Effects of four factors on the quality of male reproductive cycle in pikeperch Sander lucioperca
Introduction
In many cultured fish species, particularly in those new for intensive aquaculture such as pikeperch Sander lucioperca, unpredictable and variable reproductive performance is an important limiting factor for the successful mass production of juveniles. A better understanding and control of this variability is thus of paramount importance, especially for producing shifted or out-of season spawning. Yet, our knowledge of the process and factors affecting reproductive performances in general and gamete quality in particular is still extremely limited (Kjorsvik et al., 1990, Brooks et al., 1997, Chemineau et al., 2007). Only few studies have demonstrated the role of some factors on reproductive performances of males, among which broodstock nutrition (Izquierdo et al., 2001), stress (Schreck et al., 2001), or body condition (Burness et al., 2008).
Nutrition both before and during a reproductive cycle is important for many fish to be able to reproduce. It was indeed shown that a reduction in feeding rate could cause an inhibition of gonadal maturation in several fish species, including goldfish (Carassius auratus), European seabass (Dicentrarchus labrax) and Atlantic salmon (Salmo salar) (Izquierdo et al., 2001). Percids, as possible capital breeders, are thought to store energy in the adipose tissue (i.e. mesenteric fat in percids) before the beginning of a reproductive cycle to allocate this energy to gonadal growth during gonadogenesis (Wang et al., 2006). Henderson et al. (1996) observed that the mesenteric fat content of female walleye (Sander vitreus) decreased throughout the reproductive cycle while ovarian lipid content increased. From their results, they hypothesized that a female with insufficient mesenteric fat content could not begin a reproductive cycle. Similarly, Sulistyo et al. (2000) found that the highest visceral energy stores in male Eurasian perch (Perca fluviatilis), which developed in summer by an active feeding activity, were later depleted due to gonadal recrudescence. Pikeperch, S. lucioperca, as most early-spring spawners (such as percids or esocids), starts its gametogenesis in late summer and spawns in the following year, depending on the latitude, chiefly in April–May (Lappalainen et al., 2003, Teletchea et al., 2007, Teletchea et al., in press, Müller-Belecke and Zienert, 2008). Hence, gonads mature during winter when food supplies are limited and feeding is reduced. Consequently, the intense feeding period before the onset of the reproductive cycle, i.e. May–July, seems crucial for breeders to store enough energy to be able to start and complete their entire gametogenesis.
In addition, in recirculating system, the husbandry practices to which fish are subjected are probably a major contributory factor affecting gamete quality (Kjorsvik et al., 1990, Brooks et al., 1997). For instance, chronic stress, either due to endogenous (e.g., social interactions) or exogenous (e.g., unfavourable water quality, high densities, handling) stressors, depresses the circulating levels of sexual steroids via the action of cortisol, and in fine may reduce or inhibit gametogenesis (Pankhurst and Van Der Kraak, 1997). Photoperiodic conditions (photoperiod, spectrum and intensity), which can be easily manipulated in recirculating water systems with little cost have been shown to modify fish sensitivity to stress (Huntingford et al., 2006). For instance, Karakatsouli et al. (2007) showed that red light favoured growth while blue light favoured fish acute stress response in rainbow trout Oncorhynchus mykiss juveniles. Migaud et al. (2006) found lower rates in terms of fertilization of eggs, hatching of larvae, and survival of breeders after spawning season for Eurasian perch reared in simulated natural vs natural photoperiodic conditions.
Fractional factorial design experiment allows testing several factors concurrently in few experimental units and thus enables classifying both factors and their possible interactions by order of importance (Box et al., 1978, Ruohonen et al., 2001). In fine, such experiments allow modelling and make a first step towards the optimisation of the system studied. Even though such an approach is still quite new in animal sciences, it is becoming more and more popular, e.g., Babiak et al. (2000), Hamre et al. (2004), Midelet et al. (2006), Gardeur et al. (2007), and Wildman et al. (2007). We performed here an experiment using a fractional factorial design to determine the possible effects and interactions between three nutritional factors and photoperiodic conditions on both male pikeperch condition at spawning and sperm quality.
Section snippets
Fish
Domestic breeders (F1 generation, age 2+, mean weight of 1.1 kg) were purchased from recirculating system in the fish farm Excellence Fish (The Netherlands) on June 28th, 2006. Fish were transferred by truck over ca. 400 km (5:30 h) during the night with low mortality both during (only 2 fish) and after the transfer (no delayed disease). Upon arrival, breeders were evenly distributed into eight 3 m3 outdoor tanks (19–20 fish) in an isolated 40 m3 recirculating system (Domaine de la Bouzule,
Sex determination
Based on the 11 KT assay (realized on October 9–10th), two kinds of individuals were determined: the putative “males” (32.5 ± 22.2 ng mL− 1, n = 96) and the putative “females” (3.8 ± 2.1 ng mL− 1; n = 39), resulting in 12 or13 “males” and 4 or 5 “females”, for a total of 16 to 18 individuals per tank; means significantly different (Kruskal–Wallis test, P < 0.05). The comparison with the actual sex ratio (determined during the spawning season by stripping the males) showed that the method was 95% correct.
Survival and sex determination
In our experience, fish were transported over ca. 400 km by truck and only two fish died. Besides, 95 among the 101 males survived during the entire experiment, even if fish were often handled (sometimes everyday during the spawning season). Similarly, Demska-Zakes and Zakes (2002) observed that the spawner survival rate in their two years of study was 98 and 99%, respectively. Müller-Belecke and Zienert (2008) also found that pikeperch (65 of 69 fish studied) can recover completely from
Conclusion
This study represents the first attempt to better understand the multifactorial determinism of the quality of male pikeperch reproduction, and more specifically the effects of the broodstock management. Our experience clearly demonstrates that among the four tested factors, the initial fat store was the only one to significantly influence, alone or in combination with others, all the eight variables that significantly differed between the eight combinations evaluated (Fig. 8). The initial fat
Acknowledgments
This research was funded by Europe through the project Luciopercimprove (Contract n° 017646; http://webapps.fundp.ac.be/luciopercinprove/fundp.htm). Thanks are also expressed to Czech Republic projects: USB RIFCH MSM 6007665809 and NAZV QH82119. We warmly thank two anonymous reviewers that greatly enhanced the manuscript.
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