Fish Sci (2010) 76:769–776 DOI 10.1007/s12562-010-0272-0
ORIGINAL ARTICLE
Biology
Effect of temperature and photoperiod on the reproductive condition and performance of a tropical damselfish Chrysiptera cyanea during different phases of the reproductive season Mohammad Abu Jafor Bapary • Akihiro Takemura
Received: 12 January 2010 / Accepted: 23 June 2010 / Published online: 5 August 2010 Ó The Japanese Society of Fisheries Science 2010
Abstract Effects of temperature and photoperiod on the reproductive activity of a reef associated tropical damselfish Chrysiptera cyanea were evaluated under three phases with different environmental patterns, phase I (April–May; increasing water temperature and photoperiod), phase II (June–July; increasing water temperature and peak/ decreasing photoperiod), and phase III (August–September; peak/decreasing water temperature and decreasing photoperiod). When the fish were reared at 20, 25, or 30°C under natural photoperiod, the reproductive conditions differed within and among the phases depending on experimental temperature and environmental patterns. From phases I through III, ovaries with vitellogenic oocytes were notable only at 25°C, whereas regressing and immature oocytes were noticed at 20 and 30°C. The fish underwent active spawning at 25°C, whereas no or few spawnings were observed at other temperatures. In phase III, there was a resultant prevention of decrease in the gonadosomatic index and disappearance of vitellogenic oocytes in the ovaries of fish under a long photoperiod (LD14:10) compared to those under a short photoperiod (LD10:14). These results indicate that a long photoperiod with a suitable range of water temperature is a principal determinant in continuity of reproductive activity and performance, and that a high temperature has a negative impact on their ovarian development.
M. A. J. Bapary A. Takemura (&) Department of Biology, Chemistry and Marine Sciences, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan e-mail:
[email protected]
Keywords Damselfish Ovarian development Histology Photoperiod Pomacentridae Spawning Temperature
Introduction Fish inhabiting temperate and higher latitudes exhibit a restricted annual reproductive cycle that is influenced by the periodic changes of temperature and photoperiod [1–3]. Entrainment of the gonadal development to the annual changes in these environmental factors is a form of safety assurance to increase the chance of prospective encounters with sexually matured partners as well as maximize the subsequent survival of their offspring. The importance of these environmental factors in the initiation and termination of their reproductive activities seems to differ among fish species; the gonadal development of some fish is entrained to the period when there is an increase in photoperiod and temperature [4, 5], whereas that of the others progresses during the period when these factors exhibit a decrease [6]. Although these environmental cues are considered to participate integrally in increasing the reproductive activity, the manner in which they are perceived by the sensory organs of the fish and transduced as endogenous stimuli is not fully understood. Fish inhabiting low latitudes undergo reproductive activity under environmental conditions characterized by low photoperiod and temperature variation [7, 8]. This environmental characteristic of low latitudes leads to the general perception that fish inhabiting tropical regions utilize changes in the other environmental cues of these regions in order to entrain their reproductive activity. In fact, it has been reported that the reproductive activities of certain Pomacentridae species are related to the tropical
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monsoon climate and are influenced by the periodic rainfall and wind changes that are associated with this climate [9, 10]. Similarly, the influence of temperature is well documented in certain damselfish species [7, 11, 12]. It has also been reported that photoperiod is the most important environmental factor regulating the reproductive rhythm in the sergeant major Abudefduf saxatilis found in Sa˜o Paulo, Brazil [13], and in the Indian carp Catla catla found in Santiniketan, India [14]. It is likely that the fish of tropical origin can respond flexibly to regional changes in various environmental cues in order to extend their breeding period and increase chances of reproductive success. In this regard, it has been reported that the little spinefoot Siganus spinus inhabiting the tropical regions has two reproductive seasons—a sign of entrainment to the tropical monsoon [15]—whereas the same species inhabiting the subtropical regions actively reproduces only once a year when the regions experience increases in photoperiod and temperature [16]. Similar findings have been obtained in the case of the orange-spotted spinefoot S. guttatus that inhabits the region in Karimunjawa, Indonesia [17], and Okinawa, Japan [18]. The spinefoot species that have adapted to the subtropical environments may superficially express the characteristic nature of the teleost fish inhabiting higher latitudes. Therefore, it is hypothesized that the utilization of regional and species-specific environmental cues is superimposed on the perception of fundamental environmental factors such as photoperiod and temperature. The sapphire devil Chrysiptera cyanea is a reef-associated damselfish that originates in tropical regions and is widely distributed in the coral reefs of the West Pacific Ocean [19]. A previous report has shown that the sapphire devil can initiates gonadal development during its nonreproductive season in Okinawa, when they were exposed to long photoperiodic conditions; rearing the fish at 25 and 31°C resulted in induction of vitellogenic oocytes within 60 and 15 days, respectively [8]. Although this result indicates that photoperiod and water temperature integrally regulate gonadal development of this species in the subtropics, it is still unclear how changes in these environmental factors are involved in continuing its reproductive performance during a reproductive season lasting 5 months, i.e., from April to August, when water temperature normally ranges from 24 to 30°C. The aim of this study was to examine the importance of water temperature and photoperiod in the maintenance of reproductive activities in the sapphire devil during its reproductive season. We divided the reproductive season into three phases in accordance to the periodic changes in natural environments and reared the fish under controlled conditions of water temperature or photoperiod in each phase. The ovarian histology and spawning frequency of the fish were compared among the experimental groups.
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Materials and methods Experimental fish and experimental designs The matured female sapphire devil with a body mass ranging from 1.57 to 3.96 g was collected using hand nets during daytime low tides from coral reefs (26°420 N, 127°520 E) around Okinawa Island, Japan, during the reproductive season. These fish were subsequently taken to Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, Japan. They were kept in polystyrene stock tanks (0.5 metric ton capacity) filled with running seawater to acclimate for 5–7 days. They were fed daily at 1000 h with commercial pellets (Fry Feed Kyowa C1000; Scientific Feed Laboratory, Tokyo, Japan). The experiments were conducted during the reproductive season under three distinct phases characterized by different natural environmental conditions. These phases extended from April to May (phase I, marked by increasing water temperature and photoperiod), from June to July (phase II, marked by increasing water temperature and peak/decreasing photoperiod), and from August to September (phase III, marked by peak/decreasing water temperature and decreasing photoperiod) (Fig. 1). To examine the effects of temperature on the reproductive activity under natural photoperiod, the fish (male:female = 1:5) were transferred in each phase from the stock tanks into glass aquaria (60-l capacity) equipped with a filtration and aeration system. A few plastic pipes (80–90 mm in long and 40 mm in diameter) used as spawning substrates were put onto the bottom of the aquaria. In each phase, these fish were reared for 45 days at fixed water temperatures of 20, 25, and 30°C (±1°C). They were fed the aforementioned commercial pellets daily at 1000 h. The female fish (n = 6–7) were sampled every 15 days from each aquarium after onset of the experiment.
Fig. 1 Monthly changes in photoperiod and water temperature in the experimental region
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Following anesthetization with 2-phenoxyethanol (Kanto Chemical, Tokyo, Japan), the fish were weighed and then decapitated. The ovaries were removed from their body cavities and weighed. The gonadosomatic index [GSI = (ovary mass/body mass) 9 100] was calculated for each fish. The spawning frequency of the fish was also checked under the same temperature regimes. For this experiment, 18 aquaria (20-l capacity) with ambient aeration were set up, and one pair of the fish (1 male and 1 female) was transferred to each aquarium in phase I. Plastic pipes functioning as spawning nests were put on the bottom of each aquarium. The aquaria consisting of the fish pairs were divided into three groups (n = 6) that were reared under controlled temperatures of 20, 25, and 30°C (±1°C). The commercial pellets were given to them daily at 1000 h. During the experimental period, the presence of fertilized eggs on the pipes was monitored daily by the naked eye, and the pipe was replaced with a new one when the eggs were found in the pipe. The total number of spawnings (spawning events per group) was recorded. Effects of photoperiod on the reproductive activity were examined in the present study. In phase I, 15 glass aquaria (60-l capacity) comprising running seawater and ambient aeration were set. One pair of the fish from the stock tank was transferred to each aquarium. Plastic pipes functioning as spawning nests were put onto the bottom of the aquaria. The aquaria containing the fish pairs were divided into three groups (n = 5) and reared under the natural water temperature and three different photoperiodic conditions, i.e., short photoperiod (LD 10:14; light on 0800–1800 h), long photoperiod (LD 14:10; light on 0600–2000 h), and natural photoperiod (NP, lighting hour varied in accordance with the season). The commercial pellets were given daily at 1000 h. During the experimental period, the presence of the eggs on the pipes was monitored daily by the naked eye, and the total number of spawnings was recorded and compared for each phase. At the end of the experiment (phase III), the female fish were anesthetized and then decapitated. Their ovaries were removed from the body cavities, weighed for measurement of GSI, and subjected to histological observation. Histological procedures Pieces of the fish’s ovaries were fixed in Bouin’s solution for histological observations. Following dehydration with a series of ethanol and permutation with benzene, the ovaries were embedded in histoparaffin (Paraplast plus; Sigma, St. Louis, MO), serially sectioned at 7 lm, and then stained with Delafield’s hematoxylin-eosin for microscopic observation. On the basis of the oocyte staging of the white-spotted spinefoot S. canaliculatus [20], the oocytes in the ovaries of the sapphire devil were classified into the
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following stages of development: peri-nucleolus (PNS), oil-droplet (ODS), primary yolk (PYS), secondary yolk (SYS), and tertiary yolk (TYS) stages. The post-ovulatory follicles (POF) of the ovaries were used as the indicators of spawning [18]. Statistical analyses The data were expressed as the mean ± standard error of the means (SEM) and analyzed by a one-way analysis of variance (ANOVA). A two-way ANOVA was used when the effects of temperature were analyzed at different day intervals. When significant differences were found in the course of the above, a post hoc test was performed, which was then followed by Tukey’s HSD (Honestly Significant Differences) test.
Results Effect of temperature on reproductive activities under natural photoperiodic conditions Figure 2 shows changes in GSI of the sapphire devil that were reared at fixed temperatures under natural photoperiodic conditions during the reproductive season. There was no significant difference in GSI among the temperature groups at day 15, 30, or 45 in phase I, although relatively low GSI was observed in the group at 30°C (Fig. 2a). In phase II, GSI among three temperature groups did not change within 15 days after the onset of the experiment. However, significantly lower GSIs were observed in the fish groups at 30°C at day 30 as well as in those at 20 and 30°C at day 45 (Fig. 2b). In phase III, GSI was significantly higher at day 15 in the fish reared at 25°C and at day 30 at 20 and 25°C than at 30°C. A similar result was also obtained at day 45, although the values of all the fish sampled remained relatively low during this phase (Fig. 2c). Table 1 and Fig. 3 show the changes in ovarian development of the sapphire devil under various temperature conditions during different phases of the reproductive season. Ovaries initially contained vitellogenic oocytes at TYS in phase I and II, and from PYS to TYS in phase III. In phase I, ovaries of the fish reared at 20°C for 15 days contained many vitellogenic oocytes at TYS (Fig. 3a). Vitellogenic oocytes were also observed in the ovaries of the fish reared at 25 and 30°C; most ovaries of the 25°C group contained POF and oocytes at PYS to TYS (Fig. 3b), whereas many regressing as well as atretic oocytes at TYS were found in the ovaries of the 30°C group (Fig. 3c). Similar ovarian features were observed in ovaries of the fish reared at the same temperatures for 30 and 45 days. In
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experimental period, although their frequency decreased in phase III (Table 2). No and few spawnings occurred in the pairs reared at 20 and 30°C, respectively. Effect of photoperiod on reproductive activities under natural water temperatures Spawning performance of the fish reared under different photoperiodic conditions was compared among three phases (Table 3). Spawning was confirmed in all the groups in phases I and II. During these phases, the fish pairs reared under conditions of long and natural photoperiods showed a similar spawning frequency. Fish reared under short photoperiodic conditions had lower spawning frequency than those reared under long and natural photoperiodic conditions. In phase III, spawning was evident only in the pairs reared under long photoperiodic conditions. When ovarian activities among the groups in phase III were compared, GSI was significantly higher in the females reared under long photoperiodic conditions than in those reared under short and natural photoperiodic conditions (Fig. 4). The ovaries of the females reared under short and natural photoperiodic conditions were occupied by the immature oocytes at PNS (Fig. 5a). On the other hand, many vitellogenic oocytes at TYS were observed in the ovaries of the fish kept under long photoperiodic conditions. A few oocytes undergoing regression were also evident in some of the ovaries of this group (Fig. 5b).
Fig. 2 Changes in gonadosomatic index (GSI) of the female sapphire devil at various temperature conditions during different phases of the reproductive season. The fish (n = 25) were reared for 45 days from April to May (phase I, a), from June to July (phase II, b), and from August to September (phase III, c). White, gray, and black columns indicate GSI of the fish reared under conditions of 20, 25, and 30°C, respectively. Each value represents mean ± SEM. Different letters indicate significant difference at P \ 0.05
phase II, well-developed ovaries with POF were observed in the fish reared at 25°C throughout the experimental period. On the other hand, atretic oocytes at TYS were seen in few ovaries of the fish reared at 20 and 30°C within 15 days (Fig. 3d). Ovaries of the fish reared at 20°C within 45 days and at 30°C within 30 days were exclusively occupied by immature oocytes at PNS (Fig. 3e). Similar features in ovarian histology were also obtained at 20 and 30°C in phase III, whereas in some ovaries of the fish reared at 25°C, oocytes at ODS and PYS were found even at the end of the experimental period (Fig. 3f). The spawning performance of fish pairs was compared among the phases after exposing them under above programmed temperature conditions. Active spawning was repeated in the fish reared at 25°C throughout the
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Discussion It was previously reported that the sapphire devils inhabiting the subtropical regions show a periodic change in their reproductive activity, which increases in phase I (April and May) and, thereafter, decreases gradually from phase II (June and July) to phase III (August and September) [8]. The overall pattern of the reproductive activity of these fish in the present study was nearly identical to that in the previous study, although the fish in this study were reared under different temperature or photoperiod conditions. The present study obviously demonstrated that the reproductive performance of this species during the reproductive season is influenced by these environmental factors. The GSIs of all the fish reared at different temperatures were high during phase I. Many POFs were observed among the vitellogenic oocytes in the ovaries at 25°C, whereas no POF appeared in the ovaries at 20°C. It is suggested that the fish reared at 25°C actively repeated a sequence of gonadal cycles, which included the recrudescence of new clutches of oocytes, rapid advancement of vitellogenesis and final oocyte maturation, ovulation, and
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Table 1 Histological changes in the ovaries of the sapphire devil under various temperature conditions during different phases of reproductive season Phasea
I
II
III
Initial ovarian condition
Experimental temperature (°C)
Status of ovarian development during treatment (days)b
????
20
????
???
???
25
????c
????c
????c
30 20
???c,d ??d
??d ?
??d –
25
????c
???c
??c
30
?d
–
–
20
–
–
–
25
?c
?
?
30
–
–
–
????c
??c
15
30
45
a
Phase I (April–May; increasing water temperature and photoperiod), phase II (June–July; increasing water temperature and peak/decreasing photoperiod), and phase III (August–September; peak/decreasing water temperature and decreasing photoperiod) b Ovarian development from immature (-) to well developed (????) was expressed based on histological observation of the ovaries of each group. They are the ovaries exclusively occupied by immature oocytes at peri-nucleolus stage (-), the presence of vitellogenic oocytes at primary yolk stage (?), the ovaries with few vitellogenic oocytes (\20% of total oocytes) at primary yolk stage to tertiary yolk stage (??), the ovaries with many vitellogenic oocytes (20–40% of total oocytes) at primary yolk stage to tertiary yolk stage (???), and the most developed ovaries exclusively filled with vitellogenic oocytes ([40% of total oocytes) at tertiary yolk stage (????), respectively c,d
Presence of post-ovulatory follicles and atretic oocytes in the ovaries of some of the fish, respectively
release of gametes. Since oocyte development over vitellogenic stages seemed to be restricted in the fish at 20°C, it was unlikely that the fish reared at lower temperatures would have experienced the final oocyte maturation and spawning activities. On the other hand, the fish reared at 30°C had ovaries with degenerative oocytes at the vitellogenic stage. This ovarian condition without POF lasted for at least 45 days, suggesting that the oocytes were recruited with development into the vitellogenic stage, but degenerated without spawning. The present result of spawning frequency obviously supports the results of the above histological observation; the repeated spawning occurred only in the fish reared at 25°C, but not in those reared at 20 and 30°C. The effect of temperature on the reproductive activity of fish inhabiting temperate and higher latitudes has been examined extensively in previous studies [21–23]. It was reported that the spawning period of the spring-spawning bitterling Acheilognathus tabira was regulated by temperature, but not by photoperiod; the initiation of its spawning was caused only by an increase in temperature [21]. The effect of temperature on reproductive activity has also been experimentally obtained in the spiny damselfish Acanthochromis polyacanthus, a tropical species, in which a rearing temperature shift from 24 to 28°C under a constant photoperiod (LD12:12) shortened the interval of ovulation [7]. Occurrence of spawning behavior was observed with an increase in temperature in the whitebelly damselfish Amblyglyphododon leucogaster inhabiting the Red Sea [12] and the Hawaiian damselfish Dascyllus albisella [11]. The present results clearly
demonstrate that a suitable temperature range is one of the important environmental factors for the continuity of the reproductive activity in the sapphire devil. On the other hand, it was reported that rearing under high temperatures induced ovarian atresia in the Indian catfish Heteropneustes fossilis [24] and the white sturgeon Acipenser transmontanu [25]. Elevated water temperature caused cessation of reproductive capacity in the spiny damselfish [26]. Similarly, the present result showed a negative impact of high temperature (30°C) on ovarian development in the sapphire devil. A high temperature that is close to the breakpoint in the experimental region during the summer period may be critical to the continuity of their reproductive activity. The effect of temperature on the reproductive performance of the sapphire devil was also evaluated in phases II and III. In phase II, the fish reared at lower (20°C) and higher (30°C) temperatures could no longer sustain vitellogenic activity; their ovaries were occupied by immature oocytes and showed no sign of developing from the immature to vitellogenic stage. In the same phase, the fish reared at 25°C seemed to carry out active ovarian functions, from vitellogenesis to final oocyte maturation. Since this experimental temperature of 25°C at days 30 and 45 was moderately lower than the natural temperature in the experimental region, the reproductive performance during this period may have been maintained by the experimental temperature. In phase III, on the other hand, the ovaries of the fish at all the experimental temperatures contained immature oocytes, although GSI of the fish at 20 and 25°C
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Fig. 3 Ovarian histology of the sapphire devil reared under various temperature conditions during different phases of reproductive season. a Cross section of an ovary (CSO) of the fish reared at 20°C during phase I for 15 days, b CSO of the fish reared under 25°C during phase I for 15 days, c CSO of the fish reared under 30°C during phase I for 15 days, d CSO of the fish reared under 20°C during phase II for 15 days, e CSO of the fish reared under 30°C during phase II for 45 days, f CSO of the fish reared under 25°C during phase III for 45 days. AO atretic oocyte, ODS oil droplet stage, PNS peri-nucleolus stage, POF post-ovulatory follicle, PYS primary yolk stage, SYS secondary yolk stage, TYS tertiary yolk stage. Scale bar 200 lm
Table 2 Effect of temperature on the spawning performance of the sapphire devil (n = 6) during different phases of reproductive season Temperature (°C)
Total number of spawnings Phase I
Phase II
Phase III
20
0
0
0
25
11
16
8
30
4
0
0
Table 3 Effect of photoperiod on the spawning performance of the sapphire devil (n = 5) during different phases of reproductive season Photoperiod
Total number of spawnings Phase I
Phase II
Phase III
SP
8
11
0
LP
23
22
2
NP
23
19
0
SP short photoperiod (LD 10:14), LP long photoperiod (LD 14:10), NP natural photoperiod
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Fig. 4 Changes in gonadosomatic index of the female sapphire devil after rearing under different photoperiodic conditions. The fish (n = 5) were reared under conditions of short photoperiod (LD 10:14), long photoperiod (LD 14:10), and natural photoperiod (NP), respectively. Each value represents mean ± SEM. Different letters indicate significant difference at P \ 0.05
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Fig. 5 Ovarian histology of the sapphire devil after rearing under different photoperiodic conditions. a Cross section of an ovary (CSO) of the fish reared under short photoperiod, and b CSO of the fish reared under long photoperiod, respectively. Scale bar 200 lm
was significantly higher than that at 30°C. This means that temperature is less effective as a factor in the prolongation of reproductive activity at the final phase of the reproductive season, even if it is within the suitable limits. Spawning frequency of the fish pair reared under a short photoperiod (LD10:14) was lower than that under a long (LD14:10) or natural photoperiod in phases I and II. This suggests that a long photoperiod is related to the continuity of active reproduction in this species. Few studies have been conducted on the involvement of photoperiod with the reproductive activity of fish of tropical origin. Although the connection of temperature with reproductive activity cannot be ignored, the importance of photoperiod in reproductive activity was described in the cases of the Indian carp [14] and the sergeant major [13]. The experiments regarding the abovementioned factors were carried out in the sampling points around the subtropical regions of Santiniketan, India (23°140 N, 87°510 E) and Sa˜o Paulo, Brazil (23°490 S, 45°22–250 W), respectively. On the other hand, a long photoperiod of LD18:6 induced retardation of gonadal maturation in the white spotted spinefoot in Singapore (1°140 N, 103°550 E) [27]. The physiological response to photoperiod may differ among tropical species. Spawning in phase III was observed only in the pairs reared under long photoperiodic conditions. Since the
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experimental photoperiod in phase III was moderately longer than the natural one, the spawning performance may have been maintained due to this factor. This result is supported by the histological observation of the ovaries that was carried out at the end of the experiment; vitellogenic oocytes were evident in ovaries of the fish under long photoperiodic conditions, whereas those of the fish under natural and short photoperiodic conditions had immature oocytes. Therefore, the vitellogenic activities observed in the sapphire devil could be attributed to the long photoperiod. However, it was also observed that the degenerating oocytes at the vitellogenic stage were scattered in the ovaries, suggesting that a continuity of high temperature in this phase causes a regression of gonadal activity. Other factors may have been involved in the oocyte development over vitellogenesis. In this regard, it was reported that the reproductive activity of the Hawaiian sergeant A. abdominalis is positively related to the abundance of available food [9], which is in turn closely linked to the discharge of nutrients from streams into coastal areas and a subsequent increase in plankton productivity [9, 28]. A lack of recrudesce was also found in the case of several damselfish species during the wet season in Kimbe Bay, Papua New Guinea, and it was hypothesized that this periodic change in recrudesce is due to a reduction of reproductive output as well as an increase in larval mortality, which is related to the monsoonal condition [10]. Therefore, it is possible that, in addition to broad-scale seasonal changes in temperature and photoperiod, fish inhabiting tropical regions can respond to the rhythmic changes in the local environment that are attributed to a monsoon climate [8, 17]. It is appropriate to state that there is a latitudinal and geographical difference in the environmental strength of a monsoon climate and that responses of respective fish vary with habitat [14, 29–33]. We thus conclude that the reproductive activity of the sapphire devil inhabiting subtropical regions is maintained under long photoperiod conditions and a suitable temperature range. The importance of photoperiod and temperature may be altered in phases with different dynamics in these environmental factors, because the expression and alternation of photoperiodism have been suggested in certain fish in the temperate region [22, 34]. Acknowledgments This study was supported in part by a Grant-inAid for Scientific Research from the Japan Society for the Promotion of Science (JSPS) to AT and by the 21st Century COE program of the University of the Ryukyus ‘‘The Comprehensive Analyses on Biodiversity in Coral Reef and Island Ecosystems in Asian and Pacific Regions’’ from the Ministry of Education, Culture, Sports, Science and Technology, Japan. This was a contribution of Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus.
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