Adaptive photoperiod interpretation modulates phenological timing in Atlantic salmon.

Photoperiod, the portion of 24-h cycle during which an organism is exposed to illumination, is an important phenological cue in many animals. However, despite its influence on critical biological processes, there remain many unknowns regarding how variations in light intensity translate into perceived photoperiod. This experiment examined how light intensity variations affect perceived photoperiod in Atlantic salmon (Salmo salar) to determine whether photoperiod interpretation is, a) fixed such that anything above a minimum detection threshold is regarded as 'illumination', or b) adaptive and varies with recent light exposure. To do this we compared the frequency of smoltification and sexual maturation between groups of male parr which were exposed to one of eight light regimes on a 12:12 cycling regime (12-hour day/12-hour night). The eight regimes were divided into two treatments, four with 'High' daytime light intensity and four with 'Low' daytime light intensity. The 'High' and 'Low' intensity treatments were each sub-divided into four groups for which the subjective 'night' light intensity was 100%, 10%, 1% and 0% of the daytime light intensity, with four replicate tanks of each treatment. The results show that above a minimum detection threshold, Atlantic salmon have adaptive photoperiod interpretation which varies with recent light exposure, and that adaptive photoperiod interpretation modulates the timing of the parr-smolt transformation and sexual maturation. Further, we show that photoperiod interpretation varies between closely related families. Given the influence of phenological timing on species survival, our results reveal a critical role for integration of photoperiod interpretation in attempts to understand how geographically shifting thermal niches due to climate change will affect future populations.

The potential for cleaner fish-driven evolution in the salmon louse Lepeophtheirus salmonis: Genetic or environmental control of pigmentation?

The parasitic salmon louse represents one of the biggest challenges to environmentally sustainable salmonid aquaculture across the globe. This species also displays a high evolutionary potential, as demonstrated by its rapid development of resistance to delousing chemicals. In response, farms now use a range of non-chemical delousing methods, including cleaner fish that eat lice from salmon. Anecdotal reports suggest that in regions where cleaner fish are extensively used on farms, lice have begun to appear less pigmented and therefore putatively less visible to cleaner fish. However, it remains an open question whether these observations reflect a plastic (environmental) or adaptive (genetic) response. To investigate this, we developed a pigment scoring system and conducted complimentary experiments which collectively demonstrate that, a) louse pigmentation is strongly influenced by environmental conditions, most likely light, and b) the presence of modest but significant differences in pigmentation between two strains of lice reared under identical conditions. Based on these data, we conclude that pigmentation in the salmon louse is strongly influenced by environmental conditions, yet there are also indications of underlying genetic control. Therefore, lice could display both plastic and adaptive responses to extensive cleaner fish usage where visual appearance is likely to influence survival of lice.

Cyclic Hypoxia Exposure Accelerates the Progression of Amoebic Gill Disease.

Amoebic gill disease (AGD), caused by the amoeba Neoparamoeba perurans, has led to considerable economic losses in every major Atlantic salmon producing country, and is increasing in frequency. The most serious infections occur during summer and autumn, when temperatures are high and poor dissolved oxygen (DO) conditions are most common. Here, we tested if exposure to cyclic hypoxia at DO saturations of 40-60% altered the course of infection with N. perurans compared to normoxic controls maintained at ≥90% DO saturation. Although hypoxia exposure did not increase initial susceptibility to N. perurans, it accelerated progression of the disease. By 7 days post-inoculation, amoeba counts estimated from qPCR analysis were 1.7 times higher in the hypoxic treatment than in normoxic controls, and cumulative mortalities were twice as high (16 ± 4% and 8 ± 2%), respectively. At 10 days post-inoculation, however, there were no differences between amoeba counts in the hypoxic and normoxic treatments, nor in the percentage of filaments with AGD lesions (control = 74 ± 2.8%, hypoxic = 69 ± 3.3%), or number of lamellae per lesion (control = 30 ± 0.9%, hypoxic = 27.9 ± 0.9%) as determined by histological examination. Cumulative mortalities at the termination of the experiment were similarly high in both treatments (hypoxic = 60 ± 2%, normoxic = 53 ± 11%). These results reveal that exposure to cyclic hypoxia in a diel pattern, equivalent to what salmon are exposed to in marine aquaculture cages, accelerated the progression of AGD in post-smolts.

Metabolic and functional impacts of hypoxia vary with size in Atlantic salmon.

The most capricious environmental variable in aquatic habitats, dissolved O2, is fundamental to the fitness and survival of fish. Using swim tunnel respirometry we test how acute exposure to reduced O2 levels, similar to those commonly encountered by fish in crowded streams and on commercial aquaculture farms, affect metabolic rate and swimming performance in Atlantic salmon of three size classes: 0.2, 1.0 and 3.5 kg. Exposure to 45-55% dissolved O2 saturation substantially reduced the aerobic capacity and swimming performance of salmon of all sizes. While hypoxia did not affect standard metabolic rate, it caused a significant decrease in maximum metabolic rate, resulting in reduced absolute and factorial aerobic scope. The most pronounced changes were observed in the smallest fish, where critical swimming speed was reduced from 91 to 70 cm s-1 and absolute aerobic scope dropped by 62% relative to the same measurement in normoxia. In normoxia, absolute critical swimming speed (Ucrit) increased with size, while relative Ucrit, measured in body lengths s-1, was highest in the small fish (3.5) and decreased with larger size (medium = 2.2). Mass specific metabolic rate and cost of transport were inversely related to size, with calculated metabolic scaling exponents of 0.65 for bSMR and 0.78 for bMMR. Metabolic O2 demand increased exponentially with current speed irrespective of fish size (R2 = 0.97-0.99). This work demonstrates that moderate hypoxia reduces the capacity for activity and locomotion in Atlantic salmon, with smaller salmon most vulnerable to hypoxic conditions. As warm and hypoxic conditions become more prevalent in aquatic environments worldwide, understanding local O2 budgets is critical to maximizing the welfare and survival of farmed and wild salmon.