A Review on Embryonic Development of Inland Fishes of Bangladesh

The early developmental pattern of inland fishes of Bangladesh are not well studied though it has a great importance in fisheries and aquaculture sector. The embryonic study provides interesting information on further growth and health of the fish and considered as an essential component for optimization of fish seed production by natural and induced breeding. Therefore, the current review work has been undertaken to provide a detail information on embryonic development of important inland fishes of Bangladesh. Information was collected from published scientific papers, un-published Masters and PhD dissertations from universities, popular articles and other published and grey literature. Diameters of unfertilized egg of the reviewed fish species were found to be 0.5 to 1.3 mm and fertilized egg were 0.49 to 1.6 mm. Shapes of the egg were also variable from species to species. There is little information available on egg activation and egg micropyle of fish species of Bangladesh. The fertilization rate of different fishes ranged from 40.1% to 93.9%. There are different stages of early development in different species and time needs to complete the stages also vary. The timing of post hatching development by metamorphosis was found to vary based on the fish species from several days to weeks. Different factors like temperature, photoperiod, DO, seasonality and presence of chemicals in water were found to affect the early development of fish. The review included eighteen inland fishes and unearthed useful insights of their embryonic development and influence of different factors. As we expect, the outcome of the study would provide a baseline and would be very useful in conducting further research on the embryology of indigenous fishes of Bangladesh. Keyword: Fish embryo, ontogenic development, early life stage, hatching, larvae


Introduction
Bangladesh is a land with massive potential water bodies with a wide diversity of fishes. During several decades' fishes of Bangladesh has declining due to various natural causes. Different man-made activities are also influencing the process. IUCN (2015) reported that 64 fish species are threatened which comprises 9 Critically Endangered, 30 Endangered and 25 Vulnerable fish species. Therefore, the conservation of this fishes is considerably important. The knowledge on early developmental pattern is essential for establishment of proper conservation measure. However, there is a very little knowledge available about the early embryonic and larval development of fishes of Bangladesh. Embryonic development is a complex process in which cellular differentiation and proliferation occur simultaneously at different rate (Hall, 2003). Changes in the pattern of the entire structure of an organ or of specific organ in relation to the environment are decisive for evaluating the developmental pattern of a species. Information on early life history is an essential requirement for optimization of mass seed production, culture and management of fishes. Embryonic development and larval development providing remarkable information in itself are imperative and consequential to the successful rearing of larvae for large scale seed production. Therefore, it is indispensable to conduct study to characterize different embryonic and larval stages of fish. In addition, embryonic developmental stages of fish life are also used in various investigational studies; especially in aquaculture as well as toxicological studies ).

Fish Embryo
Embryo is the earliest developing stages of fish from the time when the fertilized egg starts to divide, while it is continued within the egg until hatching. The embryo goes through several complex stages before hatching. Embryo is the result of fusion of male and female gamete and the first stage of life in fish as well as other animals (Langeland & Kimmel, 1997).

Gametogenesis
The process of gamete formation in the sexually reproducing animals is gametogenesis. The male gamete is known as spermatozoon or sperm, and the female gamete is known as ovum or egg. Fish produce gametes directly through meiosis in organs called gonads (testis in males and ovaries in females). Gametogenesis are of two types; spermatogenesis and oogenesis (Andrade et al., 2001).

Spermatogenesis
Spermatogenesis involves two distinct process known as formation of the spermatids and Spermiogenesis (Sharma et al., 2018). The primordial germinal cells called spermatogonia undergoes repeated mitotic divisions to maintain a supply of cells for the production of sperm. After meiosis primary spermatocytes form secondary spermatocytes; after the second meiotic division, they are spermatids (Avidor-Reiss et al., 2015). The metamorphosis or differentiation of the spermatids into the sperm is called spermiogenesis. Spermiogenesis is characterized by changes in the nucleus, acrosome formation and Centrioles (Avidor-Reiss et al., 2015).

Oogenesis
The primordial germinal cells divide repeatedly to form the oogonia which multiply by the mitotic divisions and form the primary oocytes and pass through the growth phase. In the primary oocyte, large amount of fats and proteins become accumulated in the form of yolk and due to its heavy weight, it is concentrated towards the lower portion of the egg (forming vegetal pole). After this process cytoplasm of egg divides unequally forming three polar body and one egg (Lubzens et al., 2010).

Fertilized Eggs
Prior to fertilization, the egg is in a quiescent state, arrested in metaphase of the second meiotic division. Upon binding of a sperm, the egg rapidly undergoes a number of metabolic and physical changes. The yolk is usually translucent and yellowish in color; the oil droplets are unchanged (Kinsey et al., 2007). Aerobic respiration increases in the egg (Nakano, 1953). Enzyme systems become activated. In most animals, a burst of protein synthesis begins and the nucleus undergoes the second division of meiosis after fertilization.

Cleavage
The zygote experiences a quick cell cycles with no significant growth, producing a cluster of cells within few minutes of fertilization is called cleavage (Sperber, 1995). Cleavage is basically occurring in the blastodisc region of the animal pole of the eggs which further converts into embryo (Fukazawa et al., 2010). After several successive cell division, the egg forms a thick layer of cell known as germ ring and is made up of superficial layer, ectoderm, endoderm mesoderm (Lee et al., 2004). A dorsal-ventral axis forms at that time that may be referred as prenotochord from which a neural plate is formed. Cells of the neural plate fold to form the neural groove and the surrounding neural folds which fuse, forming a hollow neural tube (Forgacs & Newman, 2005).

Morula, Blastula and Gastrula
A series of cleavage of zygote forms a solid ball of cell is called morula which occurs within few hours of fertilization. Soon after development of the 8-cell or 16-cell embryo (depending on the species), the blastomeres begin to form mulberry-shaped mass of cells called a morula. This change in shape of the embryo is called compaction (Forgacs & Newman, 2005). This compaction leads to form a hollow sphere called blastula, surrounding by a hollow blastocoel (Forgacs & Newman, 2005). The blastula enhances gastrula formation in which embryo form germ layers (Gilbert, 2010). Gastrula is a dramatic rearrangement of the cells of the blastula. Initially blastoderm cells move outwardly to intercalate with the more superficial cells which leads to the formation of gastrula (Warga & Kimmel, 1990). At this stage the yolk syncytial layer starts expansion around the yolk cell (Trinkaus, 1984). By the end of gastrulation, embryonic cells have rearranged into three layers' ectoderm, mesoderm and endoderm.

Importance of Embryonic Developmental Study of Fishes of Bangladesh
Different organs of fish develop in different embryonic stage. Knowledge about the timing of different organ development of fish can be extended by embryonic study. Knowledge on cleavage pattern of Bangladeshi fish can be achieved by embryonic study. Embryonic study can be helpful to optimize survival and growth rate of fish larvae in our country. Embryonic development besides, providing interesting information are imperative and substantial to the successful rearing of larvae for large scale seed production of any species and thus important for hatchery operators.

Factors Affecting Embryonic Development
A wide-ranging literature is present on the problem of the effect employed by some environmental factors upon the embryonic stage in fishes. These factors are like temperature, salinity, light, and some mechanical factors. Among this factors temperature is the most prominent factor as it is well known, the rate of the embryonic development of a given species is directly related to the temperature. Salinity is another important factor that affect the embryonic development of fishes. Every fish species has a tolerance limit of salinity beyond which in cannot survive. Light is not always controls the development of fish embryo. However, it has been shown in case of some species e.g. some salmonids, light usually has a negative impact on the early development of embryo (Eisler, 1957). Rather than these factors, some mechanical factors like pressure, shock etc. can sometime influence the embryonic development of fishes (Ciechomski, 1964).

Justification and Objectives of the Study
The embryonic and larval stages are considered very sensitive indicators of environmental disturbances (Marimuthu and Haniffa 2007). They are also indispensable in the study on ontogeny and phylogeny of their families (Legendre and Teugels 1991;Verreth et al., 1992). In addition, such studies on the embryonic development of any cultivable species can be useful in directing the husbandry efforts of fish farmer. In Bangladesh the embryonic study of fish has been not yet gained so much attention though it has a huge potential in the sector of fish and fisheries. The current review work is therefore has been undertaken to provide a details knowledge about the embryonic development of fishes of Bangladesh, its current status and future research importance on embryonic development of fishes of Bangladesh.

Literature Collection and Review
Literature were collected from different journals, published paper, Magazines related to fish and fisheries. Unpublished research from masters and PhD research were also considered. Personal communication with the experts on the field of fish embryology were done for collection of some information. The fish species under this review are given in Table 1.

Data Analyses, Tabular and Graphical Representation
All collected data were subjected in computer software MS Excel v2016 for analysis and graphical representation.

Fertilization
The egg and spermatozoa are the main component for fertilization. The eggs and spermatozoa of many fish have an extremely short functional life after spawning. Marimuthu & Haniffa, (2007) showed in case of Channa striatus fertilized egg were free floating, spherical, non-adhesive translucent and yellow in color. In case of Rita rita, Mollah et al., (2011) reported the same result but it was demersal and brownish in color. They reported a redish spot in the fertilized egg which indicates the blastodisc. Same blastodisc has been reported in case of Macrognathus aculeatus, Labeo bata, Anabas testudineus, Nandus nandus, Heteropneustes fossilis, Mystus cavasius, by Farid et al., (2008); Miah et al., (2009);Karim et al., (2012); Das et al., (2002); Nesa et al., (2017); Rahman et al., (2004). The diameter of fertilized and unfertilized eggs is varying in species to species. Fertilization rate, hatching rate, diameter of fertilized and unfertilized egg of different fish species are given in the Table 2.
The fertilization rate of different fish species is different. Fertilization rate are also season dependent in case of many species. Fertilization rate also differs depending on the natural or striping. The event of egg activation is thought to be the result from the introduction of protein or other component from the sperm plasma to the egg. The existence of some factors which are capable of triggering egg for activation has been reported by Coward et al., (2003). The majority of the evidence to date indicates that the critical sperm component is a phospholipase isoform (phospholipase zeta) Saunders et al., 2002). One of the exceptions of this was found in the study by Lee et al. (1999), which described the apparently normal activation as.ideasspread.org Agricultural Science Vol. 2, No. 1; of zebrafish egg in the absence of sperm. This may be defined as parthenogenic activation egg. In general, some morphological changes occur during fertilization while the egg is being activated. According to Kinsey et al. (2007), some morphological changes occur in the fish egg at fertilization like progressive disintegration of cortical alveoli, reduction in volume, transformation of the chorion, expulsion of second polar body, bipolar differentiation. Kusa (1953) says that the first observable change after fertilization involves the outline of the alveolus becoming indistinct. The alveolus then disappears. Till date no researches were recorded on egg activation of fishes of Bangladesh. Details study is needed for the proper knowledge about the activation of fish egg of Bangladesh.

Micropyle
There is no significant record of micropyle study of Bangladeshi fish. At the internal aperture of the micropylar canal a site of sperm attachment was found on the egg membrane (Kudo, 1982), recognized as a gentle cytoplasmic swelling, bearing 19-27 cytoplasmic finger-like projections (Kudo, 1982).

Embryonic Developmental Stages and Timing of Development in Different Fish Species
The timing of development is species specific and also stage specific, that means different developmental stage needs different time for each species. In Bangladesh, the developmental timing for all species is not well known. However, in case of some species, research shows some good findings. A complete chart on the timing of development is shown in the Table 3.

Organogenesis and Hatching Temperature
In organogenesis stage different organs of the fish are formed. In case of Bangladeshi fish, organogenesis is not well studied except only a limited number of species. In an experiment conducted by Farid et al. (2008) reported that organogenesis in case of Tara baim starts almost 11 hours after fertilization. Both tail and head ends were clearly differentiated and the beating heart was visible in this stage. Gills and pectoral fins start to appear. Auditory and optic vesicle develops. These aspects of organogenesis were similar to L. rohita ((Khan, 1943) and C. mrigala (Chakraborty and Murty, 1972). In another study in case of Labeo bata conducted by Miah et al. (2009) concluded that, at the organogenesis stage, appearance of heart rudiment pectoral fin buds and gill rudiment occurs. Notochord becomes visible, auditory and optic vessels developed in 16-18 hours after fertilization. Das et al. (2002) on the other hand, reported that organogenesis occurs 13 hours after fertilization. At this stage both tail and headend were clearly visible and heart beat starts in case of Nandus nandus. Out of this species discussed, there are many commercially important fish species which organogenesis are not well defined in the previous research. However, the pattern of organogenesis is found more or less similar in the species of the country. It may be due to similarity in environmental condition, food supply and geographical location.
Optimum incubation temperature for different fish species is different found. A list of optimum incubation temperature reported for different fish species of Bangladesh is presented in Table 4.

Post Hatching Development of the Hatched Larvae
Post hatching development means the development of the larvae from the hatching till metamorphosis. The pattern of post hatching development of different species is different. Timing of development is also dependent on some environmental factors, like temperature of the water, available DO of the water, salinity etc. A typical chart on the development timing of different fish species reported for Bangladesh is given in the Table 5.

Factors That Influence Embryonic Development
There are many factors that influences embryonic development of fish has been identified by different scientist. These factors may be categories into some category. These are internal factors like endocrine regulation of the fish or may be other external physico-chemical factors.

Endocrine Regulation
Study on endocrine regulation of the developing embryo is not well studied in Bangladeshi fishes except Shing and Koi. In case of Shing, Nesa et al., (2007) reported that a dorso-ventral unpaired fin, and some melanophores appeared on the head region, ventral side of the notochord and dorsal side of the body, probably by influence of some endocrine glands. Karim (2012) also reported some endocrine regulatory development of the Koi embryo, but didn't mentioned any special type of name of the gland. This two research clearly indicates that the development of early stages of the fishes are somehow regulated by the endocrine gland. But there is a lack of clear information that which gland is responsible for development of which organ. More research on this aspect is necessary in case of fish species of Bangladesh.

Physico-Chemical Factors
Embryonic stage is very crucial stage of a fish life. In this stage certain factors plays important role in the development of the embryo. There are many external factors that are responsible for regulation of the embryonic development of fish. These factors may be physical or may be chemical also. Temperature is the most vital factor that determines the proper development of the embryo. It has been proved as one of the major factors that regulate the development of the early embryonic stages of fish. Legendre & Teugels, (1991) indicated that temperature have an influence on the development of the embryo. In a study in case of Labeo bata embryonic and larval development were reported optimum from 27 °C-31°C . Similar influence of temperature was observed in case of Shol, koi, indigenous Magur, Shing, Taki, pabda, Pangas in discrete study conducted by Ramanathan et al., 1985;Karim et al., 2012;Singh & Vidyarthi, 1990;Benerji, 1975;Sarma et al., 2012;Ferosekhan et al., 2015, respectively. In a study conducted by Chattopadhyay and Chattoraj (2017), reported that gonadal development and spawning stops with the fall of temperature that happen with the approach of winter. This provides a straight indication that temperature along with photoperiod is the key controlling factor for maturation and spawning in fish. In case of spawning of fish such as carp and many other cyprinids, gonadal maturation begins in late winter or early spring. Therefore, it can easily be said that increasing temperature influence the maturation of gonad as well as influence the early developmental stages of fish which is also agreed by the result showed by Chakraborty et al., (2007) in case of Puntius sarana where the author found significant variation in the larval development in different temperature treatments. In case of Australian strain of Lates calcarifer the rate of embryonic development was positively correlated to the increase in incubation temperature and the thermal tolerance range for the Australian strain of L. calcarifer eggs was found to be 28-34 °C in a study conducted by Thepot and Jerry (2015). In case of Bangladeshi strain of L. calcarifer it may be more or less similar however it needs further research on Bangladeshi strain. In a study conducted by Das et al., (2006) reported highest hatching rate and least time for attaining each ontogenic stage at 31 > 33 > 26 > 36 °C and were significantly different (p < 0.05) in case of Labeo rohita. The lowest hatching percentage and maximum time duration for attaining a given ontogenic stage for L. rohita were observed at 36 °C and also resulted in malformed embryos. Another important factor that affect the embryonic development of fishes is salinity. In case of L. rohita, Pillai et al., (2003) reported that survivability limit of L. rohita embryo in waters up to 8 ppt salinity but best embryonic development was obtained at 0 to 2 ppt.
Deprived of temperature and salinity, there are some other factors that may have influence on embryonic development of the fishes in Bangladesh. This are sound, light, chemical compounds of water such as DO, pH, Alkalinity etc. (Rahman et al., 2011). But those factors are not well studied yet. Study on this factors that may influence the embryonic development is very important for Bangladeshi fish.

Conclusion
One of the major goals of fisheries biology is to inspect a fish stock and in terms of fisheries biology it is vital to know the embryonic and larval development. As these type of studies are essential to define the spawning periods and areas, to determine the chronological variations of the spawning period, to predict the mature stock of fish, to predict the rate of death of fish at the end of spawning period and to inspect the relation of the growth with its environment. In Bangladesh we need more research on the developmental biology of fishes, especially native or indigenous fish needs more concentration on this aspect.