Advanced ovarian development of Murray cod Maccullochella peelii peelii via phase-shifted photoperiod and two temperature regimes

Abstract

The timing and characteristics of reproductive development in adult female Murray cod exposed to a simulated seasonal photothermal cycle (14:45 to 09:45 daylight h; 12–26 °C) (CONTROL) were compared to the development of females exposed to a three month phase-shifted (advanced) seasonal photothermal cycle (PHOTOTHERMAL) and to females exposed to a three month phase-shifted (advanced) photoperiod cycle in combination with constant temperature (19.5 °C) (PHOTOPERIOD). Females in PHOTOTHERMAL and PHOTOPERIOD treatments reached maturity up to three (June) and four (May) months in advance of CONTROL fish (October), respectively. Biannual maturation was also observed in four PHOTOPERIOD females (13%). Mean ovary diameter and relative fecundity of mature females were similar between treatments (p > 0.05), and viable eggs were produced in all groups (100% ovulated; 14.02%–39.12% mean survival to hatching). Ovary diameters and plasma levels of E₂ and T in phase-shifted females remained at basal levels and/or were significantly reduced (p < 0.05) relative to CONTROL fish throughout the early to mid phases of the maturation period. However, rapid increases in plasma T (0.54–4.39 ng ml^− 1) and ovary diameter (20.0–42.4 mm) in the 60 to 90 days preceding the onset of maturity in phase-shifted females revealed a capacity of Murray cod to accelerate development processes to compensate for earlier delays in photo-responsiveness. Low levels of E₂ that persisted throughout the maturation period of PHOTOTHERMAL and PHOTOPERIOD females did not appear to greatly affect ovarian growth. The successful maturation of photoperiodically-manipulated females under constant temperature demonstrates an alternative approach for influencing maturation patterns in Murray cod that may improve the versatility and cost-effectiveness of broodstock conditioning procedures.

Introduction

The Australian Murray cod Maccullochella peelii peelii is a large endemic freshwater fish with a distinct annual reproductive cycle and seasonally-defined spawning period (Rowland, 1998). Gonad development is initiated in austral autumn (March) and is generally completed by September as water temperatures approach 20 °C (Gooley et al., 1995, Newman et al., 2007).

Murray cod are currently the basis of a small, but emerging domestic and international aquaculture industry (Ingram et al., 2005). Intensive production methods for this species are developed (Ingram and De Silva, 2004), however, the confined spawning period and the current dependency of hatcheries on spawn harvested from earthen ponds, means that the present supply of seed stock commonly suffers from a lack of continuity and inconsistent production. The use of modified seasonal cycles of photoperiod and water temperature to advance the timing of broodstock maturation and spawning (reviewed by Bromage et al., 2001) appears to offer the greatest potential towards overcoming current restraints to Murray cod gamete production. However, the adaptation of these methods to this species is unrefined and is yet to be formally evaluated.

Various alterations to seasonal photothermal cycles have been employed to advance reproduction in a number of fish species, including uniformly compressed cycles, phase-shifted cycles, and strategic combinations of constant short and long days (e.g. Blythe et al., 1994a, Tate & Helfrich, 1998, Davies & Bromage, 2002). Photoperiod is generally acknowledged as the principal regulatory component in each of these regimes (Bromage et al., 2001), however, many environmental control protocols have ensured that both photoperiod and temperature cycles are modified concomitantly so that synergistic interaction between the two factors is maintained. Preserving the natural light-temperature interaction would theoretically enable conditions during gonad development to be optimised. However, in temperate zones, modifying high-amplitude seasonal temperature cycles so that they are in synergy with altered photoperiod cycles demands considerable heating and cooling of broodstock holding water and as a consequence, photothermal control of reproduction typically requires specialised thermal conditioning facilities that are often limited to their specific function. Therefore, the development of modified photoperiod cycles in conjunction with constant temperatures should enable individual rearing systems to facilitate more than one farming activity (e.g. division of broodstock to separate lighting regimes; egg/larval rearing; grow-out production; etc.) and thereby improve the versatility and cost-effectiveness of commercial operations. Nevertheless, the adoption of such alternative thermal regimes must first ensure that gonad function and photo-responsiveness of fish are not adversely impacted.

The present study quantified the effects of phase-shifted seasonal phototherm (incl. cycling temperature) and phase-shifted seasonal photoperiod (incl. constant temperature) on the timing of maturation and reproductive performance of female Murray cod. Temporal changes in ovary diameter (via ultrasound) and levels of plasma gonad steroids (17β-oestradiol [E₂] and testosterone [T]) were monitored throughout the reproductive cycle to indicate changes in oocyte development (Hobby & Pankhurst, 1997, Newman et al., 2008a).