biology of white leg shrimp, penaeus vannamei: review2)18/1.pdfworld journal of fish and marine...

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

Corresponding Author: Hailu Dugassa, Van Den Nestlaan 104, 2520 Broechem, Belgium. 5

Biology of White Leg Shrimp, Penaeus vannamei: Review

Hailu Dugassa and De Gyrse Gaetan1 2

Van Den Nestlaan 104, 2520 Broechem, Belgium1

Salisburylaan 133, 9820 Merelbeke, Belgium2

Abstract: Shrimp aquaculture plays a significant role in the world economy. According to the information ofthe Food and Agriculture Organization (FAO) of the United Nations, marine and brackish water shrimp cultureproductions have expanded from less than 10, 000 metric tonnes in 1970 more than 4, 000, 000 metric tonnes in2014. 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 theseyears, the annual economic losses due to disease were estimated to be approximately 1 billion US dollar per yearsince the early 1990s. Viruses and bacteria mainly cause the diseases of the shrimp. Hence, most of thepublished reviews focused on the diseases and production aspects of P. vannamei. However, the biology ofthis species is neglected during the last two decades. For better production and health management systemsof 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 reviewof the biology of the shrimp for efficient health management and production of the shrimp. The life cycle of thisspecies 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 basicinternal morphology and physiology of this species. There is limited information on the understanding ofnatural behaviour and feeding habits of this animal. Therefore, further studies are needed in future to have solidknowledge of internal morphology and physiology, natural behaviour and feeding habits of P. vannamei inorder 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

Aquatic food production has transformed from which has reached 3.18 million of tonnes with anprimarily based on fisheries to the culture of increasing estimated first sale value of 12.15 billion Euros. The othernumbers of farmed species. According to the statistics of most important species are the black tiger shrimpFAO [1], the total world aquaculture production was (Penaeus monodon). The production of this speciesfound around 73.8 million tonnes in 2014. This figure has reached 0.86 million tonnes with a value of 3.22 billionalmost 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 theworld aquaculture production of crustacean was 6.9 world economy. According to the information of the Foodmillion tonnes in 2014 with an estimated total value of and Agriculture Organization (FAO) of the United32.33 billion Euros. This figure of crustacean production Nations, marine and brackish water shrimp cultureis almost increased by 7% compared to the production productions have expanded from less than 10, 000 metricfigures of 2012 (6.4 million tonnes) with a value of 27.60 tonnes in 1970 more than 4, 000, 000 metric tonnes in 2014billion Euros FAO [1]. Till now, more than 62 crustacean [1]. The most of the aquaculture shrimp contribution hasspecies have been cultured in aquaculture farms around come from Penaeus vannamei (P. vannamei) whichthe world. The mariculture contributes to 60.8% of the accounts 80% of the whole shrimp production. Althoughcrustacean production. The remaining 39.2% of the the cultivated shrimp production has rapidly increased

production from mariculture is dominated by P. vannamei

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

6

during these years, the annual economic losses due todisease were estimated to be approximately 1 billion USdollar per year since the early 1990s [3]. Viruses andbacteria mainly cause the diseases of the shrimp. Theapplication of antibiotics in shrimp culture can solve theproblem related to the bacterial diseases. However,frequent and non-selective use of antibiotics can lead tothe development of bacterial resistance and new diseasedevelopment [4]. From the previous reviews and studies, Fig. 1: Schematic drawing of P. vannamei [7]we understand that most of the published reviewsfocused 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 insystems of this shrimp species, it is paramount to have inshore water areas such as coastal estuaries, lagoons orbasic and solid knowledge of the biology of P. vannamei. mangrove areas. The females of P. vannamei grow fasterHowever, there are limited reviews available on the compared to the male of this species. The matured femalebiology 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 verymanagement and production of the shrimp. Therefore, the complex (Figure 2). The matured females of P. vannameiobjective of this paper is to review of the biology of white spawn their eggs in the offshore waters [8]. Theleg shrimp, P. vannamei. fertilization occurs in the external environment. The

Biology of Penaeus vannamei: fertilization. After hatching process, the first larval stage,Taxonomy: The white leg shrimp, Penaeus vannamei [7]belongs to the phylum Arthropoda, which is defined byhaving joined appendages and an exoskeleton or cuticlewhich is periodically shed [8]. The taxonomicclassification of P. vannamei as described by severalauthors [9 - 11] is as follows:

Domain: EukaryaKingdom: AnimaliaPhylum: ArthropodaSubphylum: CrustaceaClass: MalacostracaSubclass: EumalacostracaSuperorder: Eucarida contains 19 pairs of body segments (Figure 3). The firstOrder: Decapoda five pairs of the segments make up the cephalon part.Suborder: Dendrobranchiata The next eight pairs of the segments are located in theSuper family: Penaeoidea thorax part. The last six pairs of the segments are found inFamily: Penaeidae the abdomen. The head and thorax are fused together toGenus: Penaeus form cephalothorax (pereon). The exoskeleton of theSpecies: Penaeus vannamei cephalothorax covers the gills and it also protects the gill

Life Cycle of P. vannamei: The white leg shrimp, penaeid shrimp has six pairs segments. The swimmingP. vannamei (Figure 1) is native to the Eastern Pacificcoast of Mexico and Northern Peru. This species likesareas where water temperatures are usually over 25°C thewhole year. The female shrimp grow faster than males.They shrimp like muddy bottom areas [1].

hatching process of the egg occurs after spawning and

nauplii are released from hatching eggs. Nauplii feed onthe internal reserves of egg yolk sack. The nauplii aredeveloped in different larval stages by the help ofmetamorphosis. The next stages of larvae includeProtozoea, mysis and early stage of post larvae,respectively. The Protozoea feed on phytoplankton(unicellular algae), while mysis and early stage of postlarvae feed mainly on zooplankton (rotifer, Artemia andcopepods). The early post larvae develop into a late postlarvae stage, which is very similar in morphology to thejuvenile and adult stages [12, 13].

External Morphology of P. vannamei: The penaeid shrimp

chamber (branchiostegite). The abdomen (pleon) of the

legs (pleopods) are located on the first five pairs of thesegments of the abdomen. The last pair of the segment isthe tail fan. This segment comprises of 2 pairs of uropodsand the telsons which can help a shrimp to jump quicklybackwards in the case of hazardous [14].


7

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

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


8

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. vannameiDigestive System: The digestive tract of the penaeidae the gut from mechanical damage, pathogens, toxins andshrimp is divided into three regions (Figure 4): namely, other harmful chemicals [20]. The hepatopancreas coversforegut, midgut and hind gut. The embryological origin of a large part of the cephalothorax and it is the masterthe epithelial cells in the foregut and hindgut are derived digestive gland. The main functions of this gland are thefrom the ectodermal and covered with a cuticle. However, synthesis and secretion of digestive enzymes, absorptionthe epithelial cells of the midgut are derived from of nutrients, metabolism of lipid and carbohydrate andendodermal 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 tractmembrane [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 andpart 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 thatmucus secreting glands [16, 17]. The oesophagus is the anus is lined with a thick and calcified cuticle and itlocated dorsally to the stomach and it divides the stomach opens onto the surface of the exoskeleton below theinto two parts: the anterior and posterior chamber. telson [22, 23].The anterior chamber serves as a gastric mill and musclesin this chamberhelp the wall of the stomach to move Respiratory System: Gills are the respiratory organs ineasily. The presence of cuticular tooth-like structures in shrimp and other crustaceans. They are attached to thethe anterior chamber functions for the grinding of the pereon by a tubular structure. The genus Penaeus hasfood. The posterior chamber serves as a ballow with a pairs of gills, which are enclosed in a branchial chambersieve in it. Normally, food passes dorsally over the sieve [9, 24]. The gill structure is classified as dendrobranchiatewhich is composed of uniformly spaced cuticular hairs. gills in the shrimp, while it is trichobranchiategills in otherBoth 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 centralLarger 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). Thecephalothorax to the hind in the 6 segment of the trichobranchiate gill (Figure 5C, D) is characterized byth

abdomen (pleon). This gut is composed of the anterior serial tubular rami from the central brachial axis. Nomidgut ceca, posterior midgut, hepatopancreas (digestive secondary rami are ever present as in dendrobranchiategland) and intestine (midgut trunk) [18, 19]. The gills [26]. Gills of the shrimp have a tree like shape whichperitrophic membrane, epithelium, basal lamina, consists of an axis with a series paired branches along itshaemocyte layer (granulocytes) and a connective layer of length. Each branch of the gills gives rise to verticalthe circular and longitudinal muscles and the outer intima filaments. The longitudinal septum separates the primaryare composedof the wall of the midgut [19]. The afferent vessel from the primary efferent vessel. Theperitrophic membrane is produced by the epithelial cells primary afferent vessel supplies blood to the axis of thein the midgut. The function of the membrane is to protect gills. The secondary afferent vessels direct the blood into


9

Fig. 5A: Dendrobranchiate gills of the genus Penaeus, B: close up of Dendrobranchiate of gill lamellae of the genusPenaeus, C: Trichobrachiate gills of the genus Stenopus, D: close up of Trichobrachiate of gill lamellae of thegenus 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 ofgill lamella. The water blood barrier is found in each the vertebrate. The haemolymph is responsible forfilament and it consists of cuticle, epithelium and basal transport of different nutrients, salt, water and oxygen tolamina. The barrier involves in allowing rapid diffusion of all tissues. It also plays a major role in the excretion ofgases. The efferent vessel carries oxygenated blood from metabolic waste, excess salts and water [26, 32]. Thethe 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, electrolytesmain roles such as salt and water balance, ammonia and metals [33]. Several authors have reported that theexcretion and calcium uptake [24, 28, 29]. The gills are also haemocyanin accounts for 87% of the total haemolymphinvolved in the capturing and the elimination of foreign proteins in P. vannamei [34, 35]. In addition to oxygenparticles in the haemolymph particularly bacteria [30]. transport, haemocyanin proteins also have other

Circulatory System: The circulatory system of shrimp defense [38].consists of a heart, associated conduits and haemal Haematopoietic tissues are located dorsal from of thesinuses, haematopoetic tissues and lymphoid organs stomach and the tissues often continue towards the(Figure 6). Penaeids and other arthropods have a antennal gland [22, 39]. The Haematopoietic tissues aresemi-open circulatory system. The heart is located made up of lobules of tissue, which produce thedorsally in the cephalothorax. The haemolymph vessels haemocytes [40]. Therefore, haemocytes are thought to beleave the heart. Then, the vessels branch into several derivedfrom two main cell lines where one non-granulartimes before they end in the sinuses, which are present cell and other cell line produces a granular cell. Four mainthroughout the body. The haemolymph passes first cellular types were described in the haematopoieticthrough the gills and then after, it returns to the heart by tissues of P. monodon [41]. These cells are type I cellsmeans of efferent vessels [23, 31]. The haemolymph of (other haemocyte cells), type II cells (non-granularshrimp 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 bytransported by free flowing hemocyanin proteins and the Dantas Lima et al. [42] have also separated five main

functions such as energy storage [36, 37] and immune


10

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 asiodixanol density gradient centrifugation. These X-organ/sinus gland complex, postcommisural andsubpopulations 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 andsubpopulation 5 [42]. The lymphoid organs are a pair of androgenic glands [16, 47].nodular structures which are located on a major artery atthe craniodorsal surface of the hepatopancreas [22, 40]. Reproductive System: In penaeids shrimp, theThe primary functions of these organs are the elimination reproductive tract of males includes paired testes, a vasof bacteria and infected virus-infected cells [41, 43, 44]. deferens and ejaculatory ducts or terminal ampoules

Nervous System: The nervous system of shrimp and up of convoluted seminiferous tubule which surroundedother crustacean is composed of the brain which is by haemal sinuses. The spermatids are produced in thelocated dorsally in the cephalothorax and it is connected spermatogonia which are differentiated from germinal cellsto the ventral cord by two connectives which pass around in the testes [48]. The spermatozoa (spermatids) ofthe esophagus [26]. The brain is composed of three decapods are non-motile and non-flagellate compared toregions (Figure 7), namely: protocerebrum, the other invertebrates [26]. The maturation of thedeuterocerebrum and tritocerebrum [26]. In shrimp, the spermatids takes place in the different regions of thepaired thoracic and abdominal ganglia are medially fused, seminiferous tubule. The petasma and appendix masculinebut the paired connectives separate the ganglia of of the male abdominal appendages are used foradjacent segments from the thoracic and abdominal delivering sperm cells to the external thelycum of theganglia [26, 46]. The central nerve is regulated via female which is located between the bases of the fifthneurohormones secreted by two main divisions of glands. walking legs [8].

[26, 48]. The testes are multi-lobed and each lobe is made


11

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 theposterior end of the pleon and oviducts which terminate mesoderm. The wall of coelomosac is composed of aadjacent 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 aexternal environment via the gonophore which is located similar role with that of the vertebrate glomerular nephronon the 3 walking legs (pereiopods) [26]. In shrimp, the [16].rd

thelycumis used for receiving the spermatophores and it The labyrinth (Figure 9B-G) is made up of a networkis located between the bases of the 4 and 5 walking legs of coiled simple columnar epithelial cells. It has two cellth th

of the female shrimp. The white leg shrimp has an open types: namely, (i) labyrinth I cells characterized bythelycum system. Thus, the spermatophore should be having tall columnar cells with basal nuclei and apicalplaced 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

Integument System: Integument of the penaeid shrimp is involved in the movement of ions and reabsorption offorms an exoskeleton (cuticle) which covers all the proteins. The proximal and distal tubules serve as theexternal 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 canphysical barrier which prevents the entrance of pathogens be used as a reservoir for urine storage. It may also haveinto the body [49, 50]. The histological structure of the a role in the final urine modification [26]. The bladder hascuticle consists of outer epicuticle, exocuticle, endocuticle epithelial cells similar to the labyrinth [16]. The urinaryand the inner membranous layer [51]. The cuticle is a bladder is connected to the nephropore (Figure 9A) via amineralized tissue which is composed of different ureter [22, 56]. The nephropore is a cuticular wave likehistological 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 thethe different moulting cycles [51]. Moulting is a complex base of the epithelial cells of the labyrinth with the help ofprocess for the growth by which a shrimp sheds the old capillaries. Haemolymph bathes the antennal glands andcuticle and produces a new one. Several authors have it flows to the hemocoel through a series of channels inalso demonstrated that the moulting cycle can influence the glands. Different authors have reported that the urineother functions such as development, growth, of P. vannamei remains isosmotic with that ofregeneration, hematopoietic and defenseresponse [35]. haemolymph [35, 58]. The known main functions of theSeveral 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 acidificationlate post-molt stages (A and B), inter-moult stage (C), and heavy metal detoxification, excretion of nitrogenousearly 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 byneurohormones. However, it is also affected by Immune System of P. vannamei: The innate immuneenvironmental factors like temperature, light and salinity.These factors can also influence metabolism andneurohormones production [55].

Excretory System: The antennal glands are the mainexcretory organs of shrimp and other crustaceans andthese glands are located at the base of secondaryantennae. The excretory (nephropore) exists on the coxaof the antenna. These glands are composed of fourregions (Figure 8): namely, end sac (coelomosac),

throughout the anterior part of the pereon. The labyrinth

system of the crustacean mainly reacts againstpathogenic microorganisms. However, some authorshypothesize that crustaceans are also capable ofexhibiting a specific immune response via antibodyindependent mechanisms [59]. For example, when shrimpare injected with antigens, these vaccines like treatmentssomewhat temporarily increased resistance or tolerancethe pathogen from which the antigen was originallyderived [60]. The shrimp’s innate immune system hasboth cellular and humoral immunity components to fight


12

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 ofthe 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 indicatedin arrow E [26]

invading microbes [61]. The cellular immunity involves Of all the cellular components of the crustaceannodulation, melanization, encapsulation and innate immune system, the cellular melanoticphagocytosis, while the humoral immune component encapsulation is the most efficient mechanism againstincludes antimicrobial peptides, anti-oxidant defense foreign antigens. The complex melanization cascadeenzymes, proteinase inhibitors, prophenoloxidase- requires the circulating haemocytes and severalactivating 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 moreenzymes, blood clotting cascade and agglutinins and potent humoral components of many crustaceans. Thecytokine like factors [61, 62]. The immune system of proPO activating system plays a major role in non-selfshrimp can involve in different functions such as recognition that occurs in the innate immune responserecognizing 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


13

which leads to initiation of phagocytosis, melanization, CONCLUSIONcytotoxic reactant production, encapsulation, theformation of nodules and capsules [64]. The proPOactivating system also has different roles in other humoralresponses such as reactive oxygen species (ROS),antimicrobial peptides and lysozymes [65, 66].

Based on the type and size of cytoplasmic granulespresent in the haemolymph cell, the crustaceans havethree different types of haemocytes subpopulations,namely: hyaline cells, semi-granular and granularhaemocytes [31, 67]. However, the recent studiesconducted by [42] have categorized the subpopulationsof haemocytes from the P. vannamei into five groups ofcells. According to this classification, the cell types are(i) subpopulation 1, (ii) subpopulation 2, (iii)subpopulation 3, (iv) subpopulation 4 and (v)subpopulation 5 [42]. The hyaline cells account for 5-20%of the haemocyte population. These cells are ovoid tospindle shaped and they are smaller than the other threetypes. The semi-granular cells represent (60-75%) ofhaemocyte subpopulations. The remaining granulocytescells represent around 10-25% of the haemocytepopulation [68].

The detailed functions of the differentsubpopulations of shrimp haemocyte have not yet beenwell described. However, some studies indicated that thehyalinocytes perform the phagocytosis role by releasinganti-microbial and pro-inflammatory compounds [42].The semi-granular cells perform different functions suchas encapsulation [69], phagocytosis [70], storage andrelease of the proPO system [71] and cytotoxicity role [72].These cells take up and digest the foreign particles insidethe phagolysosomes by using respiratory burstmechanisms which produce lysozymes and reactiveoxygen species. The granulocytes are the main source ofthe proPO system which plays an important role forencapsulation and nodulation during combat of fungi andbacteria, respectively [73]. Several studies are mainlyfocused on antifungal, anti-parasites and anti-bacterialresponses rather than anti-viruses responses [65, 66].However, the RNA interference (RNAi) is one of the fewwell-described pathways which play a major role in thecrustacean antiviral immune response [74]. The otherstudies by [75] reported the discovery of an antiviralgene, PmAV from P. monodon shrimp. This gene mayprovide a clue to explain the innate antiviral immunity ofshrimp and it may be helpful to control shrimp viraldisease [75, 76].

Shrimp aquaculture plays a significant role in theworld economy. The most of the aquaculture shrimpcontribution has come from P. vannamei which accounts80% of the whole shrimp production. The life cycle of thisspecies is very complex and it usually takes around 1.5years to complete the whole life cycle of P.vannamei.However, the life cycle of this shrimp takes around 6months to reach a market size for human consumption.The external morphology of P.vannamei is well describedand understood. However, there is no solid knowledge ofthe internal morphology and physiology of this speciesparticular in areas of nervous system development andstructure. Further, there is limited information on theunderstanding of behavior and feeding habits of thisanimal. Therefore, further studies are needed in future tohave solid knowledge of internal morphology andphysiology, natural behaviour and feeding habits of P.vannamei in order to improve the production and healthmanagement systems.

REFERENCES

1. FAO, 2016. FAO Statistical Yearbook: Fishery andAquaculture Statistics. The organization of Food andAgriculture of the United Nations,Rome.http://www.fao.org/3/478cfa2b-90f0-4902-a836-94a5dddd6730/i3740t.pdf.

2. FAO, 2012. FAO Statistical Yearbook: Fishery andAquaculture Statistics. The organization of Food andAgriculture of the United Nations,Rome.http://www.fao.org/3/478cfa2b-90f0-4902-a836-94a5dddd6730/i3740t.pdf.

3. Flegel, T.W., D.V. Lighter, C.F. Lo and L. Owens,2008. Shrimp disease control: past, present andfuture. In: Bondad-Reantaso, MG, Mohan, CV,Crumlish, M., Subasinghe, R.P., (Eds.), Diseases inAsian aquaculture volume 6. Manila, Philippines:Fish Health Section. Asian Fisheries Society,6:355-378.

4. Rodgers, C.J. and M.D. Furones, 2009. Antimicrobialagents in aquaculture: practice, needs and issues.Ciheam.Options Mediterraneennes, 86: 41-59.

5. Stentiford, G.D., J.R. Bonami and V. Alday-Sanz, 2009.A critical review of susceptibility of crustaceans toTaura syndrome disease, Yellow head disease andWhite spot disease and implications of inclusion ofthese diseases in European legislation. Aquaculture,291: 1-17.


14

6. Thuong, V.K., V. Tuan, W. Li, P. Sorgeloos, 18. Icely, J.D. and J. Nott, 1992. Digestion andP. 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.), thelegged 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 thesetiferus (Decapoda, Penaeidae). Journal of mid gut trunk in the penaeid shrimp SicyoniainMorphology, 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 structureFast, 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 ofdignoses 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 aquacultureclassification 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., Newof 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 ofOrlando, 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 ofandpost-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. IonHarrison, 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 similisand physiology of the Digestive system of Some (Decapoda, Penaeidae): description andCrustacean species studied in France. Journal of experimental testing of function. Journal ofReviews in Fishery Science, 6: 13-39. Morphology, 242:125-139.


15

30. Martin, G.G., M. Quigley, M. Quintero and 41. Van de Braak, C.B., M. Botterblom, W. Liu,H. Khosrovian, 2000. Elimination of sequesteredmaterial from the gills of decapod Crustaceans.Journal of Crustacean Biology, 20: 209-217.

31. Bauchau, A.G., 1981. Crustaceans. In: Ratcliffe, N.A.,Rowley, A.F., (editors), Invertebrate blood cellsvolume 2, Academic Press, London, pp: 385-425.

32. Hose, J.E., G.G. Martin, V.A. Nguyen, J. Lucus andT. Rosenstein, 1987. Cytochemical features of shrimphemocytes. Biological Bulletin, 173: 178-187.

33. Shimizu, C., H. Shike, K. Klimpel and J. Burns, 2001.Hemolymph analysis and evaluation of newlyformulated media for culture of shrimp cells (Penaeusstylirostris). Journal of Morphology, 37: 322-329.

34. Figueroa-Soto, C.G., A.M. Calderon, Dela Barca,M. Vazquez, I. Higuera-Ciapara and Yepiz-G.Plascencia, 1997. Purification of hemocyanin fromwhite shrimp Penaeus vannaemi (Boone) byimmobilized metal affinity chromatography.Comparative Biochemistry Physiology, 117: 203-208.

35. Chen, L.L., H.C. Wang, C.J. Huang, S.E. Peng,Y. Chen, S.J. Lin, W. Chen, C.F. Dai, H.T. Yu,C.H. Wang, C.F. Lo and G.H. Kou, 2002a.Transcriptional analysis of the DNA polymerasegene of shrimp white spot syndrome virus (WSSV).Journal of Virology, 301: 136-147.

36. Sannchez, A., C. Pascual, A. Sanchez, F. Vargas-Albores, G. Le Moullac and C. Rosas, 2001.Hemolymph metabolic variables and immuneresponse in Litopenaeus setiferus adult males: theeffect of acclimation. Aquaculture, 198: 13-28.

37. Pascual, C., G. Gaxiola and C. Rosas, 2003. Bloodmetabolites and hemocyanin of the white leg shrimp,Litopenaeus vannamei: the effect of cultureconditions and a comparison with other crustaceanspecies. Marine Biology, 142: 735-745.

38. Destomieux-Garzon, D., D. Saulnier, J. Garnier,C. Jouffrey, P. Bulet and E. Bachere, 2001. Antifungalpeptides are generated from the C- terminus of shrimphaemocyanin in response to microbial challenge.Journal of Biological Chemistry, 276: 70-77.

39. Martin, G.G. and J.E. Hose, 1992. Vascular elementsand blood (hemolymph). In: Harrison, F.W., Humes,A.G. (Editors), Microscopic anatomy of invertebrates,volume 10, Decapod Crustacea. Wiley-Liss, Inc., NewYork, pp: 45-75.

40. Martin, G.G., J. Kim and J.E. Hose, 1987. Structureofhemaotopoietic nodules in the ridgeback prawn,Sicyoniain gentis: light and electron microscopyobservations. Journal of Morphology, 192: 193-204.

N. Taverne, W.P. van der Knaap and J.H. Rombout,2002a. The role of the haematopoietic tissue inhemocyte production and maturation in the blacktiger shrimp (Penaeus monodon). Fish and ShellfishImmunology, 12: 253-272.

42. Dantas Lima, J.J., M.Corteel, K.Grauwet, N.T.T. An,P. Sorgeloos and H.J. Nauwynck, 2013. Separation ofPenaeus vannamei hemocyte subpopulations byiodixanol density gradient centrifugation.Aquaculture, 408-409: 128-135.

43. Duangsuwan, P., I. Phoungpetchara, Y. Tinikul,J. Polijaroen, C. Wanichanon and P. Sobhon, 2008.Histological and three dimensional organisations oflymphoid tubules in normal lymphoid organ ofPenaeus monodon. Fish and Shellfish Immunology,24: 426-435.

44. Rusaini, P. and L. Owens, 2010. Insight into thelymphoid organ of penaeid prawns: A review. Fishand Shellfish Immunology, 29: 367-377.

45. Escobedo-Bonilla, C.M., L. Audoorn, M. Wille,V. Sanz, P. Sorgeloos, M.B. Pensaert and H.J.Nauwynck, 2006. Standardized white spotsyndrome virus inoculation procedures forintramuscular or oral routes. Diseases of AquaticOrganisms, 68: 181-188.

46. Govind, C.K., 1992. Nervous system. In: Harrison,FW, Humes, AG. (Eds.), Microscopic anatomy ofinvertebrates, volume 10. Decapod Crustacea, Wiley-Liss, Inc., New York, pp: 395-438.

47. Diwan, A.D., 2005. Current progress in shrimpendocrinology: A review. Indian Journal ofExperimental Biology, 43: 209-223.

48. Krol, R.M., W.E. Hawkins and R.M. Overstreet, 1992.Reproductive components. In: Harrison F.W., Humes,A.G. (Eds.), Microscopic anatomy of invertebrates,volume 10, Decapod Crustacea. Wiley-Liss, Inc., NewYork, pp: 295-343.

49. Armstrong, P.B. and J.P. Quigley, 1999. Alpha-macroglobulin: an evolutionarily conserved arm ofthe innate immune system. Developmental andComparative Immunology, 23: 375-390.

50. Tincu, A.J. and S.W. Taylor, 2004. Antimicrobialpeptides from marine invertebrates. AntimicrobialAgents and Chemotherapy, 48: 3645-3654.

51. Roer, R. and R. Dillaman, 1984. The structure andcalcification of the crustacean cuticle. AmericanZoology, 24: 893-909.


16

52. Compere, P., C. Jeuniaux and G. Goffinet, 2004. The 62. Cerenius, L., S.I. Kawabata, B.L. Lee, M. Nonaka andintegument: morphology and biochemistry. In: K. Soderhall, 2010. Proteolytic cascades and theirForest, J., Schram, F.R., von Vaupel Klein, J.C. (Eds.), involment in invertebrate immunity. Trends inThe 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. TheB.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 haemolymphPhysiology, 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 andV. 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. McCollmonodon. 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 viruszoology, 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 andstudies 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 andand 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 CrayfishCrustacean 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 proteinsvarious salinity conditions. Molecular and and Beta-1, 3-glucan binding-proteins from 2Integrative 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 of24: 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 Environmental2011. 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 anda vibrio vaccine. Journal of Invertebrates K. Bertheussen, 1985. The cytotoxic reaction ofPatholology, 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 ofanti-microbialdefense of marine invertebrates: the granulocytes in the ridgeback prawn Sicyoniapenaeid shrimps and the oyster Crassostrea gigas. ingentis. Journal of Invertebrate Pathology,Immunology Review, 198: 149-168. 53: 335-346.


17

74. Bartel, D.P., 2004. Micro RNAs: genomics, 76. Tassanakajon, A., P. Supungul, K. Somboonwiwatbiogenesis, mechanism and function. Cell, and S. Tang, 2013. Discovery of immune molecules116: 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 shrimpPenaeus monodon. FEBS Letters, 551: 53-57.

biology of white leg shrimp, penaeus vannamei: review2)18/1.pdfworld journal of fish and marine...

Documents