2.1 Models of teleostean reproductive cycles
2.2 Reproductive cycles of other teleost groups
2.3 Photoperiod-thermoperiod relationship
A majority of teleost fishes are seasonal breeders, while a few breed continuously. Among the seasonal breeders, there is wide variation in the time of the year when breeding occurs. Fresh water temperate zone fishes spawn in spring and early summer, while others such as the salmonids do so in autumn. Fresh water fishes of the Murray-Darling river system of New South Wales, Australia, are stimulated to spawn when flood waters come into contact with dry soil (Lake, 1967). Similarly the fresh water fishes of the central Amazonian floodplain lakes spawn during the rainy season (Schwassmann, 1978). In the Indian subcontinent, a vast majority of the fresh water fishes breed during the monsoon season when rainfall is heaviest (Jhingran, 1975). The time of breeding of each species is so precisely timed that fry are produced in an environment in which the chances of survival are maximal. Natural selection possibly favours genomes of individuals that produce their young ones at a time most suitable for survival.
Due to paucity of information, an integrated concept of the impact of environmental factors on the reproductive process of fishes has not yet emerged. Nevertheless, it is known that fishes integrate their physiological functions with environmental cycles. It is now clear that endogenous periodicities of physiological processes are responsible in part for seasonal reproduction (Bullough, 1951, 1959; Sundararaj and Sehgal, 1970a; Sundararaj, 1978). In addition, certain proximate environmental factors that act as cues for the approaching favourable season for reproduction impinge on the exteroceptors and, through them, affect the central nervous system, the pituitary and, finally, the gonads. It is through such environmental factors that the endogenous rhythm is brought into phase for the precise breeding time. The literature on this topic has been reviewed by Pickford and Atz (1957), Atz and Pickford (1964), Schwassmann (1971, 1978), de Vlaming (1972a, 1974), Donaldson (1973), Sundararaj and Vasal (1976), Peter and Hontela (1978) and Peter and Crim (1979).
Photoperiod, temperature and seasonal rainfall, among other factors, are important in regulating reproductive cycles in teleost fishes. They show considerable but precisely-timed annual fluctuations in temperate regions, whereas in the tropics, dry seasons alternate with wet ones and lead to seasonal differences in water quality and food availability.
In many salmonids, that spawn in autumn, gradually increasing photoperiods followed by decreasing ones or even short photoperiods play a dominant role in the regulation of reproductive cycles. In cyprinid and perciform fishes, temperature may also be a significant regulatory factor in the reproductive cycling. Thus, even among teleost fishes, mechanisms for reproductive timing vary considerably. A comprehensive and meaningful assessment of the regulatory role of environmental factors on teleost reproductive cycles is not yet possible in view of the diverse experimental conditions, the lack of proper controls and the short-term nature of many of the experiments. Only 51 out of nearly 20 000 species of fishes have so far been experimented upon (see Htun-Han, 1977; Poston, 1978).
Nevertheless, it is possible to select a few teleost species that have been studied more intensively than others to serve as models for developing a working hypothesis for environmental regulation of reproductive cycles. They are the catfish, Heteropneustes fossilis; the rainbow trout, Salmo gairdneri; and the brook trout, Salvelinus fontinalis; the grey mullet, Mugil cephalus, and the common carp, Cyprinus carpio.
2.1.1 Catfish, Heteropneustes fossilis
2.1.2 Rainbow trout, Salmo gairdneri and brook trout, Salvelinus fontinalis
2.1.3 Grey mullet, Mugil cephalus
2.1.4 Common carp, Cyprinus carpio
The catfish, a native of India, Burma and Sri Lanka, is a seasonal breeder. Its annual gonadal cycle in the vicinity of Delhi (lat. 28°35'N; long. 77°12'E) comprises the preparatory (February to April), the prespawning (May to June), the spawning (July to August), and the postspawning (September to January) periods. Two consecutive sets of physiologic events intimately interwoven with environmental changes are involved in the completion of the circannual reproductive cycle in the catfish. The first set of events leads to the gradual enlargement of the gonads with concomitant vitellogenesis or spermatogenesis during the late preparatory-prespawning period, when in nature both the daily photoperiod and mean environmental temperature increase progressively (Nayyar and Sundararaj, 1970a; Sundararaj and Sehgal, 1970a, b, c; Sehgal and Sundararaj, 1970a, b; Sundararaj and Vasal, 1976; Vasal and Sundararaj, 1976). The second set of physiologic events, involving ovulation and spawning of oocytes or spermiation, seems to be triggered by a consortium of environmental factors prevailing during the monsoon season (July to August) - the prime time for breeding in the environmental niche. The catfish as also other fishes living in these latitudes appear to anticipate the monsoon season by the preceding warm dry summer when photoperiod is long and temperatures are warm.
A significant increase in ovarian weights as well as in the formation of yolky oocytes can be brought about even during the preparatory period (ambient water temperature 15.5-17°C) by exposing the catfish to photoperiod regime of LD 12:12 or 14:10 for 36 days provided the water temperature is maintained at 25°C or above up to 34°C. The threshold temperature for the formation of yolky oocytes appears to be 25°C; the tempo of vitellogenesis increases at higher temperatures and comes to a virtual halt at lower ones. During the postspawning period (November) a significant increase in ovarian weight with concomitant vitellogenesis is observed only in catfish exposed to 30°C for 60 days, irrespective of photoperiod. Since this catfish regulates its body temperature by behavioural means (the preferred temperature is 31.3° to 32°C), it is not surprising that the rate of ovarian recrudescence is very rapid around 30°C (Vasal and Sundararaj, 1976, 1978). In the male catfish, the optimum temperature for the onset and maintenance of spermatogenesis is 25°C and higher temperatures do not alter the tempo of spermatogenesis.
During the postspawning period, ovarian regression in the unspawned catfish is retarded more effectively by a temperature of 30°C than by cooler temperatures (25°C), regardless of photoperiod. Nevertheless, ovaries eventually regress in the first week of October (Vasal and Sundararaj, 1976). It is apparent that in this species termination of the reproductive phase is endogenously timed, and the postspawning ovarian regression is obligatory even under constant laboratory conditions. The annual ovarian cycle of the catfish is primarily influenced by seasonal temperature variations while photoperiod plays an important but facilitatory role.
Mature female catfish exposed for almost 3 years to continuous illumination (LL) or darkness.(.DD) at 25°C still show a circannual ovarian rhythm comparable to that seen in fish collected from nature (NL). However, there is a change in period length, at least in LL, as evidenced by the fact that the acrophase (period when ovarian weight is maximal) occurs earlier in LL than in DD or NL, and what is more important, the interval estimate of the circannual acrophase in LL does not overlap with the corresponding interval estimate for the data from NL. Thus the computed acrophase differences establish, at least indirectly, a circannual rhythm desynchronization (Sundararaj, Vasal and Halberg, 1973; Sundararaj, 1978). A circannual ovarian rhythm expresses itself, albeit slightly out of phase, even under constant environmental conditions. It appears that daylength and temperature act as synchronizers to bring the ovarian rhythm into phase.
Even though the catfish responds to photoperiod, the mechanisms involved in the measurement of daily photoperiod are not clear. Interruption of the scotophase (dark period) of a short day (LD 6:18) by 1 hour of light induces ovarian recrudescence that is significantly greater than that obtained in the control group exposed to LD 7:17. Obviously, the catfish has in addition to a circannual rhythm, a circadian rhythm of photosensitivity with two sensitive periods occurring between 16-17 h and 20-21 h after the onset of the daily photo-period (Vasal and Sundararaj, 1975).
Extensive basic research on the role of environmental factors in the regulation of breeding cycles of the catfish has been made use of to harvest multiple crops of eggs at monthly intervals in this species. Precociously gravid catfish obtained as early as April by photothermal treatment have been induced to spawn in the laboratory by administration of ovine luteinizing hormone (LH). Ripe eggs after fertilization hatched into seemingly normal fry. Further, the spent fish when subjected to the same photothermal treatment developed fresh crop of yolky eggs within one month; such gravid females have been again induced to spawn with LH. This process has been repeated so that the same set of fish has been spawned four times between April and July of the same year. Thus, it is possible to get catfish fry not only early but also in much larger numbers than usually available from each female during the spawning season (Anand and Sundararaj, 1974a; Sundararaj and Vasal, 1976). The aquacultural potentialities of this laboratory observation are very considerable.
In autumn-spawning rainbow trout, photoperiod is the main factor involved in gonadal development (Nomura, 1962; Goryczko, 1972; Kunesh et al., 1974; Breton and Billard, 1977; Poston, 1978; Whitehead et al., 1978a). In this fish, gametogenesis occurs in summer and autumn and is associated with decreasing photoperiod and possibly temperature (Billard and Breton, 1978; Billard et al., 1978). Long (LD 16:8) or short (LD 8:16) photoperiod and even continuous illumination do not induce gonadal recrudescence, whereas a decreasing photoperiod (from LD 16:8 to LD 8:16) from February to June induces full spermatogenesis and spermiation. Plasma gonadotropin levels and tempo of spermatogenesis are significantly elevated at decreasing photoperiods and warm (16°C) rather than at cool (8°C) temperatures showing that temperature is indeed a factor, though not limiting, in trout reproduction (Breton and Billard, 1977). Whitehead et al. (1978a, b) have advanced spawning by 6-12 weeks in rainbow trout by exposing them to normal yearly photoperiod cycles condensed into 9 or 6 months at 9°C. These results show that telescoped or accelerated versions of the annual daylength cycle such as increasing followed by decreasing photoperiod induce earlier gonadal recrudescence in the rainbow trout. Photoperiod appears to be the major environmental factor involved in the sequence of endocrine events leading to spawning and suggests that it may act by modifying an inherent reproductive rhythm (see Billard et al., 1978).
In the brook trout, which also spawns in autumn, exposure to an accelerated light regime of increasing followed by decreasing photoperiods results in precocious functional maturity (Henderson, 1963; Carlson and Hale, 1973; Htun-Han, 1977).
The grey mullet in Hawaiian waters is a seasonal breeder and spawns during January and February. In nature, vitellogenesis commences shortly before the attainment of minimal day-length (Kuo, Nash and Shehadeh, 1974a, b; Kuo and Nash, 1975). The vitellogenic response to artificial photoperiod cycle has been examined by comparison of ovarian recrudescence in females exposed to either a condensed daylength cycle or a natural daylength cycle at ambient temperatures. The results show that constant short photoperiod regime of LD 6:18 was effective in stimulating vitellogenic oocytes within 49-62 days, whereas in controls, vitellogenic oocytes did not appear up until 235 days. Thus, in the mullet, ovarian recrudescence can be triggered out of season by a photoperiod-temperature combination of LD 6:18 at 21°C (Kuo and Nash, 1975). Kuo, Nash and Shehadeh (1974b) have successfully prolonged the breeding season of mullet to obtain ripe eggs throughout the year.
In the common carp, the pattern of reproductive cycle is dependent more on temperature than on photoperiod. In Israel, the carp normally breeds in April and May (Moav and Wohlfarth, 1973). Maintenance of carp at a warm temperature (23°C) accelerates ovarian recrudescence and spawning (Gupta, 1975). In India, the common carp shows two main peaks of breeding activity in a year, once during spring and again in autumn when optimal thermal conditions prevail in nature. In France, the common carp spawns in the summer. Pituitary concentration of gonadotropin as measured by radio immunoassay, is low in winter and increases in spring at the time of gonadal recrudescence and in the spawning season (Billard and Breton, 1978). Plasma gonadotropin increases in late winter and decreases in spring when ovarian weights are highest (Billard et al., 1978). Spermatogenesis occurs in summer and early autumn and plasma and pituitary gonadotropins increase at this time. Spermiation takes place from June to October but is blocked up until the following spring or summer when thermal conditions promote spawning. Therefore, gonadal development in the carp is associated with increasing temperature and spawning occurs when the temperature is at its maximum (Billard and Breton, 1978).
Bieniarz et al. (1978) reported that carps in Poland attain sexual maturity in 4-5 years and spawn in late May when water temperature reaches 18°C. Fresh vitellogenesis starts within 2 months after spawning and is associated with high serum levels of gonadotropin (July-September). Thereafter, the gonadotropin levels remain low but increase at the time of spawning. Atresia of oocyte is associated with the lowest levels of gonadotropin when water temperatures are below 14°C.
2.2.2 Indian major carps and Chinese carps
2.2.3 Snappers and groupers
2.2.4 Prochilodus sp. and Brycon sp.
2.2.5 Milkfish, Chanos chanos
2.2.6 Miscellaneous teleost species
Many species of the genus Sarotherodon (Tilapia) have been studied not only in the tropics but also in the equatorial zone. They show seasonal reproductive activity even though photoperiod and temperature are relatively constant throughout the year in the equatorial zone. Hyder (1970) reported that in Sarotherodon (Tilapia) leucosticta, Sarotherodon (Tilapia) nigra, Sarotherodon (Tilapia) zilli of the equatorial zone, testicular activity is restricted to autumn and winter, and testes and ovaries are in resting phase from July-September. Ovarian development occurs in Sarotherodon (Tilapia) leucosticta during the period of highest temperature and maximal sustained light. Spawning is associated with the period of highest temperature and onset of rainy season. The regulatory role of photoperiod is, however, not properly understood. However, at the same latitude, the duration of the breeding season varies with the altitude and possibly with temperature (Billard and Breton, 1978). Increasing water temperature above 22°C induces ovarian growth and spawning in Sarotherodon (Tilapia) aurea (Fishelson, 1966). In Sarotherodon (Tilapia) aurea kept at 30°C, the plasma levels of testosterone, 11ß-hydroxytestosterone, 11-ketotestosterone and 11-deoxycorticosterone are considerably higher than in those kept at 18°C (Katz and Eckstein, 1974).
Indian major carps, Labeo rohita, Catla catla and Cirrhina mrigala, show gonadal recrudescence as early as March in Assam (lat. ca. 25°N), June in Orissa (lat. ca. 20°N) and July in other parts of India depending on their geographical location (Khanna, 1958; Jhingran, 1975). Since the Indian major carps show gonadal recrudescence from March to June, at a time when both photoperiod and temperature are increasing, it is surmised a posteriori that these two factors may be involved in initiating gonadal recrudescence. To date, experimental work has been conducted on only one species of Indian carp, Cirrhina reba, a closely allied species to the commercially important Indian major carps (see Verghese, 1967, 1970, 1975). Exposure of males and females to a long photoperiod (LD 14:10 or 18:6) at ambient temperatures (19° to 30°C) hastens gonadal recrudescence; males attain maturity earlier than females. However, when fish are subjected to gradually increasing photoperiod from LD 4:20 to 14:10 and finally to 20:4, females mature earlier than males at ambient temperatures, whereas at elevated temperatures (27.1° to 31°C), males mature earlier than females (Verghese, 1970). Further, males kept in constant darkness mature simultaneously with those under natural photoperiod, whereas in females, constant light hastens and constant darkness retards functional maturity (Verghese, 1975). Since the males of the Indian major carps show gonadal recrudescence earlier than females under natural conditions, it is surmised that the threshold temperature for testicular recrudescence is lower than that for ovarian recrudescence. Properly designed experiments with rigorously controlled photoperiod-temperature regimes have to be conducted to understand the relative roles of these two factors in gonadal recrudescence.
Chinese carps have been reared in temperate and tropical climes and they attain sexual maturity earlier in the tropical (2 years) than in the temperate waters (10 years). Warm temperatures and long photoperiod coupled with good diet are responsible for accelerated growth and gonadal maturity.
Spawning in the Indian major carps is precipitated by environmental factors that prevail during the rains or the monsoon season. However, in standing waters they develop the roe but do not spawn and this problem remains yet unsolved (see Sinha, Jhingran and Ganapati, 1974). In West Bengal and Madhya Pradesh, Indian major and Chinese carps spawn in wet 'bundh' type tanks where fluviatile conditions are simulated during monsoon rains (Dubey and Tuli, 1961; Sinha, Jhingran and Ganapati, 1974; Jhingran, 1975). Even though some attempts have been made to study the environmental factors that prevail in the bundhs at the time of spawning no definitive information is available. The role of sandy laterite, muddy or clayey soils in triggering spawning in wet and dry bundhs has not been studied. Rains bring about an increase in the level and velocity of flow of water, flooding of shallow areas, dilution of certain ions and concentration of others, changes in smell and taste of water, as well as biotic parameters such as growth of algae and other green vegetation. Specific combinations of some or all of these factors are perceived through exteroceptors of fish and conveyed to the hypothalamus which then activates the pituitary to produce gonadotropin to induce maturation, ovulation and spawning.
Indian major carps, Labeo rohita, Catla catla, and Cirrhina mrigala, are known to breed only once a year during the monsoon season. However, after spawning had been induced by hypophysation in June, the spent fish became gravid again and could be spawned a second time by hypophysation (Bhowmick et al., 1977). Chen, Chow and Sin (1969) have reported multiple spawning cycles in a single year in Chinese carps in Malaysia. Bighead carp and silver carp have been spawned almost at monthly intervals in Malacca (Harvey and Hoar, 1979). These are encouraging observations and will help obtain more spawn from the same fish in one season. Similar work should be extended to other cultivated species to increase the availability of quality fish seed.
Spawning in the groupers (Serranidae) and snappers (Lutjanidae) in the Caribbean is virtually confined to the period between January and May. But the peak in spawning is reached when the water temperatures are minimal between January and April (Munro et al., 1973) Arnold et al. (1978) have reported that the red snapper, Lutjanus campechanus, spawned in captivity when held at temperatures and photoperiods which approximated normal conditions in the Texas Gulf of Mexico region. They also observed multiple spawns in May and June. It is worthwhile extending such studies to other related cultivated fishes.
Important food fishes in the Central Amazonian floodplain lakes such as Prochilodus sp. and Brycon sp., spawn during the rainy season when the water level in the lake system begins to rise. Females have fully developed ovaries by January-February (Schwassmann, 1978).
Kuo and Nash (1979) have reported on the annual reproductive cycle of the milkfish in Hawaiian waters. It has a short breeding season between June and August and their data suggest a synchronous spawning behaviour.
The role of photoperiod and temperature in the reproductive cycling of other teleost species has been summarized by de Vlaming (1972a, 1974), Htun-Han (1977) and Peter and Crim (1979). In many temperate zone freshwater fishes that spawn in spring or early summer, gonadal recrudescence takes place in winter or spring in response to increasing photoperiod and rising temperatures, some fishes being more dependent on the one factor than on the other. In Phoxinus laevis (Bullough, 1939), Carassius auratus (Kawamura and Otsuka, 1950), Gambusia affinis (Medlen, 1951), Fundulus confluentus (Harrington, 1959), Etheostoma lepidum (Hubbs and Strawn, 1957), Cymatogaster aggregata (Weibe, 1968) and Heteropneustes fossilis (Vasal and Sundararaj, 1976) vitellogenic response is a function of warm conditions and seems to preclude any photoperiodic effect. However, warm temperature along with a long photoperiod augments gonadal development in Notropis bifrenatus (Harrington, 1957), Gasterosteus aculeatus (Baggerman. 1957, 1972; Schneider, 1969), Oryzias latipes (Yoshioka, 1962, 1963), Sarotherodon (Tilapia) leucosticta (Hyder, Shah and Krischner, 1970), Lepomis cyanellus (Kaya and Hasler, 1972) and Notemigonus crysoleucas (de Vlaming, 1975b).
In the ayu, Plecoglossus altivelis, short photoperiod (LD 8:16 at 14°-19 C) accelerates and long photoperiod (LD 16:8 or 20:4 at 14°-19°C) retards maturation in both sexes and the minimum light intensity that retards maturation is 0.1 Lux for males and 0.2 Lux for females (Shiraishi, 1965a, b, d). Further, long wavelengths (red and yellow) retard gonad maturation, while short wavelengths (blue and green) accelerate gonadal maturation (see Shiraishi, 1965c).
A period of posts pawning refractoriness that marks the end of reproductive activity and prevents the immediate recurrence of gonadal recrudescence has been demonstrated in the stickleback, Gasterosteus aculeatus (Baggerman, 1972), the cyprinid fish, Notropis bifrenatus (Harrington, 1957), the catfish, Heteropneustes fossilis (Sundararaj and Vasal, 1976), and the medaka, Oryzias latipes (Egami and Hosokowa, 1973). The refractoriness is overcome in some species by exposure to low temperatures and/or decreasing photoperiods (Sundararaj and Sehgal, 1970c; de Vlaming, 1974; Peter and Crim, 1979). In the cyprinid fish, Couesius plumbeus, the early stages of spermatogenesis are favoured by low temperatures (Ahsan, 1966a), while in the golden shiner (de Vlaming, 1975b) and the goldfish (Gillet, Breton and Billard, 1978), lower temperatures favour early stages of oogenesis and warm temperatures inhibit oogenesis in the goldfish (Gillet, Breton and Billard, 1978) and the sunfish, Lepomis cyanellus (Kaya, 1973).
A few marine and estuarine temperate-zone fishes have been studied. In the viviparous seaperch, Cymatogaster aggregata, males and females respond to different environmental cues (Wiebe, 1968).Warm temperatures and short photoperiods of late summer accelerate ovarian recrudescence, while final oocyte maturation occurs under cold temperatures. In males, cold temperatures favour spermatogonia formation, while warm temperatures and long photo-period stimulate later stages of spermatogenesis. Although copulation occurs in the summer months, fertilization of the mature oocytes takes place only later, by spermatozoa stored during the intervening period. In the marsh killifish, Fundulus grandis, the early stages of gametogenesis are dependent on cold temperatures, while rapid gonadal recrudescence is stimulated by warm temperatures (de Vlaming, 1972a). In the winter-spawning estuarine gobiid fish, Gillichthys mirabilis, temperature is the primary environmental cue; cool temperatures stimulate gonadal recrudescence, whereas warm temperatures induce gonadal regression (de Vlaming, 1972b). In the dab, Limanda limanda, exposure to accelerated photoperiod at 11°C in six months similar in pattern to a normal year's cycle resulted in the formation of ripe eggs 2-3 months ahead of the season, while in turbot, Scophthalmus maximus and Solea solea, long photoperiod (LD 18:6 or 20:4) induced formation of ripe eggs (Htun-Han, 1977). In the rabbit fish, Siganus caniculatus, long photoperiod (LD 18:6 at 29°C) retards gonadal development in both sexes, while short photoperiod (LD 12:12) does not (Lam and Soh, 1975).
In teleost fishes which are ectotherms, the principal mode of thermoregulation is behavioural, involving exploitation of thermal heterogeneity in the environment by swimming into desired areas and remaining there. Behavioural thermoregulation has been demonstrated in over 100 species of teleost fishes of which only a few are cultivated (see Coutant, 1977).
The assumption that thermal control of metabolism and reproduction in ectothermic vertebrates is merely concerned with providing optimal temperatures for enzyme activities and receptor-hormone complexes is no longer valid in view of the new evidence in some fishes. Recently, a photoperiod-thermoperiod relationship on body and testicular weight gain in goldfish subjected to increased temperatures at one of six different times in a 24-h period has been demonstrated (Spieler et al., 1977). Depending upon the time of day when the thermo-cycle is commenced, body and testicular weight gain can be stimulated or inhibited. This interesting observation is similar to the presence of a daily rhythm in photoresponsiveness with sensitive phases occurring between 12-18 h, after onset of photoperiod in the case of Gasterosteus aculeatus (Baggerman, 1972) and between 16-17 h and 20-21 h after the onset of photoperiod in Heteropneustes fossilis (Vasal and Sundararaj, 1975).
In the marsh killifish, Fundulus grandis, where both prolactin and cortisol levels show circadian rhythmic variations, warm temperature (28°C) produces a 16-h relation between the hormone rhythms (prolactin peak occurs 16 h after the cortisol peak) and cool temperature (20°C) produces 0-h relation between rhythms (Meier et al., 1978). Further, injections of cortisol and prolactin in the 0-h and 16-h relations establishes winter and summer conditions, respectively. The winter conditions stimulate gonadal growth and preference to saline waters.
The physiological basis and ecological implications of this chronobiological approach is of considerable importance to aquaculture and may hold the key to producing precociously gravid fish. Such studies should be validated and extended to other fresh water and brackish water species of cultivated fishes. Timed application of warmth into fish ponds or even into recirculating systems can optimize growth and reproduction.
The above review indicates that gonadal recrudescence is chiefly regulated by seasonal variations in photoperiod and temperature, while spawning is controlled by temperature and/or rainfall. The environmental information is converted to neural inputs by the sensory receptors and this neural information is transduced into a hormonal output via hypothalamic releasing hormones and finally the pituitary which releases the gonadotropic hormone(s). This leads on to the study of the endocrinology of reproduction in fishes viz., the hypo-thalamus, the pituitary and the gonad.