World Journal of Fish and Marine Sciences 10 (2): 05-17, 2018 ISSN 2078-4589 © IDOSI Publications, 2018 DOI: 10.5829/idosi.wjfms.2018.05.17

Biology of White Leg Shrimp, Penaeus vannamei: Review

12Hailu Dugassa and De Gyrse Gaetan

1Van Den Nestlaan 104, 2520 Broechem, Belgium 2Salisburylaan 133, 9820 Merelbeke, Belgium

Abstract: Shrimp aquaculture plays a significant role in the world economy. According to the information of the Food and Agriculture Organization (FAO) of the United Nations, marine and brackish water shrimp culture productions have expanded from less than 10, 000 metric tonnes in 1970 more than 4, 000, 000 metric tonnes in 2014. The most of the aquaculture shrimp contribution has come from Penaeus vannamei which accounts 80% of the whole shrimp production. Although the cultivated shrimp production has rapidly increased during these years, the annual economic losses due to disease were estimated to be approximately 1 billion US dollar per year since the early 1990s. Viruses and bacteria mainly cause the diseases of the shrimp. Hence, most of the published reviews focused on the diseases and production aspects of P. vannamei. However, the biology of this species is neglected during the last two decades. For better production and health management systems of this species, it is paramount to have basic and solid knowledge of the biology of P. vannamei. However, there are limited reviews available on the biology of P. vannamei. This is, thus, we are very motivated to review of the biology of the shrimp for efficient health management and production of the shrimp. The life cycle of this species is very complex and it usually takes around 1.5 years to complete the whole life cycle of P.vannamei. The external morphology of P.vannamei is well described and understood. We also highlighted the basic internal morphology and physiology of this species. There is limited information on the understanding of natural behaviour and feeding habits of this . Therefore, further studies are needed in future to have solid knowledge of internal morphology and physiology, natural behaviour and feeding habits of P. vannamei in order to improve the production and health management systems.

Key words: Morphology Physiology Life Cycle Biology P. vannamei Shrimp

INTRODUCTION production is from inland aquacultures [2]. The production from mariculture is dominated by P. vannamei Aquatic food production has transformed from which has reached 3.18 million of tonnes with an primarily based on fisheries to the culture of increasing estimated first sale value of 12.15 billion Euros. The other numbers of farmed species. According to the statistics of most important species are the black tiger shrimp FAO [1], the total world aquaculture production was (Penaeus monodon). The production of this species found around 73.8 million tonnes in 2014. This figure has reached 0.86 million tonnes with a value of 3.22 billion almost increased by 11% compared to the production of Euros [2]. 2012 which was around 66.5 million tonnes[1]. The total Shrimp aquaculture plays a significant role in the world aquaculture production of was 6.9 world economy. According to the information of the Food million tonnes in 2014 with an estimated total value of and Agriculture Organization (FAO) of the United 32.33 billion Euros. This figure of crustacean production Nations, marine and brackish water shrimp culture is almost increased by 7% compared to the production productions have expanded from less than 10, 000 metric figures of 2012 (6.4 million tonnes) with a value of 27.60 tonnes in 1970 more than 4, 000, 000 metric tonnes in 2014 billion Euros FAO [1]. Till now, more than 62 crustacean [1]. The most of the aquaculture shrimp contribution has species have been cultured in aquaculture farms around come from Penaeus vannamei (P. vannamei) which the world. The mariculture contributes to 60.8% of the accounts 80% of the whole shrimp production. Although crustacean production. The remaining 39.2% of the the cultivated shrimp production has rapidly increased

Corresponding Author: Hailu Dugassa, Van Den Nestlaan 104, 2520 Broechem, Belgium. 5 World J. Fish & Marine Sci., 10 (2): 05-17, 2018 during these years, the annual economic losses due to disease were estimated to be approximately 1 billion US dollar per year since the early 1990s [3]. Viruses and bacteria mainly cause the diseases of the shrimp. The application of antibiotics in shrimp culture can solve the problem related to the bacterial diseases. However, frequent and non-selective use of antibiotics can lead to the development of bacterial resistance and new disease development [4]. From the previous reviews and studies, Fig. 1: Schematic drawing of P. vannamei [7] we understand that most of the published reviews focused on the diseases and production aspects of P. Penaeus vannamei lives in tropical marine habitats. vannamei [3 - 6] .However, the biology of this species is The adults of this species live and spawn in the Ocean. neglected. For better health management and production However, the larvae and juveniles are usually found in systems of this shrimp species, it is paramount to have inshore water areas such as coastal estuaries, lagoons or basic and solid knowledge of the biology of P. vannamei. mangrove areas. The females of P. vannamei grow faster However, there are limited reviews available on the compared to the male of this species. The matured female biology of the shrimp. This is, thus, we are very motivated of P. vannamei weighing 30-45 g can spawn 100, 000-250, to review of the biology of shrimp for efficient health 000 eggs. The life cycle of the white leg shrimp is very management and production of the shrimp. Therefore, the complex (Figure 2). The matured females of P. vannamei objective of this paper is to review of the biology of white spawn their eggs in the offshore waters [8]. The leg shrimp, P. vannamei. fertilization occurs in the external environment. The hatching process of the egg occurs after spawning and Biology of Penaeus vannamei: fertilization. After hatching process, the first larval stage, Taxonomy: The white leg shrimp, Penaeus vannamei [7] nauplii are released from hatching eggs. Nauplii feed on belongs to the phylum Arthropoda, which is defined by the internal reserves of egg yolk sack. The nauplii are having joined appendages and an exoskeleton or cuticle developed in different larval stages by the help of which is periodically shed [8]. The taxonomic metamorphosis. The next stages of larvae include classification of P. vannamei as described by several Protozoea, mysis and early stage of post larvae, authors [9 - 11] is as follows: respectively. The Protozoea feed on phytoplankton (unicellular algae), while mysis and early stage of post Domain: Eukarya larvae feed mainly on zooplankton (rotifer, Artemia and Kingdom: Animalia copepods). The early post larvae develop into a late post Phylum: Arthropoda larvae stage, which is very similar in morphology to the Subphylum: Crustacea juvenile and adult stages [12, 13]. Class: Subclass: Eumalacostraca External Morphology of P. vannamei: The penaeid shrimp Superorder: Eucarida contains 19 pairs of body segments (Figure 3). The first Order: five pairs of the segments make up the cephalon part. Suborder: The next eight pairs of the segments are located in the Super family: Penaeoidea thorax part. The last six pairs of the segments are found in Family: the abdomen. The head and thorax are fused together to Genus: Penaeus form cephalothorax (pereon). The exoskeleton of the Species: Penaeus vannamei cephalothorax covers the gills and it also protects the gill chamber (branchiostegite). The abdomen (pleon) of the Life Cycle of P. vannamei: The white leg shrimp, penaeid shrimp has six pairs segments. The swimming P. vannamei (Figure 1) is native to the Eastern Pacific legs (pleopods) are located on the first five pairs of the coast of Mexico and Northern Peru. This species likes segments of the abdomen. The last pair of the segment is areas where water temperatures are usually over 25°C the the tail fan. This segment comprises of 2 pairs of uropods whole year. The female shrimp grow faster than males. and the telsons which can help a shrimp to jump quickly They shrimp like muddy bottom areas [1]. backwards in the case of hazardous [14].

6 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

Fig. 2: The production life cycle of P. vannamei [1]

Fig. 3: External morphology of P. vannamei [2]

7 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

Fig. 4: The digestive tract of P. vannamei [2] Key: E= Esophagus, GM=gastric mill, HP= hepatopancreas, MG=mid gut, HG=hind gut and A= anus

Internal Morphology of P. vannamei Digestive System: The digestive tract of the penaeidae the gut from mechanical damage, pathogens, toxins and shrimp is divided into three regions (Figure 4): namely, other harmful chemicals [20]. The hepatopancreas covers foregut, midgut and hind gut. The embryological origin of a large part of the cephalothorax and it is the master the epithelial cells in the foregut and hindgut are derived digestive gland. The main functions of this gland are the from the ectodermal and covered with a cuticle. However, synthesis and secretion of digestive enzymes, absorption the epithelial cells of the midgut are derived from of nutrients, metabolism of lipid and carbohydrate and endodermal origin. This region of the gut shows a lack of calcium absorption [17, 18]. cuticle; however, it is lined by a protective peritrophic The hindgut is the terminal part of the digestive tract membrane [15]. of the shrimp. The epithelium of this gut is lined with The foregut starts at the mouth which is located non-calcified cuticle which links the midgut with the anus. rostroventrally in the cephalothorax region. The rostral The hindgut starts behind the posterior midgut cecum and part of the foregut is covered by the labrum and mouth bacterial growth has been reported in the hindgut [21]. parts. The appendages around the mouth are packed with Furthermore, several authors have demonstrated that mucus secreting glands [16, 17]. The oesophagus is the anus is lined with a thick and calcified cuticle and it located dorsally to the stomach and it divides the stomach opens onto the surface of the exoskeleton below the into two parts: the anterior and posterior chamber. telson [22, 23]. The anterior chamber serves as a gastric mill and muscles in this chamberhelp the wall of the stomach to move Respiratory System: Gills are the respiratory organs in easily. The presence of cuticular tooth-like structures in shrimp and other . They are attached to the the anterior chamber functions for the grinding of the pereon by a tubular structure. The genus Penaeus has food. The posterior chamber serves as a ballow with a pairs of gills, which are enclosed in a branchial chamber sieve in it. Normally, food passes dorsally over the sieve [9, 24]. The gill structure is classified as dendrobranchiate which is composed of uniformly spaced cuticular hairs. gills in the shrimp, while it is trichobranchiategills in other Both liquid and solid particles less than 1 µm can pass via decapods [25]. The dendrobranchiate gill (Figure 5A, B) the sieve (in the ventral direction) to the hepatopancreas. has paired lateral branches arising from the central Larger particles pass to the midgut [17, 18]. branchial axis, with a series of subdivided secondary rami The mid gut extends from the stomach in the coming off each lateral branch (Figure 5B). The cephalothorax to the hind in the 6th segment of the trichobranchiate gill (Figure 5C, D) is characterized by abdomen (pleon). This gut is composed of the anterior serial tubular rami from the central brachial axis. No midgut ceca, posterior midgut, hepatopancreas (digestive secondary rami are ever present as in dendrobranchiate gland) and intestine (midgut trunk) [18, 19]. The gills [26]. Gills of the shrimp have a tree like shape which peritrophic membrane, epithelium, basal lamina, consists of an axis with a series paired branches along its haemocyte layer (granulocytes) and a connective layer of length. Each branch of the gills gives rise to vertical the circular and longitudinal muscles and the outer intima filaments. The longitudinal septum separates the primary are composedof the wall of the midgut [19]. The afferent vessel from the primary efferent vessel. The peritrophic membrane is produced by the epithelial cells primary afferent vessel supplies blood to the axis of the in the midgut. The function of the membrane is to protect gills. The secondary afferent vessels direct the blood into

8 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

Fig. 5A: Dendrobranchiate gills of the genus Penaeus, B: close up of Dendrobranchiate of gill lamellae of the genus Penaeus, C: Trichobrachiate gills of the genus Stenopus, D: close up of Trichobrachiate of gill lamellae of the genus Stenopus [26] the paired branched and they also supply blood to the clotting mechanism is regulated by clotting proteins. individual filaments. The gas exchange takes place in the The haemocytes are comparable to white blood cells of gill lamella. The water blood barrier is found in each the vertebrate. The haemolymph is responsible for filament and it consists of cuticle, epithelium and basal transport of different nutrients, salt, water and oxygen to lamina. The barrier involves in allowing rapid diffusion of all tissues. It also plays a major role in the excretion of gases. The efferent vessel carries oxygenated blood from metabolic waste, excess salts and water [26, 32]. The the round tip of the filaments to the heart [27]. In addition compositions of haemolymph of shrimp are proteins, to the respiratory functions, the gillsalso havethe other lipoproteins, glycoprotein, free amino acids, electrolytes main roles such as salt and water balance, ammonia and metals [33]. Several authors have reported that the excretion and calcium uptake [24, 28, 29]. The gills are also haemocyanin accounts for 87% of the total haemolymph involved in the capturing and the elimination of foreign proteins in P. vannamei [34, 35]. In addition to oxygen particles in the haemolymph particularly bacteria [30]. transport, haemocyanin proteins also have other functions such as energy storage [36, 37] and immune Circulatory System: The circulatory system of shrimp defense [38]. consists of a heart, associated conduits and haemal Haematopoietic tissues are located dorsal from of the sinuses, haematopoetic tissues and lymphoid organs stomach and the tissues often continue towards the (Figure 6). Penaeids and other have a antennal gland [22, 39]. The Haematopoietic tissues are semi-open circulatory system. The heart is located made up of lobules of tissue, which produce the dorsally in the cephalothorax. The haemolymph vessels haemocytes [40]. Therefore, haemocytes are thought to be leave the heart. Then, the vessels branch into several derivedfrom two main cell lines where one non-granular times before they end in the sinuses, which are present cell and other cell line produces a granular cell. Four main throughout the body. The haemolymph passes first cellular types were described in the haematopoietic through the gills and then after, it returns to the heart by tissues of P. monodon [41]. These cells are type I cells means of efferent vessels [23, 31]. The haemolymph of (other haemocyte cells), type II cells (non-granular shrimp and other Crustacean lack the red blood cells or haemocyte cells), type III cells (granular haemocyte) [32] platelets as seen in vertebrate blood. Oxygen is and type IV cell (interstitial cell) [41]. The other studies by transported by free flowing hemocyanin proteins and the Dantas Lima et al. [42] have also separated five main

9 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

Fig 6. Schematic drawing of the circulatory system and associated organs in P. vannamei [46]

Fig. 7: Schematic drawing of the regions of the brain [26] subpopulations of haemocytes from P. vannamei by These glands include (1) neuroendocrine glands such as iodixanol density gradient centrifugation. These X-organ/sinus gland complex, postcommisural and subpopulations are (i) subpopulation 1, (ii) subpopulation pericardial organs and (2) the epithelial endocrine glands, 2, (iii) subpopulation 3, (iv) subpopulation 4 and (v) which include the Y-organ, mandibular organ and subpopulation 5 [42]. The lymphoid organs are a pair of androgenic glands [16, 47]. nodular structures which are located on a major artery at the craniodorsal surface of the hepatopancreas [22, 40]. Reproductive System: In penaeids shrimp, the The primary functions of these organs are the elimination reproductive tract of males includes paired testes, a vas of bacteria and infected virus-infected cells [41, 43, 44]. deferens and ejaculatory ducts or terminal ampoules [26, 48]. The testes are multi-lobed and each lobe is made Nervous System: The nervous system of shrimp and up of convoluted seminiferous tubule which surrounded other crustacean is composed of the brain which is by haemal sinuses. The spermatids are produced in the located dorsally in the cephalothorax and it is connected spermatogonia which are differentiated from germinal cells to the ventral cord by two connectives which pass around in the testes [48]. The spermatozoa (spermatids) of the esophagus [26]. The brain is composed of three decapods are non-motile and non-flagellate compared to regions (Figure 7), namely: protocerebrum, the other invertebrates [26]. The maturation of the deuterocerebrum and tritocerebrum [26]. In shrimp, the spermatids takes place in the different regions of the paired thoracic and abdominal ganglia are medially fused, seminiferous tubule. The petasma and appendix masculine but the paired connectives separate the ganglia of of the male abdominal appendages are used for adjacent segments from the thoracic and abdominal delivering sperm cells to the external thelycum of the ganglia [26, 46]. The central nerve is regulated via female which is located between the bases of the fifth neurohormones secreted by two main divisions of glands. walking legs [8].

10 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

The reproductive tract of the female is composed of labyrinth, proximal and distal tubules and bladder [16, 22, paired ovaries which extend from the mid thorax to the 26]. Embryologically, the end sac is derived from the posterior end of the pleon and oviducts which terminate mesoderm. The wall of coelomosac is composed of a adjacent to a single thelycum. The oviducts play a role in single layer of podocytes which is lined by a basal lamina. leading the eggs to the gonophores. The eggs exit to the The function of podocytes is ultra filtration, which has a external environment via the gonophore which is located similar role with that of the vertebrate glomerular nephron on the 3rd walking legs (pereiopods) [26]. In shrimp, the [16]. thelycumis used for receiving the spermatophores and it The labyrinth (Figure 9B-G) is made up of a network is located between the bases of the 4th and 5 th walking legs of coiled simple columnar epithelial cells. It has two cell of the female shrimp. The white leg shrimp has an open types: namely, (i) labyrinth I cells characterized by thelycum system. Thus, the spermatophore should be having tall columnar cells with basal nuclei and apical placed on the thelycum by the male within hours of membrane and (ii) labyrinth II which has cells with shorter, spawning. The presence of spermatophore on a female is with central nuclei, brush border and larger vacuoles. the sign of mating [8]. In shrimp, the labyrinth is located and scattered throughout the anterior part of the pereon. The labyrinth Integument System: Integument of the penaeid shrimp is involved in the movement of ions and reabsorption of forms an exoskeleton (cuticle) which covers all the proteins. The proximal and distal tubules serve as the external surfaces and some of the insides as well. It conduit between the labyrinth and the bladder [16]. protects the body of the shrimp; the integument is a The bladder is a large multi-lobed structure which can physical barrier which prevents the entrance of pathogens be used as a reservoir for urine storage. It may also have into the body [49, 50]. The histological structure of the a role in the final urine modification [26]. The bladder has cuticle consists of outer epicuticle, exocuticle, endocuticle epithelial cells similar to the labyrinth [16]. The urinary and the inner membranous layer [51]. The cuticle is a bladder is connected to the nephropore (Figure 9A) via a mineralized tissue which is composed of different ureter [22, 56]. The nephropore is a cuticular wave like histological structures such as connective tissues, split protruding at the base of the second antennae, proteins, carbohydrate, lipid and calcium salt [52, 53]. which is controlled by a sphincter muscle system [57]. However, the compositions of the cuticle are affected by The haemolymph can supply oxygen and nutrients to the the different moulting cycles [51]. Moulting is a complex base of the epithelial cells of the labyrinth with the help of process for the growth by which a shrimp sheds the old capillaries. Haemolymph bathes the antennal glands and cuticle and produces a new one. Several authors have it flows to the hemocoel through a series of channels in also demonstrated that the moulting cycle can influence the glands. Different authors have reported that the urine other functions such as development, growth, of P. vannamei remains isosmotic with that of regeneration, hematopoietic and defenseresponse [35]. haemolymph [35, 58]. The known main functions of the Several authors have reported that there are five major antennal glands are osmotic and ionic regulations, moulting stages. These are namely: earlypost-moult and maintenance of haemolymph volume, gastric acidification late post-molt stages (A and B), inter-moult stage (C), and heavy metal detoxification, excretion of nitrogenous early pre-moult and late pre-moult stages (D1 and D2) and waste (ammonia and urea) and storage of urine [21, 35, 58]. moulting stage (E) [35, 54]. Moulting is controlled by neurohormones. However, it is also affected by Immune System of P. vannamei: The innate immune environmental factors like temperature, light and salinity. system of the crustacean mainly reacts against These factors can also influence metabolism and pathogenic microorganisms. However, some authors neurohormones production [55]. hypothesize that crustaceans are also capable of exhibiting a specific immune response via antibody Excretory System: The antennal glands are the main independent mechanisms [59]. For example, when shrimp excretory organs of shrimp and other crustaceans and are injected with antigens, these vaccines like treatments these glands are located at the base of secondary somewhat temporarily increased resistance or tolerance antennae. The excretory (nephropore) exists on the coxa the pathogen from which the antigen was originally of the antenna. These glands are composed of four derived [60]. The shrimp’s innate immune system has regions (Figure 8): namely, end sac (coelomosac), both cellular and humoral immunity components to fight

11 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

Fig. 8: Schematic drawing of the antennal gland of the shrimp [26]

Fig. 9: Ultrastructural features of the antennal gland: A: nephropore (arrow) at base of the antennal pendicle, B: Labyrinth region of the antennal gland; arrow indicates region that exists to the proximal tubule, C: close up of the convoluted cell layers of the labyrinth, D: region of labyrinth that leads to the proximal tubule, E: ultrastructure of the labyrinth cells; note centrally located nucleus (n), F: close up of brush border labyrinth cells; note mitochondria (m) and long microvilli, G: close up of mitochondria packed within the basal lamina indicated in arrow E [26] invading microbes [61]. The cellular immunity involves Of all the cellular components of the crustacean nodulation, melanization, encapsulation and innate immune system, the cellular melanotic phagocytosis, while the humoral immune component encapsulation is the most efficient mechanism against includes antimicrobial peptides, anti-oxidant defense foreign antigens. The complex melanization cascade enzymes, proteinase inhibitors, prophenoloxidase- requires the circulating haemocytes and several activating system (proPO system), antimicrobial peptides, associated proteins of the prophenoloxidase (proPO) lectins, reactive oxygen species (ROS), lysosomal activating system [64]. This system is one of the more enzymes, blood clotting cascade and agglutinins and potent humoral components of many crustaceans. The cytokine like factors [61, 62]. The immune system of proPO activating system plays a major role in non-self shrimp can involve in different functions such as recognition that occurs in the innate immune response recognizing foreign antigens, killing different types of through accompanying with the cellular responses. pathogens and limiting the host’s tissue damage [63]. These responses include the attraction of haemocytes

12 World J. Fish & Marine Sci., 10 (2): 05-17, 2018 which leads to initiation of phagocytosis, melanization, CONCLUSION cytotoxic reactant production, encapsulation, the formation of nodules and capsules [64]. The proPO Shrimp aquaculture plays a significant role in the activating system also has different roles in other humoral world economy. The most of the aquaculture shrimp responses such as reactive oxygen species (ROS), contribution has come from P. vannamei which accounts antimicrobial peptides and lysozymes [65, 66]. 80% of the whole shrimp production. The life cycle of this Based on the type and size of cytoplasmic granules species is very complex and it usually takes around 1.5 present in the haemolymph cell, the crustaceans have years to complete the whole life cycle of P.vannamei. three different types of haemocytes subpopulations, However, the life cycle of this shrimp takes around 6 namely: hyaline cells, semi-granular and granular months to reach a market size for human consumption. haemocytes [31, 67]. However, the recent studies The external morphology of P.vannamei is well described and understood. However, there is no solid knowledge of conducted by [42] have categorized the subpopulations the internal morphology and physiology of this species of haemocytes from the P. vannamei into five groups of particular in areas of nervous system development and cells. According to this classification, the cell types are structure. Further, there is limited information on the (i) subpopulation 1, (ii) subpopulation 2, (iii) understanding of behavior and feeding habits of this subpopulation 3, (iv) subpopulation 4 and (v) animal. Therefore, further studies are needed in future to subpopulation 5 [42]. The hyaline cells account for 5-20% have solid knowledge of internal morphology and of the haemocyte population. These cells are ovoid to physiology, natural behaviour and feeding habits of P. spindle shaped and they are smaller than the other three vannamei in order to improve the production and health types. The semi-granular cells represent (60-75%) of management systems. haemocyte subpopulations. The remaining granulocytes cells represent around 10-25% of the haemocyte REFERENCES population [68]. The detailed functions of the different 1. FAO, 2016. FAO Statistical Yearbook: Fishery and subpopulations of shrimp haemocyte have not yet been Aquaculture Statistics. The organization of Food and well described. However, some studies indicated that the Agriculture of the United Nations, hyalinocytes perform the phagocytosis role by releasing Rome.http://www.fao.org/3/478cfa2b-90f0-4902-a836- anti-microbial and pro-inflammatory compounds [42]. 94a5dddd6730/i3740t.pdf. The semi-granular cells perform different functions such 2. FAO, 2012. FAO Statistical Yearbook: Fishery and as encapsulation [69], phagocytosis [70], storage and Aquaculture Statistics. The organization of Food and release of the proPO system [71] and cytotoxicity role [72]. Agriculture of the United Nations, These cells take up and digest the foreign particles inside Rome.http://www.fao.org/3/478cfa2b-90f0-4902-a836- the phagolysosomes by using respiratory burst 94a5dddd6730/i3740t.pdf. mechanisms which produce lysozymes and reactive 3. Flegel, T.W., D.V. Lighter, C.F. Lo and L. Owens, oxygen species. The granulocytes are the main source of 2008. Shrimp disease control: past, present and the proPO system which plays an important role for future. In: Bondad-Reantaso, MG, Mohan, CV, encapsulation and nodulation during combat of fungi and Crumlish, M., Subasinghe, R.P., (Eds.), Diseases in Asian aquaculture volume 6. Manila, Philippines: bacteria, respectively [73]. Several studies are mainly Fish Health Section. Asian Fisheries Society, focused on antifungal, anti-parasites and anti-bacterial 6:355-378. responses rather than anti-viruses responses [65, 66]. 4. Rodgers, C.J. and M.D. Furones, 2009. Antimicrobial However, the RNA interference (RNAi) is one of the few agents in aquaculture: practice, needs and issues. well-described pathways which play a major role in the Ciheam.Options Mediterraneennes, 86: 41-59. crustacean antiviral immune response [74]. The other 5. Stentiford, G.D., J.R. Bonami and V. Alday-Sanz, 2009. studies by [75] reported the discovery of an antiviral A critical review of susceptibility of crustaceans to gene, PmAV from P. monodon shrimp. This gene may Taura syndrome disease, Yellow head disease and provide a clue to explain the innate antiviral immunity of White spot disease and implications of inclusion of shrimp and it may be helpful to control shrimp viral these diseases in European legislation. Aquaculture, disease [75, 76]. 291: 1-17.

13 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

6. Thuong, V.K., V. Tuan, W. Li, P. Sorgeloos, 18. Icely, J.D. and J. Nott, 1992. Digestion and P. Bossier and H.J. Nauwynck, 2016. Per os infectivity absorption: digestive system and associated organs. of white spot syndrome virus (WSSV) in white In: F.W., Harrison, Humes, A.G. (Eds.), the legged shrimp (Litopenaeus vannamei) and role of Microscopic anatomy of invertebrates, volume 10, peritrophic membrane. Veterinary Research, 47: 39. Decapod Crustacea. Wiley-Liss, Inc., New York, 7. Lovett, D.L. and D.L. Felder, 1989. Ontogeny of the pp: 147-201. gut morphology in the white shrimp Penaeus 19. Martin, G.G. and A. Chiu, 2003. Morphology of the setiferus (Decapoda, Penaeidae). Journal of mid gut trunk in the penaeid shrimp Sicyoniain Morphology, 201: 253-272. gentis: highlighting novel pore particles and fixed 8. Bailey-Brock, J.H. and S.M. Moss, 1992. Penaeid haemocytes. Journal of Morphology, 258: 239-248. taxonomy, biology and Zoogeography. In: A.W., 20. Lehane, M.J., 1997. Peritrophic matrix structure Fast, Lester, L.J. (editors). Marine shrimp culture: and function. Annual Reviews in Entomology, principles and practices. Amsterdam Elsevier Science 42: 525-550. Publishers, 23: 9-27. 21. Wheatley, M.G., 1999. Calcium homeostasis in 9. Perez-Farfante, I. and B. Kenslev, 1997. Penaeoid and Crustacean: the evolving role of branchial, renal, sergestoid shrimps and praws of the world: Keys and digestive and hypodermal epithelia. Journal of dignoses for the families and genera, volume 175, Experimental Zoology, 283: 620-640. Paris, France, pp: 10-55. 22. Bell, T.A. and D.V. Lightner, 1988. A handbook of 10. Martin, J.W. and G.E. Davis, 2001. An updated normal penaeid shrimp histology. World aquaculture classification of the recent crustacean science series society, Baton, Louge, Louisiang, USA, pp: 144. number 39. Natural History Museum of Los Angeles 23. Dall, W., B.J. Hill, P.C. Rothlisberg and D.J. Sharpies, Country, Los Angeles, pp: 124. 1990. The biology of the Penaeidae. In: Advances in 11. Ma, K.Y., T.Y. Chan and K.H. Chu, 2011. Refuting the Marine Biology, Volume 27, Academic Press, six-genus classification of Penaeus s.l. London, pp: 489. (Dendrobranchiata, Penaeidae): A combined analysis 24. Taylor, H.H. and E.W. Taylor, 1992. Gills and lungs: of mitochondrial and nuclear genes. Zoologica exchange of gases and ions. In:Harrison, FW, Humes, Scripta, 50: 498-508. AG (Eds.). Microscopic anatomy of invertebrates, 12. Bray, W.A. and A.L. Lawrence, 1992. Reproduction volume 10 Decapod Crustacea. Wiley-Liss, Inc., New of Penaeus species in captivity. In: A.W., Fast, York, pp: 203-293. Lester, L.J., editors. Marine shrimp culture: principles 25. McLaughlin, P.A., 1983. Internal anatomy. In: Mantel, and practices. Amsterdam, Elsevier Science I.H. (Eds.), the biology of crustacean, volume 5. Publisher, 23: 93-170. Internal anatomy and physiological regulation, 13. Wickins, J.F. and D.C. Lee, 2002. Crustacean farming, Academic press, New York and London, pp: 1-52. ranching and culture. Blackwell Science, UK, pp: 446. 26. Felgenhauer, B.E., 1992. Internal anatomy and 14. Ruppert, E.E. and R.D. Barnes, 1994. Invertebrate integumentary structures. An overview In: Harrison, zoology, 6th edition. Saunders College Publishing, F.W., Humes, A.G. (Eds.), Microscopic anatomy of Orlando, Florida, USA, pp: 1056. invertebrates, volume 10, Decapod Crustacea. Wiley- 15. Lovett, D.L. and D.L. Felder, 1990a. Ontogenetic Liss, Inc., New York, pp: 45-75. change in the digestive enzyme activity of larval 27. Young, J.H., 1959. Morphology of the white shrimp of andpost-larval white shrimp Penaeus setiferus Penaeus setiferus (Linnaeus 1758). US Fisheries and (Crustacea, Decapoda, Penaeidae). Biological Wildlife Service. Fish Bull, 59: 1-168. Bulletin, 178: 144-159. 28. Ahearn, G., J.M. Duerr, Z. Zhuang, R.J. Brown, 16. Fingerman, M., 1992. Glands and secretion. In: A. Aslamkhan and D.A. Killebrew, 1999. Ion Harrison, F.W., Humes, AG. (Eds.), Microscopic transport processes of Crustacean epithelial cells. anatomy of invertebrates, volume 10. Decapod Physiological and Biochemical Zoology, 72: 1-18. Crustacea, Wiley-Liss Inc., New York, pp: 345-394. 29. Bauer, R.T., 1999. Gill cleaning mechanisms of a 17. Ceccaldi, H., 1998. A synopsis of the morphology dendrobranchiate shrimp, Rimapenaeus similis and physiology of the Digestive system of Some (Decapoda, Penaeidae): description and Crustacean species studied in France. Journal of experimental testing of function. Journal of Reviews in Fishery Science, 6: 13-39. Morphology, 242:125-139.

14 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

30. Martin, G.G., M. Quigley, M. Quintero and 41. Van de Braak, C.B., M. Botterblom, W. Liu, H. Khosrovian, 2000. Elimination of sequestered N. Taverne, W.P. van der Knaap and J.H. Rombout, material from the gills of decapod Crustaceans. 2002a. The role of the haematopoietic tissue in Journal of Crustacean Biology, 20: 209-217. hemocyte production and maturation in the black 31. Bauchau, A.G., 1981. Crustaceans. In: Ratcliffe, N.A., tiger shrimp (Penaeus monodon). Fish and Shellfish Rowley, A.F., (editors), Invertebrate blood cells Immunology, 12: 253-272. volume 2, Academic Press, London, pp: 385-425. 42. Dantas Lima, J.J., M.Corteel, K.Grauwet, N.T.T. An, 32. Hose, J.E., G.G. Martin, V.A. Nguyen, J. Lucus and P. Sorgeloos and H.J. Nauwynck, 2013. Separation of T. Rosenstein, 1987. Cytochemical features of shrimp Penaeus vannamei hemocyte subpopulations by hemocytes. Biological Bulletin, 173: 178-187. iodixanol density gradient centrifugation. 33. Shimizu, C., H. Shike, K. Klimpel and J. Burns, 2001. Aquaculture, 408-409: 128-135. Hemolymph analysis and evaluation of newly 43. Duangsuwan, P., I. Phoungpetchara, Y. Tinikul, formulated media for culture of shrimp cells (Penaeus J. Polijaroen, C. Wanichanon and P. Sobhon, 2008. stylirostris). Journal of Morphology, 37: 322-329. Histological and three dimensional organisations of 34. Figueroa-Soto, C.G., A.M. Calderon, Dela Barca, lymphoid tubules in normal lymphoid organ of M. Vazquez, I. Higuera-Ciapara and Yepiz-G. Penaeus monodon. Fish and Shellfish Immunology, Plascencia, 1997. Purification of hemocyanin from 24: 426-435. white shrimp Penaeus vannaemi (Boone) by immobilized metal affinity chromatography. 44. Rusaini, P. and L. Owens, 2010. Insight into the Comparative Biochemistry Physiology, 117: 203-208. lymphoid organ of penaeid prawns: A review. Fish 35. Chen, L.L., H.C. Wang, C.J. Huang, S.E. Peng, and Shellfish Immunology, 29: 367-377. Y. Chen, S.J. Lin, W. Chen, C.F. Dai, H.T. Yu, 45. Escobedo-Bonilla, C.M., L. Audoorn, M. Wille, C.H. Wang, C.F. Lo and G.H. Kou, 2002a. V. Sanz, P. Sorgeloos, M.B. Pensaert and H.J. Transcriptional analysis of the DNA polymerase Nauwynck, 2006. Standardized white spot gene of shrimp white spot syndrome virus (WSSV). syndrome virus inoculation procedures for Journal of Virology, 301: 136-147. intramuscular or oral routes. Diseases of Aquatic 36. Sannchez, A., C. Pascual, A. Sanchez, F. Vargas- Organisms, 68: 181-188. Albores, G. Le Moullac and C. Rosas, 2001. 46. Govind, C.K., 1992. Nervous system. In: Harrison, Hemolymph metabolic variables and immune FW, Humes, AG. (Eds.), Microscopic anatomy of response in Litopenaeus setiferus adult males: the invertebrates, volume 10. Decapod Crustacea, Wiley- effect of acclimation. Aquaculture, 198: 13-28. Liss, Inc., New York, pp: 395-438. 37. Pascual, C., G. Gaxiola and C. Rosas, 2003. Blood 47. Diwan, A.D., 2005. Current progress in shrimp metabolites and hemocyanin of the white leg shrimp, endocrinology: A review. Indian Journal of Litopenaeus vannamei: the effect of culture Experimental Biology, 43: 209-223. conditions and a comparison with other crustacean 48. Krol, R.M., W.E. Hawkins and R.M. Overstreet, 1992. species. Marine Biology, 142: 735-745. Reproductive components. In: Harrison F.W., Humes, 38. Destomieux-Garzon, D., D. Saulnier, J. Garnier, A.G. (Eds.), Microscopic anatomy of invertebrates, C. Jouffrey, P. Bulet and E. Bachere, 2001. Antifungal volume 10, Decapod Crustacea. Wiley-Liss, Inc., New peptides are generated from the C- terminus of shrimp York, pp: 295-343. haemocyanin in response to microbial challenge. 49. Armstrong, P.B. and J.P. Quigley, 1999. Alpha- Journal of Biological Chemistry, 276: 70-77. macroglobulin: an evolutionarily conserved arm of 39. Martin, G.G. and J.E. Hose, 1992. Vascular elements the innate immune system. Developmental and and blood (hemolymph). In: Harrison, F.W., Humes, Comparative Immunology, 23: 375-390. A.G. (Editors), Microscopic anatomy of invertebrates, 50. Tincu, A.J. and S.W. Taylor, 2004. Antimicrobial volume 10, Decapod Crustacea. Wiley-Liss, Inc., New York, pp: 45-75. peptides from marine invertebrates. Antimicrobial 40. Martin, G.G., J. Kim and J.E. Hose, 1987. Structure Agents and Chemotherapy, 48: 3645-3654. ofhemaotopoietic nodules in the ridgeback prawn, 51. Roer, R. and R. Dillaman, 1984. The structure and Sicyoniain gentis: light and electron microscopy calcification of the crustacean cuticle. American observations. Journal of Morphology, 192: 193-204. Zoology, 24: 893-909.

15 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

52. Compere, P., C. Jeuniaux and G. Goffinet, 2004. The 62. Cerenius, L., S.I. Kawabata, B.L. Lee, M. Nonaka and integument: morphology and biochemistry. In: K. Soderhall, 2010. Proteolytic cascades and their Forest, J., Schram, F.R., von Vaupel Klein, J.C. (Eds.), involment in invertebrate immunity. Trends in The Crustacea: revised and updated from the Traité Biochemical Sciences, 35: 575-583. de Zoologie, volume 1. Koninklijke Brill, Leiden, the 63. Beutler, B., 2004. Innate immunity: an overview. Netherlands, pp: 59-144. Molecular Immunology, 40: 845-859. 53. Promwikon, W., P. Kirirat, P. Intasaro and 64. Sritunyalucksana, K. and K. Soderhall, 2000. The B.Withyachumnarnkul, 2007. Changes in integument proPO and clotting system in crustaceans. histology and protein expression related to the Aquaculture, 191: 53-69. molting cycle of the black tiger shrimp, Penaeus 65. Bachere, E., E. Mialhe and J. Rodriguez, 1995. monodon. Comparative Biochemistry and Identification of defense effectors in the haemolymph Physiology, part B, 148: 20-31. of crustaceans with particular reference to the shrimp 54. Corteel, M., J. Dantas-Lima, V.V. Tuan, M. Wille, Penaeus japonicus (Bate): prospects and V. Alday-Sanz, M.B. Pensaert, P. Sorgeloos and applications. Fish and Shellfish Immunology, H.J. Nauwynck, 2012. Moult cycle of laboratory 5: 597-612. raised Penaeus (Litopenaeus) vannamei and Penaus 66. Sritunyalucksana, K., L. Nielson, J. Srisala, K. McColl monodon. Aquaculture International, 20: 13-18. and T.W. Flegel, 2006. Comparison of PCR 55. Kaestner, A., 1970. Crustacean. In: Invertebrate testing methods for white spot syndrome virus zoology, Volume III. Inter science publishers, pp: 523. (WSSV) infections in penaeid shrimp. Aquaculture, 56. Khodabandeh, S., C. Blasco, G.C. Charmantier, 255: 95-104. E. Grousset and M.C. Daures, 2005. Ultra structural 67. Johansson, M.., P. Keyser, K. Sritunyalucksana and studies and Na++ K -ATPase immunological in the K. Soderhall, 2000. Crustacean haemocytes and urinary glands of the lobster Homarus americanus haematopoiesis. Aquaculture, 191: 45-52. (crustacean, Decapoda). Journal of Histochemistry 68. Martin, G.G. and B.L. Graves, 1985. Fine structure and and Cytochemistry, 53: 1203-1214. classification of shrimp hemocytes. Journal of 57. Bushman, P.J. and J. Atema, 1996. Nephropore Morphology, 185: 339-348. rosette glands of the lobster Homarus americanus: 69. Kobayashi, M., M.W. Johansson and K. Soderhall, possible sources of urine pheromones. Journal of 1990. The 76 Kd Cell Adhesion Factor from Crayfish Crustacean Biology, 16: 221-231. Hemocytes Promotes Encapsulation In vitro. Cell and 58. Lin, S.C., C.H. Liou and J.H. Cheng, 2000.The role of Tissue Research, 260: 13-18. the antennal glands in ion and body volume 70. Thornqvist, P.O., M.W. Johansson and K. Soderhall, regulation of cannulated Penaeus monodon reared in 1994. Opsonic activity of cell-adhesion proteins various salinity conditions. Molecular and and Beta-1, 3-glucan binding-proteins from 2 Integrative Physiology, 127: 121-129. crustaceans. Developmental and Comparative 59. Chambers, M.C. and D.S. Schneider, 2012. Pioneering Immunology, 18: 3-12. Immunology: insect style, curr. opin. Immunology, 71. Johansson, M. and K. Soderhall, 1985. Exocytosis of 24: 10-14. prophenoloxidase activating system from crayfish 60. Powel, A., E.C. Pope, F.E. Eddy, E.C. Roberts, haemocytes. Journal of Comparative Physiology B: R.J. Shields, M.J. Francis, P. Smith and S. Topps, Biochemical, Systemic and Environmental 2011. Enhances the immune defenses in pacific Physiology, 156: 175-181. white shrimp shrimp (P. vannamei) post exposure to 72. Soderhall, K., A. Wingren, M.W. Johansson and a vibrio vaccine. Journal of Invertebrates K. Bertheussen, 1985. The cytotoxic reaction of Patholology, 107: 95-99. hemocytes from the freshwater crayfish, Astacus 61. Bachere, E., Y. Gueguen, M. Gonzalez, J. De Lorgeril, astacus. Cellular Immunology, 94: 326-332. J. Garnier and B. Romest and, 2004. Insights into the 73. Hose, J. and G. Martin, 1989. Defense functions of anti-microbialdefense of marine invertebrates: the granulocytes in the ridgeback prawn penaeid shrimps and the oyster Crassostrea gigas. ingentis. Journal of Invertebrate Pathology, Immunology Review, 198: 149-168. 53: 335-346.

16 World J. Fish & Marine Sci., 10 (2): 05-17, 2018

74. Bartel, D.P., 2004. Micro RNAs: genomics, 76. Tassanakajon, A., P. Supungul, K. Somboonwiwat biogenesis, mechanism and function. Cell, and S. Tang, 2013. Discovery of immune molecules 116: 281-297. and their functions in shrimp immunity. Fish and 75. Luo, T., X. Zhang, Z. Shao and X. Xub, 2003. PmAV, Shellfish Immunology, 34: 954-967. a novel gene involved in virus resistance of shrimp Penaeus monodon. FEBS Letters, 551: 53-57.

17