Reduced lactate dehydrogenase activity in the heart and suppressed sex hormone levels are associated with female-biased mortality during thermal stress in Pacific salmon

Abstract

Female-biased mortality has been repeatedly reported in Pacific salmon during their upriver migration in both field studies and laboratory holding experiments, especially in the presence of multiple environmental stressors, including thermal stress. Here, we used coho salmon (Oncorhynchus kisutch) to test whether females exposed to elevated water temperatures (18°C) (i) suppress circulating sex hormones (testosterone, 11-ketotestosterone and estradiol), owing to elevated cortisol levels, (ii) have higher activities of enzymes supporting anaerobic metabolism (e.g. lactate dehydrogenase, LDH), (iii) have lower activities of enzymes driving oxidative metabolism (e.g. citrate synthase, CS) in skeletal and cardiac muscle, and (iv) have more oxidative stress damage and reduced capacity for antioxidant defense [lower catalase (CAT) activity]. We found no evidence that a higher susceptibility to oxidative stress contributes to female-biased mortality at warm temperatures. We did, however, find that females had significantly lower cardiac LDH and that 18°C significantly reduced plasma levels of testosterone and estradiol, especially in females. We also found that relative gonad size was significantly lower in the 18°C treatment regardless of sex, whereas relative liver size was significantly lower in females held at 18°C. Further, relative spleen size was significantly elevated in the 18°C treatments across both sexes, with larger warm-induced increases in females. Our results suggest that males may better tolerate bouts of cardiac hypoxia at high temperature, and that thermal stress may also disrupt testosterone- and estradiol-mediated protein catabolism, and the immune response (larger spleens), in migratory female salmon.

Population variability in thermal performance of pre-spawning adult Chinook salmon

“…Indeed, individuals may differ in their performance and thermal capacity via cellular plasticity and local adaptation ( Taylor, 1991 ). Previous work has found population-specific and sex-specific differences in the activity or density of enzymes associated with the metabolic or cardiac function of salmon ( Rodnick et al, 2008 ; Eliason et al, 2011 ; Anttila et al, 2019 ; Little et al, 2020b ), which points to the utility of cellular level investigation and variety of mechanisms that may underlie differences in organismal performance.…”

“…LDH) in tissues with high ATP demand (e.g. heart, red muscle, white muscle) might be locally adapted to thermal conditions and enzyme activity levels measured at different assay temperatures across groups (sex, populations, species) could reveal differences in thermal adaptation ( Little et al, 2020b ). Enzyme activities (CS and LDH) were measured from the ventricle, white and red muscle homogenates to determine the thermal performance of these tissues across 8, 12, 18, 24 or 25 and 28°C using established methods ( Moyes et al, 1997 ; Martínez et al, 2006 ; Little et al, 2020b ).…”

“…heart, red muscle, white muscle) might be locally adapted to thermal conditions and enzyme activity levels measured at different assay temperatures across groups (sex, populations, species) could reveal differences in thermal adaptation ( Little et al, 2020b ). Enzyme activities (CS and LDH) were measured from the ventricle, white and red muscle homogenates to determine the thermal performance of these tissues across 8, 12, 18, 24 or 25 and 28°C using established methods ( Moyes et al, 1997 ; Martínez et al, 2006 ; Little et al, 2020b ). Frozen tissues were sliced, weighed (~25 mg) and homogenized in buffer (0.1% Triton, 50 mmol l −1 HEPES, 1 mmol L −1 EDTA, pH 7.4) with 0.5 mm zirconium oxide beads in a bead beater (Fisherbrand Bead Mill 24 Homogenizer) kept at 4°C for two 6 m s −1 30 s cycles with 1 min on ice in-between.…”

Thermal tolerance of fish to heatwaves in agricultural streams: What does not kill you makes you stronger?

“…More specifically, SOD, CS activity, LDH activity all increased temporally, either after single or multiple heatwaves, implying post‐heatwave compensation costs. Besides temporal changes, the lower SOD in white muscle from 32°C to 34°C represents a reduced energy investment in antioxidant defence (Little et al, 2020). However, with higher respiratory requirements during extreme heatwaves, excessive oxidative stress from the production of reactive oxygen species should be buffered with more antioxidant agents (Heise et al, 2006).…”

Behavioral and electrophysiological study in Colossoma macropomum treated with different concentrations of Nepeta cataria oil in an immersion bath revealed a therapeutic window for anesthesia

“…Metabolic effects, such as changes in blood glucose, blood lactate, hydromineral balance, among others, correspond to the secondary effects of stress in fish, which can lead to a drop in animal production and reproduction, as well as diseases, which are characterized as tertiary stress responses (Gesto et al 2014;Jiang et al 2017;Chang et al 2020;Little et al 2020).…”