Embryonic Development of Commercially Important Portunid Crab

Soundarapandian et al., J Marine Sci Res Dev 2013, 3:2 Marine Science http://dx.doi.org/10.4172/2155-9910.1000122 Research & Development

ResearchResearch Article Article OpenOpen Access Access Embryonic Development of Commercially Important Portunid Crab, Charybdis feriata (Linnaeus) Soundarapandian P1*, Ilavarasan N2, Varadharajan D1, Jaideep Kumar1 and Suresh B1 1Faculty of Marine Sciences, Centre of Advanced Study in Marine Biology, Annamalai University, India 2Department of Zoology, Government Arts College, Karur, India

Abstract The quality and survival of newly hatched zoea will depend primarily on the embryonic development. So an attempt has been made to study the embryonic development in the portunid crab, Charybdis feriata. The embryonic development of C. feriata is divided into six stages, viz. blastula, gastrula, eye placode, pigment; heart beat and freshly hatched first zoea. In blastula stage, the eggs were round, golden yellow in colour and the diameter of the egg was 0.36 mm-0.37 mm. In gastrula stage, the eggs were round and deep yellow or yellowish orange in colour, and the diameter of the egg was 0.38 mm-0.39 mm. In eye placode stage, the eggs were round orange in colour and the diameter of egg was 40 mm-41 mm. In pigment stage, the eggs were brown in colour and the diameter of the egg was 0.42 mm-0.43 mm. In hear beat stage, the eggs were dark brown or black in colour, and the diameter of the egg was 0.44 mm-0.45 mm. The freshly hatched I zoea moved freely in the water, and its carapace length ranges from 1.05 mm-1.25 mm.

Keywords: Embryonic development; Blastula; First zoea; Crucifix Results crab; Survival The eggs of C. feriata went through different colours with its Introduction gradual development. The newly spawned eggs were bright yellow, and the number of eggs attached to each seta of the pleopod was not After the disease outbreak in shrimp farming, crabs have become definite in number. The eggs were spherical and surrounded by two a candidate species for aquaculture because of their export potential membranes, an inner and outer membrane. Both membranes were [1-7]. In order to develop a hatchery technology, the crab larval biology transparent, and the yolk was visible as yellow granules with polygonal should be thoroughly studied to produce good quality eggs and healthy areas. Owing to the large size of the egg mass, the abdomen was almost zoea from the mother crab [1,2,4,5]. So far, there is no reliable hatchery straight, continues with the cephalothorax, and the telson was slightly for crabs because of the mass mortality of the zoeal stages. Hence, tilted upwards. The newly oviposited eggs contain all the necessary embryological study forms a base line to get healthy first zoea from material for synthetic processes associated with embryogenesis and developing eggs. So, in the present study, an attempt has been made to morphogenesis, and all of the compounds required for oxidative study the embryonic development of C. feriata. metabolism and energy production. The egg contains nutritive Materials and Methods reserves, in the form of proteinaceous yolk and lipid vesicles scattered throughout the cytoplasm. The newly spawned eggs were bright Gravid females of C. feriata with early broods (yellowish orange yellow, as the yolk contains carotenoid pigments. As the development coloured eggs) were collected from the Parangipettai coastal waters progresses, the bright yellow colour changes to dull yellow and finally, and retained in separate tanks containing sea water (salinity–35 ± 1%; to dark grey, just one day before hatching. At this stage, the developing temperature-28-31ºC; dissolved oxygen was up to the saturation level larvae with its occasional twitching movements were observed under and photoperiod-12 L: 12 D). The crabs were fed with mussel and clam the microscope. During this period, there was considerable increase in meat once in a day. Every day, the excess food, excreta and shed out the egg size also. The total days of incubation varied between 8-11 days. eggs were siphoned out. Continuous aeration was given throughout the The eggs at the time of oviposition were quite distinct and large. They incubation period and the development of the egg was closely observed. could be divided into six stages, viz. blastula, gastrula, eye placode, Daily colour changes of the eggs during incubation period could be pigment, heart beat and freshly hatched first zoea [10]. noted. Small clumps of eggs were snipped from random locations in each clutch using sharp scissors. All the developing embryos were examined with a MEIJI binocular dissecting microscope (100 X), to ensure that only viable embryos were sampled, and the colour change *Corresponding author: Soundarapandian P, Faculty of Marine Sciences, corresponding to the development and length of incubation period was Centre of Advanced Study in Marine Biology, Annamalai University, noted [1,8]. The time course of embryonic development, as indicated Parangipettai-608 502, Tamil Nadu, India, Tel: 04144-243223; Fax: 04144- by the appearance of specific morphological features, including 243553; E-mail: [email protected] the development of the compound eye, initiation of the heart beat, Received March 23, 2013; Accepted April 23, 2013; Published May 03, 2013 development of the limb pigmentation and initiation of limb twitches Citation: Soundarapandian P, Ilavarasan N, Varadharajan D, Kumar J, Suresh were monitored. The gradual change in the embryonic development B (2013) Embryonic Development of Commercially Important Portunid Crab, and increase in the size of eggs were recorded to understand the Charybdis feriata (Linnaeus). J Marine Sci Res Dev 3: 122. doi:10.4172/2155- different developmental stages [9]. All these developmental stages were 9910.1000122 photographed using the digital camera (Nikon, COOLFIX 990, and Copyright: © 2013 Soundarapandian P, et al. This is an open-access article Japan), attached with the microscope. distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

J Marine Sci Res Dev ISSN:2155-9910 JMSRD, an open access journal Volume 3 • Issue 2 • 1000121 Citation: Soundarapandian P, Ilavarasan N, Varadharajan D, Kumar J, Suresh B (2013) Embryonic Development of Commercially Important Portunid Crab, Charybdis feriata (Linnaeus). J Marine Sci Res Dev 3: 122. doi:10.4172/2155-9910.1000122

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Stage–I–Blastula embryogenesis into two groups as the larger eggs utilize more lipid than protein, and the smaller ones utilize more protein than lipid [14]. Eggs were round, golden yellow in colour and were undeveloped, In most marine invertebrates, the newly laid eggs contain all the energy and mass of undifferentiated cells are found. Yolk granules were and reserves for embryonic development [15,16]. Female nutritional denser. Cleavage and gastrulation were not clear. The diameter of the and reproductive condition, temperature and salinity may affect freshly laid C. feriata egg was 0.36 mm-0.37 mm. oogenesis, embryogenesis and larval quality [17-19]. Stage–II–Gastrula As the embryo develops, the size of the eggs, increases gradually. Eggs were round and deep yellow, or yellowish orange in colour. The eggs swell as they develop, so that by the time they are ready to The space between the egg wall and the inner developing embryo was hatch, they are roughly double their new-laid volume. The egg size visible. The diameter of the egg was 0.38mm-0.39 mm. of nine species of brachyuran crabs did not vary significantly within species and mean egg size was not correlated with female body size Stage–III–Eye placode [20]. The same trend was observed inS. serrata, by where egg diameter Eggs were round orange in colour. Yolk granules were not denser. was not related in any way to female size, and also the egg diameters Segmentation and organogenesis were distinct. The eyespots were increased at a relatively steady pace throughout ontogeny [21]. There appeared as scarlet crescent. The diameter of egg was 40 mm-41 mm. was an accelerated increase in egg diameter, when the embryonic heartbeat was first observed. Similar observations were made by for Stage–IV–Pigment green crab (C. maenas), the nut crab (Ebalia turberosa), and some lobsters (Galathea dispersa and G. squamifera) [22]. Under constant Eggs were brown in colour with slightly elliptical in shape. environmental conditions, the variability in egg size and biomass has Appendages of embryonic larvae were pigmented. The diameter of the been attributed to variation in female size or age and genetic factors egg was 0.42 mm-0.43 mm. [23,24]. Stage–V–Heart beat Hamasaki et al. [25] studied batch fecundity in P. trituberculatus, in The eggs were dark brown or black in colour. Eyes were round in which they emphasized that the size of eggs decreased with increasing shape. Heart starts to beat vigorously. The diameters of C. feriata eggs temperatures, the number of first zoeae showed no fluctuation in the were 0.44 mm-0.45 mm. same-size females throughout the breeding season. They suggested that three patterns of reproductive characters may cause this phenomenon: Stage–VI–Newly hatched first zoea (1) Females invest the same amount of energy in the reproductive The freshly hatched I zoea moved freely in the water, andits output throughout the breeding season, so that they increase egg carapace length ranges from 1.05 mm-1.25 mm. The hatching success number with decreasing egg size dependent on the trade-off between of freshly hatched I zoea is 95%. egg size and number, but lose more eggs between oviposition and hatching as the breeding season advances [26]. (2) Females produce Discussion similar egg numbers, and decrease egg size and energy investment for reproductive output as the breeding season advances; and (3) Females In decapod crustaceans, the embryos develop in broods that are decrease both egg size and number, and egg loss rate decreases as the carried by the females, and experience the parental environmental breeding season advances. Seasonal and regional variability in egg size conditions. In crabs, during mating, the sperms are transferred to the and number is known for a few brachyuran species. In the Japanese seminal receptacle, which act as a storage organ. Viable sperms are mitten crab, Eriocheir japonica, egg size varies within the breeding utilized during subsequent spawnings of that particular intermoult season; large eggs are spawned and developed at low temperature and period. As the eggs are laid, they adhere to one another and to the setae small eggs at high temperature [27]. Brante et al. [28] reported the egg of the endopodites of the abdominal segment, and the maturing egg number and size for the cancrid crab, C. setosus, distributed along the mass/sponge is held between the reflexed abdomen and venter of the Chilean coast. Egg numbers produced by females showed no significant cephalothorax. The abdominal chamber acts as an incubation chamber difference along a latitudinal (temperature) gradient, but egg size and for the developing eggs. Hamasaki et al. [11] reported embryogenesis in reproductive output decreased in Northern Chile (high temperature). P. trituberculatus, in which, females extrude their eggs from gonopores In this study, the number of eggs was examined using ovaries that onto a bottom substratum such as sand, where they bury themselves; developed during the overwintering period. then they attach the extruded eggs to the ovigerous setae of the endopods of the pleopods, which are moving forward and backward. During the development, the colour of the egg changes through brown to grey, as the yolk is used up and the outline of the embryo become Needham [12] classified the animal eggs into two categories based visible. The eyes and pigment spots appear first, followed by the outlines on the major substrate (fat or protein) utilized during embryogenesis. of the abdomen and cephalothorax [29]. The eggs when deposited are They are terrestrial or cledoic eggs, utilizing fat during embryogenesis, yolky with bright yellow or yellowish orange, but they become brown and aquatic or non-cledoic eggs utilizing proteins for oxidation. and then dark brown or black before hatching. The colour change However, after working with several marine crustaceans discussed was caused by absorption of the yellow yolk and development of dark the merits and demerits of classification of eggs [12,13]. Pandian [13] pigment in the eyes [30,31]. Veera [30] reported that as the progression classified the eggs according to the habitat of the species and the main of development occurs, the embryo decreases in dry weight stage by substrate metabolized. They are: terrestrial eggs-protein metabolism stage, as it utilizes the yolk material. Subramoniam [32] studied the is greatly suppressed and oxidation of fat is geared up; freshwater yolk utilization during embryogenesis in Emerita asiatica and reported eggs-protein metabolism is predominant and limited fat metabolism; that the water content steadily increased; conversely, protein content marine eggs-fat depletes heavily and considerable suppression of showed a steady decline; protein-bound carbohydrates declined, where protein metabolism. Based on the egg size, classified the crustacean as the concentration of free carbohydrates and glycogen exhibited an

Page 3 of 5 increasing trend; lipid level remained unaltered almost up to stage V, was 8-10 days [36]. In general, the duration of embryonic development thereupon, the value fell precipitously, reaching the minimum in stage in the portunid crabs varies between 8 to 14 days depending on the IX. environmental conditions. Sun and Yu [34] have reported that the duration of embryonic development could be shortened by raising The embryonic development includes the stages of newly spawned temperature in the range of 18-25ºC. In most crustaceans, the incubation egg, multicell stage, eye stage, pigment stage, heart beat stage and period is highly dependent on temperature [37]. Incubation periods of prehatching stage. The course of embryonic development includes Moreton Bay (Australia) population of S. serrata are usually in early cleavage, blastula, gastrula, segmentation, organogenesis, formation spring, at water temperatures of 18-20ºC [37]. Water temperatures of appendages, formation and functioning of heart, and formation of in estuaries and coastal waters along the north coast of South Africa chromatophores all around the body. Similar pattern of embryonic range between 17-22ºC in winter and 23-30ºC in summer [38]. The egg development was reported for many portunid crab species [5,30,31,33]. incubation period of S. serrata exponentially decreased with increasing Many workers have divided the crustacean egg stages, based on temperature [39]. the appearance of distinctive morphological features such as the eye, Salinity also holds an important role in the embryonic development heart beat and appendage formation. However, such morphological and egg hatching. During the course of current study, while maintaining characters only begin to appear mid-way during embryonic the brooders of C. feriata at different salinities, it was observed that the development. Cellular differentiation starts soon after gastrulation hatching of eggs and release of larvae occurs in the waters of salinity and requires enormous energy expenditure. Therefore, Subramoniam ranging between 30-35%. Campbell and Fielder [40] opined that, in [32] emphasized the importance of a detailed classification of early P. sanguinolentus, the occurrence of prezoeae increased when eggs development of decapod crustaceans, to understand the changes in were hatched at salinities below the oceanic salinities that this species the metabolic pathways involving interconversion of already stored normally encounters in nature. Similarly, found that prezoeae were substrates within the closed system of egg development. In the more prevalent in C. sapidus, when experimental salinities were below embryology of E. asiatica, divided the egg development into nine stages 20% [41]. based on colour change and other concomitant morphological features of the embryo. His study reports on the biochemical alterations in the Among crustaceans; brachyuran crabs carry the embryos for major organic substrates, as well as the activity of non-specific esterases extended periods of time [22]. During brooding, female crabs exhibit during egg development, leading to the release of the zoea. complex behaviors, which seem to be mostly directed towards providing embryos with oxygen [15,42-45]. Since oxygen consumption of the Subramoniam [32], while studying the embryonic development in embryos increases with progressing development, brooding females S. serrata observed different stages, which includes the stages of cleavage, increase ventilation frequency, providing oxygen to the embryos blastula, gastrula, egg-nauplius, embryo with five pairs of appendages, according to their demand [44]. This change in brooding behaviour is embryo with seven pairs of appendages, embryo with compound eye related to a 2-fold increase in oxygen consumption of brooding females pigments formation, and embryo almost ready to hatch. The cleavage (after discounting oxygen consumption of the embryo mass), when evolves those from the spiral type to the superficial type was studied compared to nonbrooding females of similar size [44]. This suggests by Sun and Yu [34]. The dividing furrow can be seen from 2 cells. The that oxygen provision to the brood may account for a substantial gastrula is formed through invagination. Xue et al. [35] studied the fraction of total reproductive costs. histology of embryonic development in P. trituberculatus and reported 5 stages, i.e. two egg-nauplius stages and three egg-zoea stages. The egg- Hatching usually occurs in the early hours of the day in C. feriata, nauplius stage could be divided into egg-nauplius I and egg-nauplius as all the portunid crabs generally hatch. During the hatching process, II. The egg-nauplius I includes the formation of optic lobe, antennule, the fully developed first zoea hatch out of the egg cases and swims antenna and mandible with the cleaving cells. These appendages are freely in the water column. Davis [45] reported the process of hatching, unsegmented; the thoracoabdominal process formed abdomen with a period of swelling of the eggs followed by osmotic swelling of the proliferating cells; the labrum rudiment and labium rudiment formed inner egg membrane at the start of hatching. The swelling inner egg in the tip of the stomodeum. The maxillule, maxilla, cavity abdomen, membrane then ruptures the chorion by pressure, from within the optic ganglia and antennule ganglia formed during the egg-nauplius larvae plays no part. The inner membrane is subsequently ruptured by II. The segmentation emerged between thorax and abdomen. The egg- mechanical action of the larval abdomen. zoea stages were divided into egg-zoea I, egg-zoea II and egg-zoea III. Water quality and feed are the important criterion in rearing the The carapace, stomach, hind gut, compound eye and thoracic ganglia berried crabs. If they are not maintained properly, diseases will attack, formed in the egg-zoea I. The antenna ganglia keep in touch with each which leads to the hatching of unhealthy larvae and their mortality in other; each of the optic ganglia was independent; the abdomen was the early stages itself. Iin SD et al. [46] observed that the egg quality, divided into 6 segments. The appendages segmented during the egg- egg hatching rate and the quality of the newly hatched zoea are very zoea II. The ends of the appendages were divergent with setae; the parts good when berried crabs fed with formulated feeds compared than of the compound eye have formed; the shape of the yolk sac was like normal diets. The mortality of the eggs has been attributed to fungus, butterfly. The pigment cells, maxilliped I, maxilliped II, heart, gonad predation and suffocation in fouled water and changes in temperatures. and brain have formed. The mesoderm formed muscle, and arranged On the average, only one out of every million eggs survives to become themselves as beads in the next stage. The digestive system has formed, a mature adult [47]. The quality of the eggs produced by individual except hepatopancreas. Compared with the egg-zoea I and egg-zoea females has also been highly variable. In order to select the best eggs for II, the brain and carapace further developed in the egg-zoea III. The incubation and subsequent rearing, an estimate of egg quality had to muscle and the hepatopancreas formed at the same time. be established, and this could be achieved immediately after extrusion. In the present study, the duration of embryonic development in C. Giles [21] reported that, the newly hatched larvae could be subjected feriata lasts for 8-11 days. Almost similar duration was also reported to a variety of stress tests, including ammonium, salinity, formalin and in P. sanguinolentus [5]. Whereas in P. pelagicus, the period reported starvation stress tests, and the results of these tests would ultimately

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J Marine Sci Res Dev ISSN:2155-9910 JMSRD, an open access journal Volume 3 • Issue 2 • 1000121