Effects of different photoperiods and handling stress on spawning and reproductive performance of pikeperch Sander lucioperca

Effects of different photoperiods and handling stress on spawning and reproductive performance of pikeperch Sander lucioperca

Animal Reproduction Science 132 (2012) 213–222 Contents lists available at SciVerse ScienceDirect Animal Reproduction Science journal homepage: www...

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Animal Reproduction Science 132 (2012) 213–222

Contents lists available at SciVerse ScienceDirect

Animal Reproduction Science journal homepage: www.elsevier.com/locate/anireprosci

Effects of different photoperiods and handling stress on spawning and reproductive performance of pikeperch Sander lucioperca Sara Pourhosein Sarameh a , Bahram Falahatkar b,∗ , Ghobad Azari Takami c , Iraj Efatpanah d a b c d

Department of Fisheries, Faculty of Natural Resources, Islamic Azad University, Lahijan Branch, Lahijan, Guilan, Iran Fisheries Department, Faculty of Natural Resources, University of Guilan, Sowmeh Sara, Guilan, Iran Aquatics Health and Disease Department, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran Dr. Yousefpour Fish Hatchery Center, Siahkal, Guilan, Iran

a r t i c l e

i n f o

Article history: Received 19 November 2011 Received in revised form 14 May 2012 Accepted 16 May 2012 Available online 24 May 2012 Keywords: Light regimen Reproduction Sex steroids Stress Pikeperch

a b s t r a c t The objective of this study was to control the reproductive cycle of pikeperch (Sander lucioperca) through determining the effects of different photoperiods and handling stress on the reproduction quality, timing and quality of spawning, fertilization, sex steroids, and cortisol concentrations. In this study, 72 pikeperch broodstocks with an average weight of 1367 ± 55.3 g were exposed to different photoperiods including constant light (24L:0D), constant darkness (0L:24D), and 12 h of light, 12 h of darkness (12L:12D) for 40 days. Half of the broodstocks of each photoperiod treatment were exposed to handling stress at a specific time of the day. Applying different photoperiods caused changes in the timing of broodstocks’ spawning, so that fish under 24L:0D spawned earlier than those of other photoperiods, and stressed fish of the 0L:24D photoperiod had a delayed spawning compared to others. Also, the spawning of the broodstocks at different photoperiods which were exposed to handling stress was either delayed or did not occur at all. The highest and lowest spawnings were observed in the morning and at night, respectively. Fertilization percentage, number of eggs per gram, sex steroids including estradiol, progesterone, and testosterone, as well as cortisol and calcium concentrations did not show any significant difference in different photoperiods and handling stress. In stressed males of the 24L:0D photoperiod, there only was a significant decrease of testosterone concentration compared to the beginning of the experiment. Results indicated that the spawning performance of pikeperch broodstocks could be considerably stimulated using an effective photoperiod. Similarly, pikeperch broodstocks in culture systems are usually affected by handling stress, and this stress could lead to a poor reproductive performance and inhibition of spawning. © 2012 Elsevier B.V. All rights reserved.

1. Introduction In some northern and central European countries, pikeperch Sander lucioperca is mainly known as an edible and commercial fish and, therefore, is considered

∗ Corresponding author at: Fisheries Department, Faculty of Natural Resources, University of Guilan, Sowmeh Sara, 1144, Guilan, Iran. Tel.: +98 182 322 3599; fax: +98 182 322 2102. E-mail address: [email protected] (B. Falahatkar). 0378-4320/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.anireprosci.2012.05.011

important for aquaculture purposes (Muller-Belecke and Zienert, 2008). Because the spawning season of these fish is only once a year from April to early May (Muller-Belecke and Zienert, 2008), out-of-season spawning induction methods for this species seems important. In fact, developing pikeperch culture requires controlling their reproductive cycle so that an out-of-season spawning is achieved. Therefore, induction of the reproductive cycle should be done irrespective of season (Migaud et al., 2004b). In fish of temperate regions, inducing this cycle is usually specified by annual changes of photoperiod and temperature

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(Bromage et al., 2001). The reproductive cycle of pikeperch also depends on annual photoperiod and temperature (Migaud et al., 2003, 2004b; Wang et al., 2010). Related researches have proven that photoperiod and daily changes are involved in the environmental induction and quality of perch reproduction which includes the timing and rate of spawning, fertilization and the mortality of broodstock (Fontaine et al., 2006; Migaud et al., 2006). As a result, with photoperiod as one of the main environmental cues of the timing of reproduction (Bromage et al., 1993; Craig, 2000) taken into account which works through the hypothalamus–pituitary axis (Borg, 1994; Nagahama, 1994), and because illumination can affect the reproductive performance of perch (Fontaine et al., 2006), it is probable that photoperiod changes during the final stages of reproduction and near the time of spawning would have an effect on broodstocks’ breeding and spawning as well. Besides, handling stress is another factor which has critical effects on the reproduction success. In fact, it is assumed that in fish cultured under stressful conditions, a kind of exchange between the allocation of energy for reproduction and maintenance could happen (Schreck et al., 2001; Wang et al., 2006). Handling is among the avoidably stressful factors at breeding and culture centers that have destructive effects on the physiological systems of fish including a decrease in broodstock fecundity, incidence of abnormal behaviors and a decrease in the growth. Studying responses of the fish to handling stress with regard to the prevalence of intensive fish culture and an increased probability of exposure to stress would result in improving management methods for fish breeding and ultimately for their health and enhanced growth (Belanger et al., 2001). In fact changing the reproductive techniques under stressful situations can have important effect on the improvement reproductive fitness for fish in the wild. Clearly, understanding of such processes is helpful for management of hatchery and broodstocks (Schreck et al., 2001). Moreover, little is known about factors which facilitate induced spawning in pikeperch and, practically, there is no information about the interaction between different photoperiods and handling stress and its effect on spawning. Consequently, since determining the induction of reproduction and spawning might be a multi-factor process, conducting studies with the purpose of identifying different photoperiods and handling stress as effective factors in the reproduction success, and finding the best option to induce spawning along with its effect on the quality of reproduction are necessary. To study the effect of light severity or the direction of the change of photoperiod in the timing of spawning, in the final stages of pikeperch reproduction, fish with the same photoperiod history were exposed to three photoperiods: half days of light followed by an abrupt change to half days of darkness (12L:12D) photoperiod that represents normal photoperiod, and continuous light (24L:0D) and continuous darkness (0L:24D) to study if increasing or decreasing light in the final stages of reproduction can alter spawning times by advancing or delaying spawning period. Additionally, stress can have suppressive effect on reproduction. Therefore, the objective of this study was to enhance the understanding for environmental

controlling of the pikeperch reproductive cycle along with determining the effects of different photoperiods and handling stress on the quality of reproduction, the timing and quality of spawning, fertilization, and sex steroids concentrations during spawning season. Hatcheries can use this knowledge to manipulate maturation and spawning time to produce all-year-round supplies of eggs and fry. 2. Materials and methods 2.1. Fish and facilities In autumn, broodstocks were captured from a reservoir lake in Aras dam, located in northwestern Iran between Iran and Nakhjavan Republic as an important pikeperch habitat at the southern basin of the Caspian Sea. Then, they were transferred to the Dr. Yousefpour Fish Hatchery Center at Siahkal, Guilan, Iran. For 3 months, fish were kept in wintering earth ponds while being fed with bait fish (carp fries, etc.). In March 2009, they were transferred to 18 tanks [4 fish per tank, age 4–5 years (two females and two males as a sex ratio of 1:1)] with 1490 l in capacity, with 50 cm depth and an average water flow of 20 ± 0.88 l min−1 at a non-recirculation system. The age of the broodstocks was determined by the scales taken from the line of demarcation between the lateral line and dorsal fin. The scales were examined under microscope with magnification of 20× and the age was determined by counting the dark and light circles (Biswas, 1993). Broodstocks (including 36 males and 36 females) had an average weight of 1367 ± 55.3 g and an average length of 53.7 ± 0.6 cm (mean ± SE). At the beginning of the experiment, one fish (one male or female; totally 9 males and 9 females) was randomly selected for blood sampling from each tank. Temperature and dissoluble oxygen were checked using a thermometer and an oxymeter, respectively, three times a day at 8:30 AM, 14:30 PM and 20:30 PM. In a 40-day period, temperature was kept at 13.1 ± 0.5 ◦ C and dissolved oxygen was at 9.7 ± 0.4 mg l−1 (mean ± SE). 2.2. Experimental design In this study, three different photoperiods were applied for 40 days. To provide light during 24L:0D and 12L:12D photoperiods, a 100 W lamp (Pars Shahab, Guilan, Iran) with 630 lx was used 40 cm above the water surface for each tank. Also, black plastic was used for covering the tanks during darkness times for 0L:24D and 12L:12D photoperiods. In addition, due to low temperature and prevention of eggs eaten by baitfish, broodstocks were not fed during the experimental period. For each photoperiod, there were two groups of fish. In one group, fish were not exposed to any stress and were called the fish without stress photoperiods. In order to evaluate the effect of sampling or capture on the reproductive performance of the other group, the water level in the tank was reduced to 10 cm from the bottom at 9:15 AM every day. Then, the fish were captured by net and kept out of water for 20 s and were transferred back to the tank with its water level increased back to the first level. These fish were called the

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fish of stressful photoperiods. Each photoperiod consisted of three stressful and three stress free replications. The broodstocks of the stressful photoperiod’s conditions were under the influence of handling stress for 40 days. 2.3. Induction of spawning and sampling To induce spawning, 10 days after applying different photoperiods, inputting nest in tanks was done. In this process, nests (53 cm × 53 cm × 5 cm) were placed inside tanks such that there were two nests per tank. Then, nests were checked every 2 h for checking the spawning with very short and rapid removal of the sheet especially during the darkness. Broodstocks which had spawned were biometrically recorded for weight (g) and length (mm) of fish with their blood samples taken. At the end of 40 days of experiment, the blood samples of the remaining broodstocks that did not spawn were also taken as non respondent fish. 2.4. Spawning time and quality The time of spawning was set as follows: morning (spawning which occurred during 4–12 AM), afternoon (spawning that occurred during 12–20 PM) and night (spawning which occurred between 20 PM and 4 AM). In order to compare the quality of eggs produced by the broodstocks at different treatments, the quality of spawning was measured based on the spawning rate which included good spawning (eggs covering 100% surface of the nest) the eggs that were round, transparent, pale yellow to colorless, average spawning (eggs covering 50% surface of the nest), and the eggs that were relatively transparent, and poor spawning (eggs covering less than 25% surface of the nest), the eggs were relatively turbid. 2.5. Reproduction indices To determine the fertilization percentage and the number of eggs per gram, two batches of 400–500 eggs were randomly sampled. Egg samples were weighed using a digital scale with a 0.01 g precision. The fertilization percentage of the obtained eggs was specified in two stages: blastula (about 5 h after fertilization) and gastrula (nearly 48 h after fertilization). Fertilized eggs with a translucent appearance were counted and differentiated from unfertilized eggs (whitish appearance). Eggs were observed daily to check for embryogenesis and signs of hatching. When hatching completed, hatching rate was determined by counting the larvae and remaining dead eggs.

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2 ml blood was taken from their caudal vein using 5 ml heparinized syringes. Blood was centrifuged at 1500 × g for 10 min, and the plasma was kept in tubes at −25 ◦ C until the time of analysis. Testosterone (T), 17␤-estradiol (E2 ), and progesterone (P) concentrations were determined after two extractions with cyclohexane/ethylacetate (v/v) using the radioimmunoassay (RIA) method according to Fostier and Jalabert (1986). Samples were tested as duplicates while the standards were tested as triples. All samples were analyzed in a separate RIA for each steroid (Migaud et al., 2004b). Because of the positive relation between calcium and vitellogenin concentrations, plasma calcium concentrations were measured through spectrophotometry (Norberg et al., 2004) using the Arsenazo III calcium commercial kit (Sigma, St. Louis, MO, USA) in this experiment. Plasma cortisol concentrations were measured by RIA using a commercial antibody kit (cortisol-3-OCMOantiserum, Immunotech, Prague, Czech Republic) as described by Ruane et al. (2001). Plasma glucose concentration was measured using analytical kits (Wako Pure, Chemical Ind. Ltd., Osaka, Japan) (Ruane et al., 2001). Plasma lactate was enzymatically determined using Sigma Diagnostic Kits (St Louis, MO, USA). 2.7. Statistical analyses All data collected at the place of experiment along with those of the laboratory were recorded in Excel software and analyzed by the SPSS software (Version 13, Inc., Chicago, IL, USA). Then, these were displayed as mean ± SE. The normality of the data was measured through Kolmogorov–Smirnov test. All percent data were Arc-sin transformed before analysis. Two-way analysis of variance (ANOVA) test was used to study the effect of photoperiod (three levels) and stress (two levels) as independent variables on all biochemical parameters, while fertilization percentage and the number of eggs per gram were separately used as dependent variables. When there was an interaction, Tukey’s test as post hoc test was used for determining differences among means. Comparison of the two stresses condition (stress and no stress fish) in each photoperiod treatment was performed using the Independent Samples t-test. For nonparametric data, Mann–Whitney U test was used to find significant effect of different photoperiods or stress conditions. The significance level in this study was considered as P < 0.05. 3. Results

2.6. Blood sampling, plasma assessment and analysis

3.1. Number, timing and the quality of spawning

All parts of sampling and fish care during the experiments were conducted in accordance with the Guide for the Care and Use of Agricultural Animals in Agricultural Research and blood sampling was done after anesthetizing the brooders with a 300 mg l−1 dosage of clove powder. The first blood sampling of 18 broodstocks (one broodstock per tank) was performed a day prior to applying different photoperiods and handling stress. The second blood sampling was conducted immediately after spawning in which

Spawning occurred in a 4-week period after nesting (March 19 to April 14; Fig. 1). Out of a total number of 36 females, 29 spawned and only seven brooders of different photoperiods did not spawn due to handling stress. The ratio of spawning was not significant. The first spawning was observed 2 days after nesting in the broodstocks of 24L:0D photoperiod. The first spawning of broodstocks which were exposed to handling stress during different photoperiods was observed 14 days after nesting and

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S. Pourhosein Sarameh et al. / Animal Reproduction Science 132 (2012) 213–222 1-14Day 15-28Day

80 60 40 20 0 stressed

unstressed

stressed

24L

unstressed

stressed

12L-12D

unstressed

100

Spawning quality (%)

Spawned fish (%)

100

unstressed

stressed

80 60 40 20 0

24D

24L

12L-12D good

Days after inputting nest

24D

24L

12L-12D

24D

average

24L

12L-12D

24D

poor

Photoperiod Fig. 1. Percentage of pikeperch Sander lucioperca broodstocks which spawned during the different photoperiods including constant light (24L:0D), 12 h of light:12 h of darkness (12L:12D), constant darkness (0L:24D), constant light with stress (24L:0D-s), 12 h of light:12 h of darkness with stress (12L:12D-s), and constant darkness with stress (0L:24D-s). n = 6 females in each photoperiod by stress combination. No difference (P > 0.05) was observed in terms of handling stress or photoperiod.

during 24L:0D-s photoperiod. Totally, broodstocks of the 24L:0D photoperiod, stressed or unstressed, spawned earlier than those of other photoperiods. Also, the spawning of stressed broodstocks compared to those in the unstressed photoperiods was either delayed or did not occur. Among different stressed and unstressed photoperiods, 24L:0D and 0L:24D-s had the earliest and latest spawning, respectively. All broodstocks exposed to unstressed photoperiods spawned; however, in stressful photoperiods, 1/3 of broodstocks exposed to 24L:0D-s and 12L:12D-s photoperiods and half of those kept in 0D:24D-s did not spawn. Regarding the time of spawning, no significant difference was observed among different photoperiod treatments, while the greatest and least rates of spawning were that of the morning and night, respectively. Moreover, broodstocks of 0L:24D and 12L:12D photoperiods did not spawn at night and broodstocks exposed to 0L:24D-s spawned only in the morning (Fig. 2). No interaction was also found between light and stress. The quality of broodstocks’ spawning did not reveal any significant difference during different photoperiods, while in 0L:24D a good quality spawning (100% covered the

nest) was not observed either under stressful or unstressed condition. In addition, during 24L:0D-s, no poor quality spawning was observed (Fig. 3), but no interaction was found between light and stress. Number of eggs per gram did not show any significant difference in different photoperiods and stress conditions (Fig. 4). Hatching efficiency and fertilization percentage during blastula and gastrula stages showed no significant difference in different photoperiod treatments (Figs. 5 and 6) as well. No interaction was also found between light and stress while in all stressful photoperiods, lower fertilization percentages during the gastrula stage were observed compared to photoperiods without any stress (P > 0.05). The body weights of the broodstocks were 1195 ± 200.7 g and 1662 ± 220.4 g for males and females, respectively, in the beginning of the experiment before applying different photoperiod and handling stress, and attained to 1004 ± 125.5 g and 1535 ± 200.1 g for males and females at the end of 40 days of fasting period. No significant different was observed for both sexes during this condition. 3.2. Sex steroids Plasma testosterone concentration, in both males and females, showed no significant difference during different

100 unstressed

80

stressed

60 40 20 0 24L

12L-12D Morning

24D

24L

12L-12D

24D

Afternoon

24L

12L-12D

24D

Night

Spawning time

Number of egg per gram

Brood spawned (%)

Fig. 3. Comparison the quality of spawning pikeperch Sander lucioperca broodstocks in three condition; good, average and poor in different photoperiods including constant light (24L:0D), 12 h of light:12 h of darkness (12L:12D), constant darkness (0L:24D), with and without stress. No difference (P > 0.05) was observed in terms of handling stress or photoperiod.

1200 unstressed

1000

stressed

800 600 400 200 0 24L

12L-12D

24D

Photoperiod Fig. 2. Comparison of the pikeperch Sander lucioperca broodstocks spawning during different times: morning (4–12 AM), afternoon (12–20 PM) and night (20 PM to 4 AM) in different photoperiods including constant light (24L:0D), 12 h of light:12 h of darkness (12L:12D), constant darkness (0L:24D), with and without stress. No significant difference (P > 0.05) was observed in terms of handling stress or photoperiod.

Fig. 4. Number of egg pikeperch Sander lucioperca broodstocks/gram in different photoperiods including constant light (24L:0D), 12 h of light:12 h of darkness (12L:12D), constant darkness (0L:24D), with and without stress. No differece (P > 0.05) was observed in terms of handling stress or photoperiod.

Fertilization in gastrula (%)

Fertilization in blastula (%) 100 90

80 70 60

50 40 30 20

10 0

100 90 80

70 60 50 40 30

20 10 0

A

B 24L

24L

12L-12D 24D

24D

24D

unstressed

stressed

unstressed

stressed

unstresse d

stressed

Table 1 Sex steroids, calcium and stress indicators (mean ± SE) of pikeperch male broodstocks Sander lucioperca in different photoperiods including constant light (24L:0D), 12 h of light and 12 h of darkness (12L:12D), constant darkness (0L:24D) and start (a day before the experiment was started; n = 9), with and without stress (n = 6 for each). Samples were taken after 40 days of photoperiod/stress applying. Start

0L:24D

12L:12D

Unstressed Progesterone (ng ml−1 ) Estradiol (ng ml−1 ) Testosterone (ng ml−1 ) Calcium (mg dl−1 ) Cortisol (ng ml−1 ) Glucose (mg dl−1 ) Lactate (mg dl−1 )

0.13 35.44 2.74 10.76 64.61 97.89 28.89

± ± ± ± ± ± ±

0.01 8.32 0.63a 0.17 29.31 8.04 5.07

0.14 57.51 6.91 10.83 155 150.83 51.83

± ± ± ± ± ± ±

0.01 13.89 3.32 0.53 39.6 35.88 5.63

Stressed 0.14 37.01 0.38 10.88 96.6 115 41.8

± ± ± ± ± ± ±

24L:0D

Unstressed 0.01 15.72 0.19b 0.71 30.47 22.52 4.56

0.15 44.71 0.70 11.22 149 158.5 50

± ± ± ± ± ± ±

0.02 14.13 0.45 1.24 34.9 41.18 14.66

Stressed 0.11 41.33 1.20 9.53 97.48 87.17 41.66

± ± ± ± ± ± ±

2-Way ANOVA

Unstressed 0.01 8.30 0.82ab 0.43 38.66 17.76 6.05

0.14 43.01 2.68 10.55 124.5 136.83 38.83

± ± ± ± ± ± ±

0.00 13.45 1.63 0.27 28.07 22.97 9.08

Stressed 0.13 30.01 1.23 10.16 165.87 124.66 48.33

± ± ± ± ± ± ±

0.02 7.41 0.10ab 0.73 56.1 31.5 6.1

Stress × photoperiod

Stress

Photoperiod

NS NS

NS NS S>L NS NS NS NS

NS NS NS NS NS NS NS

*

NS NS NS NS

S. Pourhosein Sarameh et al. / Animal Reproduction Science 132 (2012) 213–222

Photoperiod

12L-12D

Photoperiod

12L-12D

Photoperiod

Fig. 5. Fertilization percentage of pikeperch Sander lucioperca broodstocks in two stages: (A) blastula and (B) gastrula in different photoperiods including constant light (24L:0D), 12 h of light:12 h of darkness (12L:12D), constant darkness (0L:24D), with and without stress. No difference (P > 0.05) was observed in terms of handling stress or photoperiod.

photoperiods, while 24L:0D-s resulted in lesser concentrations of this hormone and indicated a significant difference compared to that of the beginning of the experiment in males. Furthermore, no interaction was found between light and stress in females, an interaction was only found in testosterone concentration in males. Progesterone concentrations in males and females were not significantly different during different photoperiods, and no interaction was found between light and stress. Estradiol in both sexes was not significantly different during different photoperiods with no interaction between light and stress (Tables 1 and 2).

40

35

30

25

20

15

5

10

0 24L

Fig. 6. Hatching efficiency (%) of pikeperch Sander lucioperca broodstocks in different photoperiods including constant light (24L:0D), 12 h of light:12 h of darkness (12L:12D), constant darkness (0L:24D), with and without stress. No difference (P > 0.05) was observed in terms of handling stress or photoperiod.

Hatching efficiency (%)

S: start (the beginning of experiment); L: constant light; NS: no difference (P > 0.05) in terms of handling stress or photoperiod; S > L: start (the beginning of experiment) had a greater testosterone concentration and there was no difference with constant light (24L:0D) in terms of handling stress. a, b, ab Difference (P < 0.05) in terms of handling stress. * Interaction between light and stress.

217

An asterisk shows significant difference between with and without stress conditions in a photoperiod. S: start (the beginning of experiment); D: constant darkness; Ds: constant darkness with stress; NS: no differece (P < 0.05) in terms of handling stress or photoperiod; D > S: constant darkness (0L:24D) had a greater glucose concentration and difference from the beginning of the experiment in terms of photoperiod; D > Ds: constant darkness (0L:24D) had a greater glucose concentrations and difference with constant darkness with stress (0L:24D-s) in terms of handling stress. a, b, ab : Difference (P < 0.05) in terms of handling stress.

NS NS NS NS NS D>S NS NS NS NS NS NS D > Ds NS ± ± ± ± ± ± ± 0.13 62.67 1.65 11.46 116.66 139.33 38.33 0.01 12.74 2.81 0.77 55.76 21.82ab 2.21 ± ± ± ± ± ± ± 0.16 49.01 2.91 12.26 200.67 161.33 32 ± ± ± ± ± ± ± 0.13 66.33 5.34 11.31 103.83 95.33 36.83 0.01 5.29 0.42 0.51 22.42 27.64ab 2.43 ± ± ± ± ± ± ± 0.14 78.86 0.57 11.75 109.03 161.86 32.86 ± ± ± ± ± ± ± 0.12 63.57 3.45 10.27 110.5 84.29 41.86 0.01 50.22 0.03 0.43 20.24 28.76a* 5.86 ± ± ± ± ± ± ± 0.13 50.01 0.09 11.33 73.5 190.17 43.83 0.12 68.56 4.67 11.28 45.24 83.78 30 Progesterone (ng ml−1 ) Estradiol (ng ml−1 ) Testosterone (ng ml−1 ) Calcium (mg dl−1 ) Cortisol (ng ml−1 ) Glucose (mg dl−1 ) Lactate (mg dl−1 )

Start

± ± ± ± ± ± ±

0.01 9.72 0.67 0.33 20.99 6.09b 4.33

Unstressed

0L:24D

Stressed

0.02 9.36 1.86 0.46 32.08 17.98* 5.05

Unstressed

12L:12D

Stressed

0.01 9.47 4.07 0.73 30.25 13.74 3.66

Unstressed

24L:0D

Stressed

0.02 11.90 1.02 0.51 30.09 21.87 6.1

NS NS NS NS NS NS NS

Photoperiod Stress Stress × photoperiod

2-Way ANOVA

S. Pourhosein Sarameh et al. / Animal Reproduction Science 132 (2012) 213–222 Table 2 Sex steroids and calcium concentrations (mean ± SE) of pikeperch female broodstocks Sander lucioperca in different photoperiods including constant light (24L:0D), 12 h of light and 12 h of darkness (12L:12D), constant darkness (0L:24D) and start (a day before the experiment was started; n = 9), with and without stress (n = 6 for each). Samples were taken after 40 days of photoperiod/stress applying.

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3.3. Calcium concentration Average calcium concentration of males was not significantly different while applying different photoperiods and handling stress. No significant difference was observed in females regarding average calcium concentrations when exposed to different photoperiods and handling stress. In addition, there was no interaction between light and stress treatments (Tables 1 and 2). 3.4. Cortisol, glucose and lactate concentrations Average plasma cortisol concentrations were not significantly different in male broodstocks during different photoperiods and handling stress (Table 1). Females did not show any such difference in terms of average cortisol concentrations during the photoperiods and stress handling as well (Table 2). Maximum average cortisol concentration of male broodstocks was observed during the 24L:0D-s photoperiod, and in females, it was seen in the 24L:0D. These maximum concentrations were 165 ± 57 and 309 ± 181 ng ml−1 in males and females, respectively. Average glucose concentrations in male broodstocks showed no significant difference in the different photoperiods and handling stress (Table 1). Although no significant difference of glucose concentrations was observed in different photoperiods in female broodstocks, 0L:24D had a greater glucose concentration and there was a significant difference from the beginning of the experiment (P < 0.05). Furthermore, this concentration in stressed fish during the 0L:24D-s (constant darkness with stress) photoperiod had a significant difference from that of the unstressed fish (Table 2). Average lactate concentrations were not significantly different in male broodstocks which were exposed to different photoperiods and handling stress (Table 1). Females did not show any significant difference in this regard either (Table 2). Overall, the interaction of light and stress in terms of stress responses was not observed in male and female broodstocks. 4. Discussion Results obtained from this study indicated that different photoperiods affect the induction of spawning of pikeperch broodstocks during their final stages of reproduction and lead to changes in the timing of their spawning. Moreover, the greatest and least number of spawnings was observed in the morning and at night, respectively. Some researches have stated that the timing of spawning depends on the harmony of a rhythm or an annual internal clock by changing photoperiods (Bromage et al., 1992; Bon et al., 1999; Bonnet et al., 2007). Results from the present study were consistent with those of Migaud et al. (2004a, 2006) showing that daily changes of illumination are important to control the spawning of Eurasian perch Perca fluviatilis. In addition, in the present study, the greatest and least amount of spawning that occurred in the morning and at night, respectively indicated that illumination changes function as an

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important stimulant for determining the time of spawning in pikeperch. So, it confirmed the results obtained by Migaud et al. (2006), who had observed the greatest amount of spawning in the morning in Eurasian perch exposed to different photoperiods. The present study also indicated that continuous illumination (24L:0D) during the final stage of reproduction accelerates the time of spawning, while 0L:24D delays spawning. Lengthening photoperiods during the final stage of reproduction, therefore, induces spawning in these fish and shortening photoperiods delays their spawning. The findings of the present study confirm those obtained by Muller-Belecke and Zienert (2008), that they stimulated the fish by photothermal and photoperiod regimens and made it possible for pikeperch to spawn 2 months prior to the spawning season. In the present study, number of eggs per gram, percentage of fertilization during blastula and gastrula stages, sex steroids, and calcium concentrations were the same among different photoperiods and handling stress. Also, cortisol concentrations in treatments with different photoperiods and handling stress did not show a significant difference which could be explained by the fish being adapted to daily stress because, according to reports by researchers, longterm exposure to a stressor could lead to allostasis, which is practically considered as the ability to return to the physiological concentrations observed prior to exposure to stress (McEwen, 1998; Schreck, 2000). No increase in cortisol concentrations of brooders which were stressed for a long time during the present research could be the result of a negative feedback of a daily increase of the cortisol concentration in the hypothalamus–pituitary–interrenal axis (Pickering and Pottinger, 1987; Fast et al., 2008), and fish were adapted with the stress after a long period of exposure. As mentioned, adaptation to stress during the experiment seems possible. However, the effect of stress on cortisol concentrations may be detectable while comparing concentrations with those obtained before treatments began at “start”. Biswas et al. (2006a,b) found that different photoperiods do not cause a considerably significant stress response (glucose–cortisol) in red sea bream Pagrus major which confirms results here. Moreover, results obtained from a study conducted by Fast et al. (2008) on salmons (Salmo salar) and those of Wang et al. (2004) on striped bass (Morone saxatilis) brooders showed that continuous acute handling stressor did not result in a long-term increase in glucose and cortisol concentrations. It is also probable that a significant increase in glucose concentrations of female brooders of the 0L:24D photoperiod compared to that of the beginning of the experiment and the 0L:24D-s photoperiod is due to the fact that long exposures to darkness (considering the delayed spawning during this photoperiod compared to other photoperiods) would cause a stress response through increasing the glucose concentration. Also, it seems that pikeperch brooders are sensitive to darkness and, in the long run, react to it by an increased glucose concentration as a secondary stress response. In as much as stressor responses might change in different photoperiods, these may cause greater or lesser sensitivity (Biswas et al., 2006a). In addition,

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the exposure time during which pikeperch are exposed to stressors could affect the magnitude of the physiological response, and the sensitivity of their response depends on stressor type (Acerete et al., 2004), which justifies the reason for a significant decrease in the glucose concentration in brooders during 0L:24D-s compared to that of the 0L:24D. In the present study, handling stress resulted in a delay or lack of spawning in pikeperch which could be due to the fact that in fish kept under stressful conditions some kind of exchange between allocations of energy for reproduction and maintenance occurs (Schreck et al., 2001; Wang et al., 2006). Wang et al. (2006) demonstrated that handling stress is an important modulating factor in the reproductive cycle of fish and can be of paramount importance during the reproductive cycle. Results of Campbell et al. (1992) showed that applying acute stress during the completion of the reproduction process delays the time of spawning in rainbow trout (Oncorhynchus mykiss). They suggested that reproduction is a physiological process which is very sensitive to the harmful effects of stress. In the present study, the reason why over half of the fish exposed to handling stress spawned could be related to their relative ripeness for spawning or, in course of time, these fish became adapted to stressful conditions because, according to other researchers, long periods of exposure to a stressor could lead to allostasis which is practically the body’s ability to return to its physiological state observed before applying stress (McEwen, 1998; Schreck, 2000). Morehead et al. (2000) also showed that striped trumpeter Latris lineata, in spite of frequent handling with stressful conditions, became adapted to 9 or 12 months of consecutive photo-thermal cycles and handling stress and completed their spontaneous maturity and spawning cycles which is a confirmation of the findings of the present study. Additionally, absence of spawning in about 1/3 of broodstocks to which handling stress was applied in comparison with the spawning of over half of the handled fish could be due to individual differences among fish. Schreck (1981) stated that the fish performance, when exposed to stress, is regulated with their ability to have individual performances. Depending on the fact that in which stage of life and with what intensity a stress is experienced and for how long a stressor performance lasts, these factors may affect reproduction in different ways (Schreck, 2009). Also, nutritional factors (Bromage et al., 1992; Carrillo et al., 1995; Zohar et al., 1995; Pereira et al., 1998; Siddiqui et al., 1998), fish age and spawning rank (Kjorsvik, 1994; Navas et al., 1995; Brooks et al., 1997), the amount of stress (Campbell et al., 1992; Contreras-Sanchez et al., 1998; Schreck et al., 2001), strain (Bromage et al., 1990), and, probably, their final sexual maturity can directly influence fish reaction and reproduction quality. Because teleosts use relatively different reproduction strategies to overcome stress, it is possible that different fish species, in terms of the nature of their physiological reaction, would have different reproductive outcomes in relation to a stressful factor, and their reaction to stress depending on their species, stage of maturity, and type and intensity of a stressor could be different (Schreck et al., 2001).

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During early oogenesis or maturation, the reproductive clock could buffer some eggs from energetic or nutritional deficits by causing atresia of others. Near complete maturity, reproduction success is optimized by regulating the timing of spawning. Thus, depending on the fact that in which stage of the reproduction stressful factors are experienced, they may have different effects, and when the fish are exposed to these factors, the period of maturation seems important (Schreck et al., 2001). As a result, since in this study, pikeperch were exposed to different photoperiods in their final stages of maturity, the effect of handling stress was observed on the timing of spawning, but it did not have any significant effect on the number of eggs per gram, fertilization percentage, sex steroids, and calcium concentrations. A study conducted by Contreras-Sanchez et al. (1998) showed that rainbow trout exposed to mild stress during early vitellogenesis produced smaller eggs which were different in size, while in those stressed during late vitellogenesis, no changes in average egg size was observed. Besides, rainbow trout which were exposed to mild stress, showed no changes in average egg size, but egg sizes were more heterogeneous and consistent with the results of this research. In a study conducted by Fontaine et al. (2006) early plasma testosterone and estradiol concentrations in male and female Eurasian perch during different photoperiods 8L:16D, 12L:12D, and 16L:8D showed no significant difference. Sulistyo et al. (1998) showed that fluctuations in sex steroids in the reproductive cycle of Eurasian perch compared to other species (e.g. cyprinids and salmonids) are less, which can justify the lack of significant differences between sex steroid concentrations in different photoperiod treatments of the present research. In the present study, males of the 24L:0D-s photoperiod had lesser concentrations of testosterone and showed a significant difference with those of the beginning of the experiment. This finding suggested the negative effect of stress on the reduction of testosterone. It is probable that more reductions in testosterone in this photoperiod is due to the fact that fish kept in 24L:0D-s use more energy because of releasing some corticostroids during constant light condition. Moreover, because glucocorticostroid rhythms reflect changes in the balance of energy in animals, when needs for energy are more than the existing energy resources, the glucocorticostroid concentrations increase (Goymann and Wingfeld, 2004). In addition, chronic stress reduces the circulation of sex steroids through the cortisol function (Pankhurst and Van Der Kraak, 1997). Greater concentrations of cortisol, therefore, result in more reductions in testosterone concentrations (our unpublished data). Similarly, Acerete et al. (2004) found that the intensity of response in Eurasian perch depended on the type of stressor and that differences in the nature, duration of a stress along with species differences could lead to differences in the timing and magnitude of the cortisol response (Ramsay et al., 2009). The previous findings indicated that stress response was hereditary and individual responses through the passage of time were a stable characteristic (Fevolden et al., 1991; Pottinger and Carrick, 1999; Wang et al., 2004). Therefore, changes which occur due to stress may

be rapid delayed, long-term, or short-term, depending on fish species, their life stage, the nature of stressor, and other environmental factors (Schreck, 2000; Barton, 2000, 2002). In view of these results and given that fasting can induce stress and other endocrine changes (e.g. hypoglycemia) it, in the present experiment, created unique conditions under which different photoperiods and another stressinducing factor, handling, were tested. Some studies have shown that food deprivation modifies cortisol response to handling disturbance in rainbow trout (Vijayan and Moon, 1992; Reddy et al., 1995). Similarly, food deprivation also alters stressor-induced hyperglycemia in fish (Vijayan and Moon, 1992). In a study conducted by Jorgensen et al. (2002), the pre-handling plasma cortisol concentrations were much greater in food-deprived than in fed fish. Their results are in contrast to other studies showing that food deprivation either suppressed (Barton et al., 1988; Sumpter et al., 1991; Vijayan and Moon, 1994; Reddy et al., 1995) or did not affect plasma cortisol concentration in rainbow trout (Farbridge and Leatherland, 1992; Vijayan and Moon, 1992). Jorgensen et al. (2002) expressed that the reason for these differences may be related to the longer duration of the food deprivation (∼140 days) compared to other studies, up to 6 weeks. But in the present study, during the experimental period of 40 days, the fish were fasting and had greater plasma cortisol concentrations than the beginning of the experiment. Also, in Jorgensen et al. (2002) study, there was no significant difference in plasma cortisol concentrations between the fed and food-deprived fish at 6 and 23 h post-handling disturbance. Although fasting was applied to all groups in the present study, it is important to consider and monitor the effects of fasting on endocrine changes and other aspects of the physiology and reproductive performance. More detailed studies, like controlled challenge of fish fed at different photoperiod are needed. The present study increases the knowledge of reproductive processes in pikeperch and found photoperiod manipulation at the final stage of reproduction in fish leads to changes in the timing of their spawning and does not have any effect on other fertilization parameters. In addition, despite the acceleration of spawning during 24L:0D compared to other photoperiods, no changes were found in the number of eggs per gram and other fertilization parameters. Thus, an enhanced spawning performance in the final stage of reproduction can be attributed to this photoperiod. However, in order to ensure that whether applying constant light that during the final stage of reproduction caused the spawning of pikeperch to accelerate compared to other photoperiods is a species-related characteristic, or it changes during longer periods or at early stages of reproduction and maturity requires more studies to be done. Additionally, with consideration of the delayed or absence of spawning in half of the fish exposed to 0L:24D-s and 1/3 of those kept in 24L:0D-s and 12L:12Ds, it is concluded that the handling process induces stress in pikeperch and leads to a poor reproductive performance. Thus, the importance of preventing harmful effects of handling stress and identifying methods which can minimize the adverse effects of handling needs to be considered.

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