell some of their fish to fishmeal factories. The total value of marine landings, based on 2007 data, was at TRY 675 billion €. A landing from inland waters was around 43,321 mt in 2007 which is 5.6% of total production in 2007 (Figures 31 and 32). The estimated first hand sale value of inland fisheries in 2007 was 60 million €.

Marketing and Aquaculture Producer’s Organizations

Producer organizations were organized according to the Co-operatives Law (No. 1163), Agricultural Unions Law (No. 5200) and Association Law (No.5253) and related regulations. But their legal status and organization types partly comply with the provisions of the EU legislation. Agricultural Producers Union (APU) is responsible for implementing regulation on the establishment procedures and principles of APUs and implementing regulation on inspections of APUs and central union of agricultural producers. Producer Union should have a minimum of 16 producers and a minimum production capacity based on product and product group. Fisheries Cooperative is established with a main status signed by at least 7 Aquaculture in Turkey 311

partners of the cooperative. Fishery co-operatives, fishery cooperative associations, the Central Associations of Fishery Cooperatives (SUR-KOOP) and Central and Regional Fishery Advisory Committees have an important role to play as representative stakeholder organizations. Currently there are 552 fisheries cooperatives recognized under the Fisheries Cooperative Law 1163, with a total membership of 28,385. Note that a co-op can be established as long as there are at least 7 signatories to the memorandum of incorporation (DENIZ, 2006). A minimum of 7 or more cooperatives that have the same objectives can establish a central union. There are 14 regional unions of fisheries cooperatives within Turkey, comprised of reportedly 552 cooperatives and one central union in Ankara. According to 2007 data from the SPO, only 23% of fishermen in Turkey are members of a cooperative. It is reported that many of these cooperatives are usually not run according to their founding principles and objectives and are not well managed. Since their emergence in the 1940s fishery cooperatives have failed to provide the right institutional support for the sector, primarily because of “unfair competition, insufficient aids and subsidies, lack of solidarity and education, lack of leadership, wrong identification and planning, unqualified and uninspired business management” (UNAL, 2006). There is also one Turkish Fish Promotion Association. To improve the public perception of aquaculture products the industry believes the promotion of the health benefits associated with farmed products. However, some companies have reported the perception of a bad image of the aquaculture products among the consumers. The stakeholders are aware that the visual impact of the marine aquaculture activities is one of the main arguments used by the tourism industry against the aquaculture sector. One of the concerns is therefore to help improving the image of the industry by making the farms less obtrusive and to maintain the attractiveness of the environment. Furthermore it is considered necessary to explain the real environmental impacts in order to demonstrate the sustainability of the activity.

Figure 31. Fisheries imports and exports in 2002-2007 (mt) (Source: MARA).

312 Hayri Deniz

Figure 32. Fisheries imports and exports in 2002-2007 ($) (Source: MARA).

Producers also believe that food safety and especially traceability must be improved. As a general comment producers doubt that all the links of the trade chain are sufficiently committed to food safety and quality. Transport operators, distributors and agents do not have appropriate food control systems in the opinion of aquaculture producers.

Traceability, Labeling and Certification

Given below is the current Turkish legislation in respect of fish health and hygiene:

• Law No. 5179 and related regulations concerning production, consumption and inspection of foodstuff; The objectives of this law are: a) to ensure food safety, appropriate nutrition for the public and optimal hygienic production, processing, preservation, storage and marketing of all kinds of foodstuffs and materials and substances that enter in contact with food, b) to define the characteristics concerning the safety of all kinds of raw, semi- processed and processed foodstuffs, food processing aids and substances and materials that come in contact with food, in order to protect the interests of the producers and consumers and the public health, c) to identify the minimum technical and hygienic requirements for businesses that produce or sell foodstuffs; determine the procedures and principles concerning services related to an inspection of foodstuffs. • Fisheries Law (No. 1380) and Implementing Regulation on Fisheries (1995); • Aquaculture Regulation (2004); • Law No. 3285 on animal health and sanitation; and • Implementing Regulation on Wholesale and Retail Fish Markets 2004. These regulations include: criteria for establishment of markets; management and operation of fish markets; control and inspection of markets; and, minimum and general technical requirements for markets and associated facilities. • Law 1734 on animal feed; The purpose of this law is to stipulate the provisions for the preparation, manufacture, import, export, marketing and sale of animal feeding Aquaculture in Turkey 313

stuffs supplied to the market with a view to enabling rational livestock nutrition and to developing animal husbandry. • Law No. 3285 on animal health and sanitation control; the aim of this law is to prevent the transmission of diseases from animals and animal materials to humans and other animals. This law also addresses the fight against contagious animal diseases.

Traceability

The issue of quality assurance (QA) is not the nature and scope of the regulations but rather the lack of effective monitoring of the implementation of those regulations. For companies that already export to the EU, the inspection and certification procedures operated by MARA are considered effective, especially in the context of client relations and maintaining quality control and product specifications. QA and hygiene standards inside the main fish markets should be enforced by the market management, who usually engage staff that are expected to clean the market every day after the market closes. Fish samples are subject to microbiological, chemical and physical analysis and these services are provided by accredited laboratories. In Istanbul Market, one laboratory is located inside the market. The main problem in promoting QA through the marketing chain is the activities of unregistered businesses and the ease with which they can operate within the fishery sector. Such activity presents a threat to formal businesses, domestic consumers and the business interests of Turkey in export markets. The quality of fresh fish throughout the marketing chain could also in many cases be improved simply by the increased use of ice. While a number of steps may be taken, the priorities should be a strengthened inspection service, consumer education, the importance of enforcing product standards and providing assistance to all actors in the distribution chain to improve their handling of the product from the farm to the plate. The application and enforcement of market legislation is considered to have an important role in the future development of the sector, particularly as the country has the EU as a major market and it is harmonizing its legislation with the fisheries acquis. Factories with an existing ‘EU number’ will need to implement the new EU regulations related to HACCP and market standards with investments in new technology to meet these standards. This should in turn drive quality improvements in the domestic market particularly where processors operate in both markets. Local consumers will also benefit once MARA inspectors start enforcing the updated legislation. The introduction of market standards legislation should encourage greater transparency in the market place. Also, the market pressure on producers for better quality products will ultimately contribute to improved environmental management of capture fisheries. It will also have an impact on the FIS, as through the use of sales notes the collection of statistical data will be improved, thereby improving the traceability system. Assistance is also required to improve hygienic and sanitary control and enforcement, monitoring and control of the quality of imports, electronic auction facilities in key markets/landing sites and 314 Hayri Deniz technological investment to ensure compliance with the latest EU traceability requirements. There is no any obligation for traceability related seafood yet and available data.

Quality Schemes for Aquaculture Species

For companies that already export to the EU, the inspection and certification procedures operated by MARA are effective, especially in the context of quality control and product specifications. Some companies have created labels in order to differentiate their brand from the other companies, especially on the domestic markets. The quality of fresh fish throughout the marketing chain is one of the most important aspects for the producing companies, as it has been reported that this issue is one of the weakest points of the value chain. Companies as Kılıç, Pinar, Akuvatur and Bagci have their own quality label with identification of each fish. But, they are not using their quality labels for every product. For the aquaculture production companies it is important that the production conditions are monitored and protected from any potential negative effects. Increasing importance, not only for the big companies, is being given to traceability systems in order to assure that the product has been produced according to the company standards. According to the Fisheries Law and other relevant regulation all processing plants have to be registered. Those exporting to the EU have to be approved by MARA. According to MARA figures, there are 160 licensed and 17 unlicensed factories. According to the latest Consolidated List there are 101 processing facilities approved for export to the EU (EUROFISH, 2008). Due to the growth of the aquaculture sector in recent years many packing plants have also been established to handle fresh aquaculture products. The main market for frozen products is the EU and in particular Italy. There are strong opportunities for growth on the domestic market given the low level of fish consumption in large parts of Turkey, the drive to supply a low cost protein to low income segments, and the opportunity to freeze anchovy and other pelagic fish to ensure availability throughout the year. The aquaculture sector has shown an interest in processing systems, as they would like to increase the value of the production: cutting, filleting, drying, smoking and freezing are mentioned as the most probable options. As the consumption of processed fish products especially in the form of prepared meals increases in the European Union, Turkish producers see this situation as a potential market for processed products from Turkey. Still production companies do not have a clear idea about how to incorporate a processing plant into the production scheme. Investments in processing have been reported as necessary especially for inland aquaculture companies. Support from Spain as one of the leading markets of fishery products in the EU would be considered as advantageous. Dried, smoked and cured products are not very popular so the domestic market for these products is very limited. Marinated anchovy is produced for domestic consumption and export. Although smoked and dried fish products have lost ground to other processed fish, there are now several small-scale producers servicing the market, producing and exporting smoked trout, eel, and salmon. Canned products of fisheries are produced both by large scale factories exporting goods to foreign countries as well as by small family enterprises. Fishery products like tuna, mackerel, trout, bonito, anchovies and sardines are produced by the Turkish industry and they are easy to find in the local markets. One company, based in Canakkale and founded in 1983, Aquaculture in Turkey 315

invested in the sector and became in short time one of the canning leading producers in Europe. With 2,000 employees, it has an annual production capacity of 60,000 tons of fish and 30,000 tons of shelled sea food. Its market share in Turkey for canned tuna fish is 80%.

Organic Aquaculture

There are some enterprises to produce organic aquaculture. For instance, Pınar Deniz Urünleri A.Ş. has been producing mussel and trying to get organic certification. In addition, MARA DG of Agricultural Research is preparing the national project for organic aquaculture. Organic production has a high priority for MARA. Organic Production Regulation which was prepared in line with related Council Regulation 2092/91, amended by Council Regulation 392/2004 in force now. Agricultural Bank is giving the low interest credit reduced 70% than the normal standards of interest. Organic aquaculture in Turkey is almost non-existent yet. Certification is needed so that the products produced can legally be sold with the organic label. Although organic products are increasing in demand, their share on Turkish production is still close to zero. Investments in order to turn conventional aquaculture production into organic production is seen as a good opportunity to differentiate from the competitors and achieve market shares on the new market for demanding consumers willing to pay more for a better product. Turkey could also be seen as a good base for production of cheaper organic products aimed the export markets.

CONCLUSION

Turkey has access to the aquaculture resources of Aegean, Black and Mediterranean water bodies. The country is also endowed with rich inland waters and river systems with significant aquaculture potential. As a result of geographic and climatic variations, both in terms of marine and inland waters Turkey offers a wide range of species to the aquaculture sectors. Aquaculture in Turkey started in the second half of 1970. Today Turkey is the 5th largest aquaculture producer in Europe and 3rd largest excluding shellfish production. It is also the 2nd largest producer in Europe of seabass and sea bream and rainbow trout which leaves Turkey with a positive trade balance of more than 120 million Euros regarding fishery products. Turkish aquaculture industry has increased rapidly over the last years. In 1990 aquaculture production in Turkey was around 6,000 mt (Figure 33). In 2007, aquaculture production both at sea and in inland waters reached almost 129,000 mt. Moreover, since 2001 Turkish aquaculture production has doubled in production volume and the Turkish government has set a target to reach an aquaculture production of 250,000 mt in 2020 (Figure 34 and 35). Key farmed species in Turkish aquaculture are seabass, sea bream, trout and tuna, but the MARA is currently giving priority to the farming of alternative species and on the diversification of farming methods to achieve the 2020 target. Currently Turkish marine aquaculture is facing strong opposition from other coastal activities to the further expansion of coastal aquaculture activities. This situation is a consequence of the lack of Integrated Coastal Zone Management. As a consequence marine cages will have to be moved offshore. 316 Hayri Deniz

Figure 33. Development trend in aquaculture during 1994–2007.

Figure 34. Fisheries and aquaculture trend and future projection in Turkey.

This new scenario will mainly negatively affect SMEs but at the same time it will open new opportunities for increasing production and investment in new technologies. Most of the production of marine farming species and aqua feed production is carried out in the Aegean region because it offers the best suitable conditions for farming activities, with sheltered coastal waters and ideal growing temperatures year round. Most fish farms, especially seabass and sea bream farms, are concentrated on this coast. The production potential of Turkish aquaculture can be better exploited through improvements in management and handling. The Aquaculture in Turkey 317

interest for increasing production sizes for processing has been expressed as an idea for cooperation with foreign partners.

400000

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0 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020 -50000

Figure 35. Marine aquaculture trend and future projection in Turkey.

It is also suggested that the development of ecologic/organic production could help Turkey improve exports to western markets. Furthermore, the development of the south east Mediterranean coast of Turkey is seen as an area for future investments which could be interesting for foreign partners considering the good potential for inland and marine aquaculture in the area. Regarding inland aquaculture specifically, there still is scope for development of the sector by making adaptations through species and production methods diversification. Consumption of seafood on the Turkish domestic market is expected to grow thanks to growing population and expected higher per capita consumption. It is expected that the demand for prepared and ready to eat meals will increase in the urban areas. There is also a potential for export of processed fish products to the EU.

REFERENCES

Akbulut, B. Aquaculture in Turkey. CFRI, SUMEA Yunus Research Bulletin, 4:4, December 2004. Bascinar, N. Aquaculture in the world and an overview to the future of Turkey. – CFRI. SUMEA Yunus Research Bulletin, 4:4 December 2004. Deniz, H. and Karasubenli, A.Ç. Environmental policies in force and its effect on aquaculture in Turkey, MED Black Sea ICM 08. Deniz, H. (2001). Environmental impact of aquaculture in Turkey and its relationship to tourism, recreation and sites of special protection. Proceedings of the seminar of the CIHEAM Network on Technology of Aquaculture in the Mediterranean (TECAM) 318 Hayri Deniz

jointly organized by CIHEAM and FAO, Zaragoza (Spain) 17-21 January 2000. Cahier Options Mediterraneennes,55, 159-173. Deniz, H. The 1st Workshop on “Developing a Roadmap for Turkish Marine Aquaculture Site Selection and Zoning Using an Ecosystem Approach to Management” , 16 -17 July 2008, Izmir, Turkey, 2008. Deniz, H., Aquaculture development and its partnership between science and producer associations in Turkey, Report and Proceedings of the EIFAC Symposium on Aquaculture Development – Partnership between Science and Producers Associations. Wierzba, Poland, 26-29 May 2004, held in connection with the European Inland Fisheries Advisory Commission, twenty-third session. Wierzba, Poland, 26 May-2 June 2004. EIFAC Occasional Paper. No 37. Rome, FAO. 2006. 136p. Emre, Y. and Okumus, I. and Maltas, O., Trout farming, Marine Aquaculture in Turkey 2007. EUROFISH Report, Survey of the fish industry in Turkey within the special focus on cooperation and investment possibilities, 2008. Fiche, F. Rainbow trout sector in Turkey: Trends and opportunities, EASTFISH, 2000. Technical assistance to support the legal and institutional alignment of the fisheries sector to the EU Acquis, General Directorate for Protection and Control Ministry of Agriculture and rural Affairs Government of Turkey and European Commission, February 2007. Gozgozoglu, E., The fishery industry in Turkey, EASTFISH. JICA Final Report on aquaculture economy study for the Flatfish Culture Project, 2008.Gozgozoglu, E., Aquaculture Legislation, Marine Aquaculture 2007. MARA - DGAPD Aquaculture Sector Report, 2008. MEF - Communiqué on Fish Farms No 26413. Okumus, I. and Deniz, H., Past, present and future of the marine aquaculture, Marine aquaculture in Turkey, TUDAV, 2007. Saka,S. and Tuncer,H. and Firat, K. and Ucal,O. Culture of European Seabass (Dicentrarchus labrax), Gilthead sea Bream (Sparus aurata) and other Mediterranean Species, Marine Aquaculture 2007. Ünal, V. Profile of Fishery Cooperatives and Estimation of Socio-Economic Indicators in Marine Small-Scale Fisheries; Case Studies in Turkey. 2006.

INDEX

Aristichthys nobilis, 172, 185, 192, 218 A aromatase, 171, 172, 189 Artemia, 20, 49, 61, 63, 125, 143, 165, 166, 191, A. gulednstaedti, 198 200, 262 A. nudiventris, 106, 198 Artemia uromia, 200 A. ocellaris, 155, 175 ASMAK, 110, 112 A. persicus, 114, 198 Australia, 240 Abu Al Abyad, 110 Azarbayejan, 197 Acanthopagrus latus, 106, 109, 121, 122 Acipenser persicus, 106, 121 B Acipenseridae, ix, 19, 191 aeration, ix, 62, 87, 88, 89, 98, 99, 101, 115, 156, B. grypus,, 192 181, 261, 262, 272 B. sharpeyi, 114 Aeromonas, 24, 29, 30, 197, 204, 207, 208 B. xanthopterus,, 192 Aeromonas hydrophila, 24, 29, 30, 204, 207, 208 Bahrain, 93, 95, 103, 104, 105, 106, 109, 111, 112, Aeromonas hydrophila,, 24, 204 113, 119, 121, 123, 126, 127, 128, 129, 132, Aeromonas veronii,, 24, 204 134, 136, 137, 138, 139, 140, 143, 145, 146, African catfish, 118, 122, 126, 181, 257, 262, 274 147, 152 agricultural fertilizer, 88 Bandar Khyran, 109 Agriculture, 32, 37, 45, 107, 108, 115, 117, 119, 129, Barbus sharpeyi, 20, 106, 121, 191 130, 131, 132, 139, 140, 143, 144, 152, 155, barramundi, 2, 158, 163 157, 181, 188, 209, 257, 259, 261, 263, 270, Berkeh Khalaf, 107 273, 274, 275, 305, 318 Bighead, 42, 124, 126 alkaline phosphatase, 172 biofilter, 3, 178, 181 Al-Oula Marine Consulting Company, 103 biofiltration, 156, 178, 179, 180 Al-Wafra, 108, 141 Botirocephalus sp., 24, 204 Amphilina foliace, 24, 204 breeding, viii, 50, 54, 73, 74, 78, 81, 82, 83, 88, 104, Amphiprion, 15, 155, 175 106, 107, 109, 110, 117, 119, 128, 129, 171, Anisakis sp., 24, 204 172, 174, 209, 216, 217, 218, 219, 220, 228, aquaculture cage, ix, 87, 92, 95, 96, 99 229, 233, 234, 238, 243, 245, 247, 249, 250, Aquaculture History, 105 262 aquariums, 12, 88 Breeding, 49 Aquatic Animal Health, 8, 19, 132, 191 breeding grounds, 104 Arabian Gulf, ix, 50, 53, 87, 89, 91, 92, 93, 94, 95, Busheher, 26, 29, 205, 208 96, 97, 98, 100, 101, 257, 259, 266, 273 bycatch, 103, 110 Arabian Sea, 91 Arava, 156, 163, 173 C Arava valley, 156, 163, 173 Canada,, 197, 233 Ardag, 162, 165 cannibalism, 169, 183, 184, 185 320 Index capture fisheries, 103, 152, 250, 313 carotenoid, 73, 176 E Caspian Salmon, 121 E. coioides, 12, 106, 108, 109, 110, 112, 118, 139, Caspian Sea., 19, 29, 30, 106, 191, 197, 198, 207, 192 208 E. polyphekedion, 109 Caspian trout, ix, 19, 191, 192, 201 E. tauvina, 108, 109 Caspian trout (Salmo trutta caspius),, ix, 19, 191, Economy, 127 192, 201 Edwardsiell sp., 24, 204 catfish, 9, 24, 37, 42, 88, 110, 120, 138, 183, 189, Edwardsiella tarda,, 24, 204 205, 262 eggs, viii, 49, 50, 54, 55, 56, 57, 58, 59, 65, 73, 74, Caviar, 198, 207, 271 76, 77, 78, 79, 81, 82, 83, 106, 108, 116, 129, Certification, 129, 150, 267, 312, 315 134, 138, 145, 196, 230, 238, 239, 258, 262, challenges, vii, viii, ix, 16, 50, 54, 134, 180, 192, 291, 298 202, 252, 300, 303 Eilat, 1, 2, 4, 155, 156, 162, 168, 169, 178, 179, 181, Chanos chanos, 114, 121, 263 184, 187, 188 Chinese carps, 113, 114, 161, 193, 201, 218 enclosed bays, 88, 275, 304 Chlorella, 49 engineering design, 88 Choharmohal-va-Bakhteyari, 197 Environment, 87, 119, 120, 129, 131, 137, 139, 155, Cichlasoma nigrofasciatum, 36, 175, 185 181, 207, 299, 304, 306 Cochlodinium prykricoides, 199 Environmental, 26, 38, 84, 85, 91, 101, 130, 139, Color Enhancement, 176 150, 151, 183, 255, 256, 298, 299, 300, 301, Common carp, 107, 121, 124, 126, 193, 238, 261, 304, 317 280 environmental parameters, 87, 182, 242, 260 continental shelf, 42, 91 Epinephelus aeneus, vii, 1, 36, 169, 186, 294 Conversion efficiency, 197 Europe, 30, 127, 138, 173, 175, 187, 207, 208, 212, coral colonies, 178 233, 237, 239, 275, 283, 284, 315 Corynosoma stroumosum ., 24, 204 extreme waves, 95, 100 CPUE, 104 crawfish, 88 F crayfish (Astacus leptodactylus), 194, 200 Cryptocaryon, 71 F. indicus, 20, 26, 107, 108, 109, 110, 111, 114, 117, Ctenopharyngodon idella, 30, 106, 121, 126, 192, 118, 119, 120, 134, 139, 191, 193, 199, 202, 208 205, 265, 266 Cucullanus sphaerocephalus,, 24, 204 F.vannamei, 191 Cultured Brood Stock, 72, 74, 75, 78 fadrozole, 172 current intensity, ix, 87 FAO, 51, 84, 103, 104, 106, 109, 111, 112, 113, 114, Cyclopeeze, 65, 74, 75 115, 116, 117, 123, 127, 128, 136, 140, 144, CyHV–3, 155, 173 151, 152, 200, 207, 211, 213, 246, 253, 263, Cytophaga, 22, 202 266, 298, 300, 318 D FCR, 65, 135, 265, 286 Feed, 66, 73, 74, 75, 130, 137, 138, 176, 186, 243, 261, 269, 286 Dactylogyrus sp., 24, 204 Feed Composition, 66, 75 denitrification, 181 feeding behavior, 64, 85, 151, 239 Denmark,, 74, 197 Feneropeneaus semisulcatus, 20, 191 desalination, ix, 87 Fenneropenaeus indicus, 106, 121, 122, 265 design significant wave height, 98 fertilization, 50, 54, 73, 74, 82, 83, 86, 171, 239, 266 diadromous, 104 fetch length, 95 Diclybothrium armatum,, 24, 204 FFC, 109, 263, 264, 265, 266 Diplostomum spataceum,, 24, 204 filamentous, 22, 174, 202 disease outbreak, 11, 20, 21, 23, 43, 71, 132, 149, finfish, 34, 36, 41, 42, 104, 111, 112, 116, 120, 129, 173, 194, 202, 203, 300 135, 138, 141, 280, 283, 284, 300 Dissolved oxygen, 66 Index 321 fingerlings, ix, 19, 64, 66, 82, 85, 106, 108, 110, 113, 114, 116, 117, 119, 138, 140, 142, 151, 165, H 173, 191, 192, 194, 197, 201, 216, 218, 219, H. nobilis, 110 220, 226, 231, 238, 239, 240, 241, 242, 243, habitat, 103, 197, 229, 238, 239, 308 251, 260, 261, 262, 263, 266 Haliotis mariae, 108, 117, 122 Finland,, 197 Hamor, 20, 191 Fish Consumption, 136 harmful algal blooms, 103 fish farming, ix, 1, 32, 38, 88, 107, 108, 127, 129, hatching rates, 50, 59, 82, 83 130, 137, 138, 139, 144, 194, 218, 226, 250, HCG, 50, 78, 80, 81, 82, 262 259, 274, 290, 298, 300 Health, 16, 19, 20, 26, 33, 71, 84, 132, 133, 134, fisheries, 32, 35, 37, 44, 45, 54, 88, 105, 108, 111, 149, 202, 205, 248, 291, 299 113, 115, 127, 129, 130, 131, 136, 137, 139, Hebrew University, 155, 181 140, 142, 143, 151, 152, 176, 193, 207, 210, Hormonal Induction, 78 211, 218, 222, 226, 237, 246, 247, 250, 251, Hormuzgan, 107 253, 274, 276, 277, 279, 280, 286, 305, 306, Huraidha-Assir, 110 307, 309, 310, 311, 313, 314, 318 Huso huso, 24, 29, 106, 121, 198, 204, 207 fishing, 32, 41, 42, 44, 50, 53, 54, 57, 58, 103, 104, hybridization, 173, 189 118, 119, 128, 131, 156, 192, 209, 210, 216, Hypophthalmychthis molitrix, 192 217, 218, 222, 233, 235, 237, 238, 239, 240, hypothalamus, 171 241, 243, 246, 249, 250, 251, 253, 281, 290 Hypothalmichthys molitrix, 106, 121 Flavobacterium psychrophilum, 23, 29, 204, 207 Flavobactria, s, 24, 205 I Flexibacter, 22, 29, 202, 208 floating breakwater, 96, 98, 100 Ichthiophtirius multifiliis, 23, 203 flushing of the ambiant water, 87 Ichthiophtirius multifiliis,, 24, 204 Food Safety, 132, 133 IFRTO, 107, 151 formulated feeds, 49, 57, 62, 64, 244 indoor hatchery, 80 French strain, 171 Industry, 37, 103, 194 G inheritance, 175 Iranian Fishery Organization, ix, 20, 191 Isochrysis, 49 GCC, 104, 132, 137, 138 Israel, vii, ix, 1, 2, 3, 4, 155, 156, 157, 162, 163, 165, Gemma, 65, 75 166, 169, 171, 172, 173, 174, 175, 177, 178, genotype, 172, 173 179, 180, 181, 182, 183, 185, 186, 187, 188, Gilan, 22, 24, 30, 194, 195, 196, 208 189 gillnet, 54 IVO, 130, 132 Gilthead seabream, 121, 122, 124, 126 Gnathanodon speciosus, 109 J Golstan, 194, 195 Gonad, 55, 72 juveniles, ix, 36, 38, 49, 54, 61, 62, 64, 65, 71, 72, Gonado Somatic Index (GSI), 55 78, 83, 107, 108, 109, 111, 112, 116, 119, 120, Grass carp, 121 129, 135, 138, 141, 142, 144, 145, 146, 162, gravid females, 55 165, 166, 209, 226, 227, 229, 233, 238, 240, Green tiger shrimp, 121, 122 263, 265 grow-out, viii, 49, 50, 62, 64, 65, 66, 67, 69, 70, 72, Juveniles, 64 74, 82, 83, 107, 108, 119, 155, 165, 166, 169, 183, 196, 197, 213, 228, 235, 242, 243, 249, K 261, 265 Growth, 18, 64, 68, 85, 150, 153, 229, 231, 232, 254, Khozestan, 194, 196 257, 263, 273, 274, 282 KHV, 20, 24, 28, 175, 187, 205 Guilan, 106, 113, 114, 125 Kinneret, 156, 157, 158, 160 Gulf of Aqaba, 156, 162, 165, 178, 183 Koi, 24, 155, 173, 175, 187 Gulf Standards Organization, 132 Kolahi Fisheries, 107 gynogenetic, 172 322 Index

Kuwait, vii, viii, 11, 12, 14, 15, 16, 17, 18, 49, 50, maturity, 54, 55, 56, 171, 229, 261, 263, 264, 303 51, 53, 54, 56, 57, 66, 70, 71, 82, 83, 84, 85, 87, Maturity, 55 93, 95, 101, 103, 104, 105, 108, 111, 112, 113, Mazandaran,, 21, 194 116, 119, 121, 123, 125, 126, 127, 128, 130, Mean size, 58 133, 135, 136, 137, 138, 139, 141, 142, 143, mean wave period, 95, 96 144, 145, 150, 151, 152 Megaflow, 162, 183 Kuwait Institute for Scientific Research, viii, 11, 49, Mega-flow system, 168 54, 84, 85, 87, 101, 103, 108, 138, 143, 151, metamorphosis, 169, 189 152 methionine, 172 kyphosis, 166 Microalga, 61 Microgeophagus ramirezi, 176, 185 L Middle East, vii, viii, ix, x, 31, 33, 34, 103, 104, 105, 125, 134, 145, 151, 152, 257, 309 Lacotococcus garveiae, 21, 202 milt, 50, 55, 58, 72, 73, 82, 83, 171, 262 Larval Rearing, 61, 84, 146 monitoring, viii, 3, 27, 34, 35, 38, 45, 132, 133, 139, latitude, 91, 92, 257 140, 141, 145, 149, 174, 218, 244, 245, 246, Law, 129, 130, 131, 133, 134, 139, 298, 300, 304, 250, 313 310, 311, 312, 313, 314 Monodon baculovirus, 26, 205 L-carnitine, 176, 177, 184, 185 mortalities, viii, 11, 12, 13, 14, 16, 20, 25, 30, 41, 61, Legislations, 150 64, 71, 196, 202 Leptorhynchoides plagicephalus,, 24, 204 mullet, vii, 1, 2, 4, 6, 12, 25, 30, 45, 46, 71, 85, 109, Lernea sp., 24, 204 110, 117, 118, 119, 120, 122, 125, 126, 141, LH-RH, 50, 80, 81 156, 178, 180, 201, 263, 264, 278 Litopenaeus vannamei, 30, 107, 126 municipal wastes, ix, 87 live food organisms, 61 mycelium, 174 Liza sp, 121, 264 Longitude, 93 N lordosis, 166 Lorstan, 197 Nannochloropsis, 49, 61 Lutjanus argentimaculatus, 106, 121 Natural spawning, 77, 78, 108 Natural Spawning, 75 M necrosis, 19, 20, 25, 26, 34, 42, 43, 46, 71, 169, 173, 191, 205 Macrobrachium rosenbergii, 107, 121, 126, 262 Non-Indigenous, 125 Macrobracium rosenbergii, 200 North Africa, vii, ix, x, 44, 46, 103 Malachite Green, 174 Norway, 109, 119, 151, 197 Management, 19, 20, 71, 84, 86, 139, 140, 151, 188, nylon wires, 88 190, 200, 202, 266, 269, 298, 300, 307, 315, 318 O Mangrove snapper, 121 Mariculture, viii, ix, 1, 8, 11, 12, 36, 49, 54, 87, 106, O. spilurus, 108, 109, 116, 119, 260, 264 112, 118, 137, 141, 143, 146, 155, 157, 159, Obhur, 109 160, 162, 163, 165, 169, 178, 181, 263, 285 Olithodiscus, 178 Mariculture and Fisheries Department, viii, 11, 12, Oman, 91, 101, 103, 104, 105, 106, 108, 109, 112, 49, 54 113, 116, 117, 120, 122, 123, 125, 126, 127, marine aquaculture, ix, 36, 37, 87, 100, 140, 141, 128, 130, 132, 133, 135, 136, 137, 138, 139, 209, 212, 213, 215, 216, 220, 222, 228, 241, 141, 142, 143, 144, 145, 151, 152, 199 246, 247, 248, 257, 280, 287, 292, 301, 304, Oncorhynchus mykiss, ix, 19, 29, 30, 33, 36, 37, 307, 308, 309, 311, 315, 317 106, 191, 207, 208, 216, 217, 237, 285, 290, marine environments, 88 294 Marine fish, 223, 253, 310 oocytes, 55, 56 marine power, 87 Oreochromis niloticus, 37, 39, 84, 86, 108, 121, 122, Marine shrimp, 137 126, 152, 173, 174, 184, 274 Market, 127, 135, 309, 313 organic culture, 173, 183 Index 323 ornamental fish, 12, 20, 24, 28, 104, 111, 118, 125, 128, 138, 145, 155, 156, 163, 174, 175, 177, R 183, 204 Rachycentron canadum, 111, 122, 153 Ornamental fish, 157, 164, 177 Rainbow trout, 29, 114, 192, 196, 207, 216, 237, outbreaks, viii, 12, 16, 17, 19, 20, 21, 22, 24, 26, 27, 284, 294, 318 28, 30, 47, 173, 191, 199, 202, 205, 206, 208, Rainbow trout farming, 196 245 recirculating systems, 156, 180, 181, 182, 183 overfishing, 31, 88, 103, 198 recirculating-tank technologies, 88 oysters, 42, 88, 125, 178, 179, 212, 213, 220, 232, RECOFI, 104, 118, 145, 152 241, 251 red drum, 2, 156, 166, 173, 189 P Reproduction, 175, 177, 184, 253, 256 return periods, 92, 94, 95, 96 Pampus argenteus, viii, 16, 17, 18, 49, 50, 53, 66, 67, Rhabdosargus sarba, 110, 111, 122 68, 75, 84, 85, 86, 108, 121, 150, 151 Rutilus frisii kutum, ix, 19, 121, 191 pathology, viii, 6, 37, 41, 215, 218, 246 Rutilus rutilus, 121, 201, 217 Pathology, 71 pearl oyster, 20, 104, 107, 125, 145, 191 S Pearl oyster, 121 S. aurata, 4, 5, 6, 7, 107, 108, 109, 112, 116, 118 Pelvicachromis pulcher, 177, 185 S. canaliculatus, 109, 110, 112, 117, 118, 119 Per Capita, 136 S. parasitica, 174 periphyton, 174, 186 Sabaki tilapia, 109, 116, 121 Persian, 12, 20, 24, 26, 29, 30, 101, 105, 114, 121, Saccostrea cucullata, 108, 122 126, 129, 143, 191, 192, 198, 199, 201, 204, salinity, ix, 2, 55, 59, 84, 87, 105, 106, 116, 117, 207, 208 165, 166, 185, 260, 264, 274, 285 Persian Gulf, 20, 26, 143, 191, 199, 201 Salmo trutta caspius, 106, 121 Persian sturgeon, 24, 29, 30, 198, 201, 204, 208 salmon, 32, 47, 64, 65, 66, 74, 88, 106, 189, 239, Persian sturgeon (Acipenser persicus, 24, 29, 30, 282, 290, 314 204, 208 saltwater plants and animals, 88 Picnic seabream, 121 Saprolegnia, 23, 24, 174, 203, 204 Pike-perch, 121, 239 Saprolegnia spp., 24, 204 pituitary, 171, 239, 262 saprolegniosis, 23, 174, 204 Poecilia reticulata, 175, 176, 177, 184, 185 Saudi Arabia, x, 93, 95, 96, 103, 104, 105, 109, 110, pollution, ix, 2, 19, 20, 27, 35, 38, 45, 87, 88, 130, 112, 118, 119, 120, 122, 125, 126, 128, 131, 139, 145, 178, 187, 191, 192, 197, 198, 222, 132, 133, 136, 137, 138, 139, 141, 142, 144, 237, 260, 272, 281, 285, 303, 308 145, 151, 152, 257, 258, 259, 260, 261, 262, polyethylene, 88, 107 263, 265, 266, 267, 273, 274 polysaccharides, 172 Scotland, 8, 197 pond, 3, 54, 88, 116, 130, 153, 156, 173, 178, 179, Sea bass, 42, 46, 284, 285, 294 180, 181, 183, 188, 196, 203, 249, 265 seafood, x, 88, 104, 134, 142, 145, 182, 210, 231, Price, 135, 163, 188 252, 257, 267, 282, 302, 309, 310, 314, 317 productivity, vii, 107, 116, 134, 140, 169, 174, 182, seawater, 6, 58, 59, 66, 72, 74, 91, 105, 108, 109, 243, 257 137, 169, 180, 184, 185, 187, 232, 264 Pseudotracheliastes stellatus,, 24, 204 Seaweeds, 121 Q Seed, 137, 241 Sefid-Rud, 107, 198 Qatar, 93, 95, 96, 100, 101, 104, 105, 109, 111, 112, semisulcatus, 26, 30, 37, 106, 107, 108, 109, 110, 113, 117, 122, 124, 126, 127, 128, 129, 131, 111, 114, 120, 121, 122, 150, 152, 192, 199, 132, 133, 134, 136, 137, 139, 141, 142, 143, 201, 205 144, 145, 151 sex differentiation, 171, 184, 186 quality of marine water, ix, 87 sex ratios, 171 Quinaldine, 36, 66, 74 Sex ratios, 55 Quriat, 109, 116 sex-reversed, 173 324 Index shellfish, viii, x, 27, 88, 129, 157, 180, 205, 212, Trichodina sp.,, 24, 34, 204 213, 215, 220, 224, 249, 251, 252, 275, 283, tropical fish, 88, 174 284, 315 Shrimp farming, 199 U Siganus javus, 106, 121, 122 UAE, 93, 95, 96, 98, 100, 103, 104, 105, 110, 111, Silver carp, 238, 239 112, 113, 116, 119, 120, 122, 124, 125, 126, Silver Pomfret, 49, 81 127, 128, 129, 131, 132, 133, 135, 136, 137, silver pomfret hatchery, 60 138, 139, 141, 143, 144, 145 single point mooring, 90 Uronema, 11, 13, 14, 16, 17, 18, 71, 85 skeletal deformity, 165, 166 skin, 3, 6, 7, 9, 12, 14, 17, 24, 25, 71, 173 V Skrjabinopsolus semiarmatus,, 24, 204 Soybean meal, 172 Velamugil seheli, 109, 141 Spawning, 50, 54, 55, 75, 81, 84, 85, 151, 153, 229, Veterinary, 17, 19, 27, 29, 30, 33, 130, 132, 191, 230, 273 205, 206, 207, 208, 246 sperms, 58 Veterinary Organization, 130, 132 Stizostedion lucioperca, ix, 19, 191, 192, 217, 239 Vibrio alginolyticus, 26, 43, 47, 205 stocking density, 42, 59, 61, 116, 118, 152, 173, 185, Vibrio anguillarum,, 26, 205 230, 261, 264, 274, 300 Vibrio harveyi,, 26, 205 Streaked Rabbitfis, 121 Vibrio parahemolyticus 26, 205 Streptococcosis, 30, 34, 208 Vibriosis, 16, 34, 43 Streptococcus iniae, 3, 7, 9, 21, 30, 202, 208 VNN, 20, 28, 34, 43, 169, 205, 206 striped bass, 6, 8, 156, 158, 162 stripping, 57, 58, 81, 82, 181, 262 W Sturgeon, 24, 110, 114, 120, 143, 144, 147, 148, 151, 192, 197, 204, 207, 260, 271, 272 water depth, 55, 91, 92, 93, 116, 304 Sturgeon farming, 110 water filtration, 88, 239 sturgeons, 24, 25, 27, 28, 29, 106, 192, 198, 200, water quality, 12, 23, 24, 27, 28, 88, 178, 181, 186, 201, 204, 206, 207, 297, 308 187, 201, 202, 204, 206, 218, 243, 244, 260, surface skimmer, 62, 63, 64 264, 290, 291, 299 survival, 35, 49, 57, 61, 64, 72, 73, 84, 106, 150, water source, 88 153, 165, 166, 169, 172, 173, 176, 177, 184, water temperature, ix, 12, 22, 23, 24, 49, 55, 57, 66, 185, 197, 212, 245, 249, 263, 264, 265, 266, 67, 68, 69, 70, 71, 75, 77, 78, 83, 87, 117, 166, 273, 274, 295 169, 173, 175, 177, 197, 202, 204, 283 Systan-va-Balochestan, 205 wave and current induced forces, 87 wave climate, 87 T Weibull distribution, 94 white spot viral disease (WSD), 19, 191 Tehran, 19, 23, 29, 30, 106, 143, 191, 197, 208 Whitespotted Rabbit fish, 121 Tetraselmis, 178, 179 wild fisheries, 20, 88 Thunnus albacares, 109, 122 Wild Stock, 54 tidal variation, ix, 87, 96, 98, 100 World aquaculture, 104 tilapia, 4, 8, 37, 86, 88, 108, 109, 110, 112, 116, 117, 118, 125, 128, 129, 135, 137, 141, 142, 155, Y 156, 157, 158, 171, 173, 174, 180, 181, 183, 184, 186, 188, 189, 190, 219, 260, 261, 262, Yemen, 103, 104, 111, 112, 120, 122, 124, 125, 127, 263, 264, 274, 296 129, 131, 132, 134, 135, 136, 137, 138, 142, Tilapia, 105, 108, 110, 112, 116, 117, 118, 119, 122, 143, 144, 145 124, 125, 126, 128, 135, 137, 151, 152, 161, Z 173, 188, 189, 239, 260, 261, 262, 264, 273, 274 Zobaidy, 51, 84, 85 Trade, 37, 127, 134, 207 zooplankton, 36, 50, 169, 240