Body size of male Atlantic salmon (Salmo salar L.) at introduction of a 5-week LD12:12 winter signal influences their decision to mature early or smoltify

Abstract

Sexual maturation of male Atlantic salmon post-smolts (‘jacking’) is undesired in aquaculture and seems to occur due to the intensification in modern facilities. Maturation depends on internal and external factors (temperature, photoperiod, feed availability, energy levels, body size, genetic background) that act on the brain-pituitary-gonad axis to trigger maturation. This study assessed the influence that the body weight at the time of the photoperiod manipulation performed to induce smoltification can have on early maturation or smoltification. For that, 900 parr (41.3 ± 3.7 g) were assigned to four size-photoperiod treatments: constant light (LL), a winter signal (5-week LD12:12) starting when fish was 70.0 ± 8.4 g (70WS), a similar winter signal at 114 ± 9.9 g (110WS) and at 182.9 ± 35.7 g (180WS). The trial took place in fresh water, except for the last 2 weeks in each treatment carried out in full seawater. Body weight and condition, gonadosomatic index and proportion of maturing males, gill Na+, K+, ATPase activity and blood parameters (chloride and sodium, cortisol, glucose and cholesterol) were measured to assess progression of smoltification or maturation. In addition, pituitary messenger RNA (mRNA) transcription of tshβb (a paralog of the thyrotropin thyroid-stimulating hormone) was analysed to investigate its potential role in the regulation of any of the two processes. Results evidenced that body size of male salmon was relevant for the developmental response to a winter signal, be it maturation or smoltification. An early winter signal (70WS and 110WS) induced clearer signs of smoltification (reduced condition factor, high energy mobilization and little stress response in seawater among others) and no tendency to mature early. In contrast, a late or no winter signal (180WS and LL) induced a strong stress response in seawater, poor morphological signs of smolting and energy mobilization, and a higher tendency to mature early. It was difficult to directly relate pituitary tshβb transcription with both smoltification or maturation, because this gene seemed to act primarily as a timekeeper displaying large upregulations in response to increases in daylength (irrespective of size) but no changes under constant light. These results evidence that an increase in daylength when salmon is large enough to have developed sufficiently or accrued energy resources may pose high risk that a proportion of them prioritize sexual maturation over smoltification. Producers may take this into consideration when optimizing protocols for post-smolt production.