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 �:	Seasonal disparity in Fecundity and embryonic development of Cinnamon anemone fish, Amphiprion melanopus (Bleeker, 1852) in captivity
Muthuramalingam Uthaya Siva *, Jeyagoby Balamurugan , Thipramalai Thankappan Ajith Kumar, Mohideen Abdul Badhul Haq and Muthuvel Arumugam
Centre of Advanced Study in Marine Biology, Faculty of Marine Sciences, Annamalai University,
Parangipettai-608502. Tamilnadu. India.
*Corresponding author: 
M. Uthayasiva, Doctoral research scholar, Centre of Advanced Study in Marine Biology, 
Faculty of Marine Sciences, Annamalai University, Parangipettai 608502, Tamil Nadu, India
Telephone Number: +919994992532
E-mail Id:  HYPERLINK "mailto:uthayasiva.m1@gmail.com" uthayasiva.m1@gmail.com, uthayasiva007@gmail.com












Abstract -The present study explains the seasonal influence on fecundity, embryonic development and parental care of Amphiprion melanopus reared in aquaria. Water quality parameters like temperature 27�2�C, salinity 29�2ppt, ammonia 0.001ppm, dissolved oxygen 4�2 ppm, pH 7.7�0.2, light intensity 18 � mol-1sec-1and photoperiod (13 L: 11 D) were provided. Brooders were fed with boiled oyster, shrimp and clam meet thrice a day and organic wastes were removed regularly. After obtaining maturation (4 months rearing in captive condition) successful spawning was observed. The percentage of fecundity, hatching, deformation and incubation were categorized into four seasons (summer, pre-monsoon, monsoon and post-monsoon) for a year. The spawning was occurred throughout the year except in December. The fertilization, hatching and deformation rate were calculated as 92.85%, 85.64% and 7.18%. There is no significant (P>0.05) changes were observed in fecundity and hatching rate seasonally. However, the incubation hours and deformation rate of egg clutch were significantly (P<0.01) varied based on the seasons. From this study, it is concluded that the spawning efficiency of red black anemonefish is not influenced by seasons throughout the year and it is feasible to culture in Indian environment. 
Keywords: Amphiprion melanopus, Captivity, Spawning, Fecundity, Seasonality.
1. Introduction 
Marine aquarium keeping is almost tropical in nature and divided into two major sectors, fish and invertebrates. The fantastic shapes, brilliant colors and fascinating patterns of marine ornamentals have won the hearts of millions of people and hence they are aptly called �living jewels� (Ajith Kumar et al., 2007). Pomacentridae is the most dominant group in the marine ornamental fish trade, due to its feasible nature (Wabnitz et al., 2003). They are the major occupiers of reef communities (Allen, 1975) contains 350 species distributed worldwide and most of them are reported from Indo-West pacific regions and 41 species  are available in Indian waters (Allen, 1991; Randall, 2005).
The development of hatchery production technology for clown and damselfishes relieve the pressure on wild population. It is necessary to understand the biology of these fishes, before culturing them in aquaria. The ontogeny of a fish such as embryonic, larval, juvenile, young, adolescent and adult (Balon, 1981 and URHO, 2002) played an important in the study of reproduction biology. The description of eggs, embryological development, larval rearing and juvenile production are available for limited Pomacentridae fishes and many reports are lacking in Indian waters (Dhaneesh et al., 2009). However, breeding and behavioural patterns of many tropical and subtropical Pomacentrid fishes have been well documented in many countries.
Generally, the development of early life stage from fertilization to embryo formation among Teleost fish follows the same pattern (Falk-Petersen, 2005). Despite scientific description of ova, development of the embryo, methodology of larval rearing and enhancement of juvenile production is still minimal. Hatching and chronological flow of embryonic development differs between the species and its environmental conditions. The free embryo phase begins when the embryo is free of egg membranes. The beginning of the larval period is indicated when the larvae are able to capture feed objects (Chen, 2005). The present study is immensely support the aquarist to culture A. melanopus an in eco-friendly and successfully throughout the year. It is also helpful in employment generation in the coastal regions, as these fishes have high trade value.
2. Materials and methods
2.1. Broodstock development 
Anemone fish, Amphiprion melanopus (n=10) and sea anemone, Heteratics magnifica (n=3) were procured from the traders, Chennai. Animals were transferred in airtight polythene bag and acclimatized at the hatchery, Centre of Advanced Study in Marine Biology, Annamalai University. After acclimatization, the pairs along with their host anemone were transferred to separate Fiberglass Reinforced Plastics (FRP) tanks (500L). Each tank was inserted with biological filter (made with coral pieces, ceramics and activated carbon). The water quality parameters such as salinity, ammonia level, dissolved oxygen, pH, light intensity, water exchange and photo period were maintained as  28�1psu, 0.001 ppm, 4.5�0.2 ppm, 7.7�0.2, 18 � mol-1sec-1, 40% per week and 13 L:11 D respectively. Fishes were fed with boiled oyster; shrimp and clam meet, while anemones were fed with fresh shrimp meats. Excess feeds were removed regularly twice in a day to prevent water contamination. Ceramic tiles and live rocks were provided as substrates. Fishes started spawning after 3 months of rearing; batch fecundity was estimated by counting the eggs in 1 cm2 and then multiplying with the total area of deposition (Satheesh, 2002).
2.2. Embryonic development
The eggs were sampled randomly from day 1st to 8th (5 eggs/day) to document the embryonic development. Each egg was placed on a slide to observe the morphological development (Ignatius, 2001). The photographs were taken with a digital camera (Sony cyber-shot G, China) with a light microscope (Leica, Germany). 
2.3. Estimation of fertilization, hatching and deformation rate
Developed brood stocks were tested for their efficiency of fertilization, hatching and deformation rate using the formula given below (Gunasekara et al., 1996). 
Fertilization rate = No of eggs fertilized / No of total eggs laid � 100Hatching rate      = No of eggs hatched / No of total eggs fertilized �100Deformation rate= No of deformed larvae / No of larvae hatched �100 
The above mentioned spawning performance of A. melanopus were calculate for a year and categorized into four periods as Summer (May-June 2012), Pre-monsoon (July-September 2012), Monsoon (October-December 2012), Post-Monsoon (January-March 2013). Based on the seasonal variations, the water temperature, incubation and hatching times were noted. The Multiple Regression and ONE-ANOVA were performed to test the statistical significant of data using standard tool SPSS V16.0 (Norusis, 2009). 
3. Result
The fishes were brushed the algae and debris, when deliberated to lay their eggs, which is more closely or beneath the sea anemone. In A. melanopus, most of the spawning was occurred at morning (8:00-9:00 hrs), while female deposit the eggs and followed by the male to release spermatozoa for fertilization. The spawning process was extended 60-90 min to complete the entire clutch fertilization. During spawning, the fishes were not taken feed and thereafter maximum parental care (fanning or mouthing) was mainly demonstrated by the male (75%) and partially done by female (25%). Continuous fanning was observed in male 108 attempts / hour, but in the case of female only 2 attempts / hour (during first 3 days). The longest and shortest duration of single time fanning by the male (includes mouthing) were 1.25 and 0.21 min. In the case of female, maximum and minimum fanning duration were 0.57 and 0.40 min respectively.
The embryonic development was measured on 1st day and the cell division was observed at the base of embryo (Fig. 1a). On the 2nd day, cells were divided and moved to top of embryo for the development of head and tail (Fig. 1b). During 3rd day, complete formation of head and tail were observed with visible heart beats (Fig. 1c). In 4th day, organs like eyes, mouth, tail and blood circulation was observed (Fig. 1d). The larval development shows the utilization of yolk sac during its growth on 5th& 6th days (Fig. 1e& f). The development of silver color in embryo indicates the complete development of eye during the pre-hatching (7th day; Fig. 1g). On 7th day night (19:00-20:00 hrs) few larvae were hatched-out (179 hrs) with high yolk sac (Fig. 1h). Slowly, the remaining clutches begun to release form their shells and complete hatched was observed on the 8th day of incubation (Fig. 1i). The newly hatched (8th day) larva has measured at the size of 4.2�1 mm (Fig. 1k) and initial larva mouth size was measured as 330�20 �m, so it could consume rotifer (B. plicatilis-130-340 �m) and zooplankton as its primary feed.
The estimated fertilization, hatching and deformation rate are 92.85%, 85.64% and 7.18% respectively (Fig.2). The fertilization rate of the clutches are significantly (P<0.01) depends on the seasonal variations whereas, the hatching rate is showed a significant (P>0.01) changes to fertilization rate. However, the deformation and incubation hour were significantly varied at 5% and 1% level based with temporal changes. According to DMR test, the changes in fecundity, deformation and incubation hours were varied between the summer and monsoon, while during pre-monsoon and post-monsoon showed similar spawning performance (Table 1). In addition, the regression analysis showed an exponential decrease in incubation time with increase in water temperature (R2=0.673; P<0.01) (Fig. 3). 
4. Discussion
Culturing of anemonefishes in hatchery contains minimum challenges as compared to other marine fishes. There were many breeding experiments conducted successfully on different species of clownfish (Overton et al., 2008; Alva and Gomes, 1989; Wilkerson, 1998; Ajith Kumar and Balasubramanian, 2009; Swagat gosh et al., 2012: Ajith Kumar et al., 2012). However, there would be certain limitations in culture practices of anemonefish in private aquaria. The present study was analyzed about parental care, embryonic development and spawning efficiency of A. melanopus with seasonal variation in captivity. 
Fertilization, hatching, deformation rate of larvae were depends on several factors such as feed quality, brooder health and environmental parameters. Although the brooders were maintained in the backwater (with salinity variation), showed similar fecundity and spawning frequency to those kept in running seawater (Overton et al., 2008; Alva and Gomes, 1989; Wilkerson, 1998; Ajith Kumar and Balasubramanian, 2009; Swagat gosh et al., 2012: Ajith Kumar et al., 2012). 
The clutch diameter of A. melanopus was found as 4.5 cm to 8.5cm with fecundity of 197-230 eggs per clutch as per formula. While, other species of cultured clownfish in aquaria make different size of clutches, such as A. sebae (8.5-9cm), A. percula (6.5-7.0cm), A. clarkii (8.5-9.5cm), A. ocellaris (4.5- 5.5cm) and P. biaculeatus (7.5 cm) and the fecundity increased with, size of the female (Swagat gosh et al., 2012) same observations were noted in the present study also in A. percula, the female was found bigger size than A. melanopus however; fecundity rate of A. melanopus (197-230) was lesser than A. percula (350-430). Hence, the fecundity rate of the anemonefish only depends on the size of female and also its age. 
After fertilization, especially the male taken care of eggs by fanning with their pectoral fins and cleaned the clutch gently through fanning and mouthing until hatching. Similar observations were reported in other clown species also (Overton et al., 2008; Melville and Griffiths., 1997), however, there are some variations in fanning and embryonic development periods related to anemonefish species. In addition, several factors such as temperature, salinity, ammonia level, dissolved oxygen, pH, light intensity and photoperiod were known to affect the growth and development of clownfish (Alva and Gomes, 1989). In the present study also the said parameters are maintained in optimum level as temperature 27�2�C, salinity 29�3ppt, ammonia level 0.001ppm, dissolved oxygen 4�2 ppm, pH 7.7�0.2, light intensity 18 � mol-1sec-1and photoperiod 13 L: 11 D. According to Jobling (2002), Moyle and Cech (2004) the embryonic developmental period is the phase between fertilization and commencement of organogenesis. The contour of eggs in different species of Pomacentridae �sh varies from oval to capsule shape (Moyer and Nakazono, 1978; Pathiyasevee, 1994) similarly the clutch of A. melanopus was in oval shape. Hoff (1996) reported that the length of clown�shes eggs ranged from 2.0 to 2.4 mm but in the case of A. melanopus, it was 3.1�1 mm. 
The development of eggs were noted morphologically on color changes, were yellow//orange on 1st and 2nd days, black/brown from 3rd day and silvery during pre-hatching. No color change in the eggs on 3rd and 4th days was considered immature/decayed (Balamurugan et al., 2013). Similarly, the eggs of A. melanopus have been found as dark orange in color in 1st and 2nd days. Light/ dark brown was observed from 3rdto 4th/6th days and silvery in pre-hatching. All other Pomacentrids male parent also exhibited culling by removing the unfertilized or dead embryos and was done to product other embryos (Ignatius et al., 2001). Silvery coloration with distinct visible eyes is usually a good indication for the hatch out within 12 hours, because the matured eyes showed this color. These observations are also similar to those reported for other clown species (Madhu et al., 2006; Balamurugan et al. 2013). In this study, on7th day only few eggs have got silvery and 8th day completely silvery appearance was noted and it is due to variations in the fertilization time from the beginning of first to last egg during spawning. 
The larvae hatched on 179 hrs has high yolk content in their body, while larvae released after 203 hrs have less yolk which was immediately transferred into rearing tanks enriched with rotifer (B. plicatilis) and algae (N. salina). Observations of the present study on A. melanopus showed no significant change in fertilization and hatching rate as 92.85% and 85.64% throughout the year. However, the temporal variation during premonsoon, monsoon and postmonsoon would influence the incubation period and deformation rate of clutches.
5. Conclusion 
Briefly, the increasing popularity and demand of marine ornamental fish, especially clownfish in market is sustainably increased in our country. The present study states there is less influence of seasonal variations on the fecundity, parental care, incubation periods, hatching, deformation rate of A. melanopus would help the stockholders to culture the particular species to earn high price. This will help to coastal fisher folk to enhance their liveliood through setting up of backyard hatceries and significantly, it will help conserve the precious marine ornamental fish biodiversity. 
Acknowledgments
Authors are thankful to the authorities of Annamalai University for providing necessary facilities and Center for Marine Living Resource and Ecology (CMLRE-Office Memorandum No: G4/3366/2013), Ministry of Earth Sciences for financial assistant.
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$dha$gdO.�Z[[+[,[1[h[�[�[�[�[�[�[�[�[\��T�V�����������������^�����ָ��Ǹ��񸶸�妖�wgw�X�hO.h�g�CJOJQJaJhO.h�V�5�CJOJQJaJhO.hTuCJOJQJaJhO.hTu6�CJOJQJaJhO.h�=6�CJOJQJaJhO.h�V�6�CJOJQJaJUhO.h�V�CJOJQJaJhO.h�=CJOJQJaJhO.h/G�CJOJQJaJhO.CJOJQJaJhO.h�|OCJOJQJaJfish, Amphiprion clarkii (Bennett, 1830). 	International Journal of Environmental 	Science and Development 3:1.
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Table captions
Table 1.One way analysis of variance on the spawning efficiency of A. melanopus with different seasons (a,b,c indicates the significant level at 5% according to DMR test; * significant at 1%, ** significant at 5% and *** non-significant at 5%)
Figure captions 
Fig. 1. Embryonic development of Amphiprion melanopus from 1st day to 8th day. A). 4 hours old egg (YS- yolk sac, CD- cell division). B). Formation of head and tail at beside of the yolk sac. C). Half developed larva. D). Formation of body parts by utilization of yolk. E). 5th day larva. F). Reduction of yolk sac by larva. G. fully developed larva with minimum yolk sac. H). fully developed larva without yolk sac at 8th day and it was inverted position. I). 7th day hatched larva with maximum yolk sac and J). 8th day hatched larva with minimum yolk sac.
Fig. 2. The percentage spawning efficiency (� SD) of A. melanopus during Summer, Pre-Monsoon, Monsoon, Post-Monsoon (*FR- fecundity rate, HR- hatching rate, DR- deformation rate).
Fig. 3. Regression analysis showed an exponential decrease (R=0.821, F=20.62, t=-4.54; P=0.001) in incubation rate (hours) to rise in temperature (�C).














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