Introduction
The drive to produce larger Atlantic salmon smolts and postsmolts on land, has intensified the production protocols resulting in increased number of postsmolts maturing early. Early maturation represents both an economic and welfare challenge for producers. Causes for early maturation are multiple, including growth rate, energy surplus, photoperiod and temperature among others. The switch in daylength from winter to spring is the cue that entrains onset of sexual maturation (Fjelldal et al., 2018). However, high temperatures are regarded as the most important factor for early maturation (Melo et al., 2014; Pino Martinez et al., 2023) and has shown to stimulate the proses under different photoperiods (Imsland et al., 2014; Martinez et al., 2023). In these studies, high temperature has induced maturation both when kept stable high during the trial (12,15 and 18 °C), and when it has been increased up to 16 °C together with daylength after winter signal. The present study, in contrast, aimed to assess if dropping water temperature from 15 to 8 °C during or after a winter signal can arrest the development of early sexual maturation in Atlantic Salmon postsmolts.
Materials and methods
900 parr were transferred to eight freshwater tanks at the flow-through facilities of the Department of Biological Sciences (University of Bergen, Norway). Four temperature regimes were established in duplicates (Fig 1A). The first group were held at 15 °C throughout the trial (15), as this temperature is shown to promote early sexual maturation in male salmon (Martinez et al., 2023) The second group started at 15 °C and lowered to 8°C after a 5-week LD12:12 winter signal (15-8L). The third group were started at 15°C and lowered to 8 °C at the start of the winter signal (15-8E). The fourth group were held at 8 °C through the experiment (8), as this temperature is shown to inhibit maturation. We performed nine samplings, collecting n= 6 males per tank per sampling. Body and gonad weight were measured and gonadosomatic index was calculated as GSI (%) = Gonad W (g)*100/Body W (g) and used to assess maturation status (Pino Martinez et al., 2023). A Fisher’s Exact Test for Count Data used to find differences in proportion of maturing males between treatments. Statistical analyses were performed in RStudio.
Results
Maturing males were observed in the three 15°C groups from sampling 2, prior and during the winter signal. After the winter signal, a highly synchronized onset of maturation occurred in all males in group 15, and also commenced in an increasing number of individuals in 15-8L and 15-8E (Fig 1B). Hardly any sign of maturation was observed in the group held at 8 °C throughout the experiment. Some individuals maturing in 15-8L and 15-8E displayed very high GSI and running milt, in contrast to those in 15. Interestingly, other males in 15-8L and 15-8E had a relatively low GSI (i.e. 0.29%), but a white foamy testis appearance typical of spermiogenesis (differentiated spermatozoa).
Discussion and conclusions
Temperature determined the life history strategy of the experimental groups, with all males at 15°C maturing at the end, and none at 8 °C. All groups treated at 15°C had some parr maturing, and the maturation seen prior to sampling 6 was all driven only by the high temperature experienced before the LD 12:12 winter signal. The drop in temperature to 8 °C before or after LD 12:12 caused a significant reduction of maturation. However, the increasing number of males found maturing in 15-8L and 15-8E suggests that the decision to mature had been made before the winter signal, and that the drop in temperature did not reverse but only delayed the process in many individuals. Furthermore, the presence of testes in spemiogenic phase but with low GSI suggests that those fish may have irreversibly committed to maturation early, and the swich to cold water only interrupted the proliferative stage and induced meiotic and spermiogenic phases.
References
Fjelldal, P. G., Schulz, R., Nilsen, T. O., Andersson, E., Norberg, B., & Hansen, T. J. (2018). Sexual maturation and smoltification in domesticated Atlantic salmon (Salmo salar L.) – is there a developmental conflict? Physiological Reports, 6(17). https://doi.org/10.14814/phy2.13809
Imsland, A. K., Handeland, S. O., & Stefansson, S. O. (2014). Photoperiod and temperature effects on growth and maturation of pre- and post-smolt Atlantic salmon. Aquaculture International, 22(4). https://doi.org/10.1007/s10499-014-9750-1
Martinez, E. P., Balseiro, P., Fleming, M. S., Stefansson, S. O., Norberg, B., Imsland, A. K. D., & Handeland, S. O. (2023). Interaction of temperature and photoperiod on male postsmolt maturation of Atlantic salmon (Salmo salar L.). Aquaculture, 568. https://doi.org/10.1016/j.aquaculture.2023.739325
Melo, M. C., Andersson, E., Fjelldal, P. G., Bogerd, J., França, L. R., Taranger, G. L., & Schulz, R. W. (2014). Salinity and photoperiod modulate pubertal development in Atlantic salmon (Salmo salar). Journal of Endocrinology, 220(3). https://doi.org/10.1530/JOE-13-0240
Pino Martinez, E., Balseiro, P., Stefansson, S. O., Kaneko, N., Norberg, B., Fleming, M. S., Imsland, A. K. D., & Handeland, S. O. (2023). Interaction of temperature and feed ration on male postsmolt maturation of Atlantic salmon (Salmo salar L.). Aquaculture, 562. https://doi.org/10.1016/j.aquaculture.2022.738877