Thermal tolerance and vulnerability to warming differ between populations of wild Oncorhynchus mykiss near the species' southern range limit.

Fish habitat temperatures are increasing due to human impacts including climate change. For broadly distributed species, thermal tolerance can vary at the population level, making it challenging to predict which populations are most vulnerable to warming. Populations inhabiting warm range boundaries may be more resilient to these changes due to adaptation or acclimatization to warmer temperatures, or they may be more vulnerable as temperatures may already approach their physiological limits. We tested functional and critical thermal tolerance of two populations of wild Oncorhynchus mykiss near the species' southern range limit and, as predicted, found population-specific responses to temperature. Specifically, the population inhabiting the warmer stream, Piru Creek, had higher critical thermal maxima and higher functional thermal tolerance compared to the population from the cooler stream, Arroyo Seco. Arroyo Seco O. mykiss are more likely to experience a limitation of aerobic scope with warming. Piru Creek O. mykiss, however, had higher resting metabolic rates and prolonged exercise recovery, meaning that they could be more vulnerable to warming if prey or dissolved oxygen become limited. Temperature varies widely between streams near the O. mykiss southern range limit and populations will likely have unique responses to warming based on their thermal tolerances and metabolic requirements.

Corrigendum to: Sex-specific differences in swimming, aerobic metabolism and recovery from exercise in adult coho salmon (Oncorhynchus kisutch) across ecologically relevant temperatures.

[This corrects the article DOI: 10.1093/conphys/coab016.].

Sex-specific differences in swimming, aerobic metabolism and recovery from exercise in adult coho salmon (Oncorhynchus kisutch) across ecologically relevant temperatures.

Adult female Pacific salmon can have higher migration mortality rates than males, particularly at warm temperatures. However, the mechanisms underlying this phenomenon remain a mystery. Given the importance of swimming energetics on fitness, we measured critical swim speed, swimming metabolism, cost of transport, aerobic scope (absolute and factorial) and exercise recovery in adult female and male coho salmon (Oncorhynchus kisutch) held for 2 days at 3 environmentally relevant temperatures (9°C, 14°C, 18°C) in fresh water. Critical swimming performance (U crit) was equivalent between sexes and maximal at 14°C. Absolute aerobic scope was sex- and temperature-independent, whereas factorial aerobic scope decreased with increasing temperature in both sexes. The full cost of recovery from exhaustive exercise (excess post-exercise oxygen consumption) was higher in males compared to females. Immediately following exhaustive exercise (i.e. 1 h), recovery was impaired at 18°C for both sexes. At an intermediate time scale (i.e. 5 h), recovery in males was compromised at 14°C and 18°C compared to females. Overall, swimming, aerobic metabolism, and recovery energetics do not appear to explain the phenomenon of increased mortality rates in female coho salmon. However, our results suggest that warming temperatures compromise recovery following exhaustive exercise in both male and female salmon, which may delay migration progression and could contribute to en route mortality.

Field assessments of heart rate dynamics during spawning migration of wild and hatchery-reared Chinook salmon.

During spawning, adult Pacific salmonids (Oncorhynchus spp.) complete challenging upriver migrations during which energy and oxygen delivery must be partitioned into activities such as locomotion, maturation and spawning behaviours under the constraints of an individual's cardiac capacity. To advance our understanding of cardiac function in free-swimming fishes, we implanted migrating adult Chinook salmon (Oncorhynchus tshawytscha) collected near the mouth of the Sydenham River, Ontario, with heart rate (fH) biologgers that recorded fH every 3 min until these semelparous fish expired on spawning grounds several days later. Fundamental aspects of cardiac function were quantified, including resting, routine and maximum fH, as well as scope for fH (maximum-resting fH). Predictors of fH were explored using generalized least-squares regression, including water temperature, discharge, fish size and fish origin (wild versus hatchery). Heart rate was positively correlated with water temperature, which aligned closely with daily and seasonal shifts. Wild fish had slower resting heart rates than hatchery fish, which led to significantly higher scope for fH. Our findings suggest that wild salmon may have better cardiac capacity during migration than hatchery fish, potentially promoting migration success in wild fish. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

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

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.

Cardiac Performance of Free-Swimming Wild Sockeye Salmon during the Reproductive Period.

Researchers have surmised that the ability to obtain dominance during reproduction is related to an individual's ability to better sequester the energy required for reproductive behaviors and develop secondary sexual characteristics, presumably through enhanced physiological performance. However, studies testing this idea are limited. Using sockeye salmon (Oncorhynchus nerka), we explored the relationship between heart rate and dominance behavior during spawning. We predicted that an individual's reproductive status and energy requirements associated with dominance can be assessed by relating routine heart rate to changes in spawning status over time (i.e., shifts among aggregation, subordinance, and dominance). Thus, we used routine heart rate as a proxy of relative energy expenditure. Heart rate increased with temperature, as expected, and was higher during the day than at night, a known diel pattern that became less pronounced as the spawning period progressed. Routine heart rate did not differ between sexes and average heart rate of the population did not differ among reproductive behaviors. At the individual level, heart rate did not change as behavior shifted from one state to another (e.g., dominance versus aggregation). No other trends existed between routine heart rate and sex, secondary sexual characteristics, survival duration or spawning success (for females only). Therefore, while our study revealed the complexity of the relationships between cardiac performance and reproductive behaviors in wild fish and demonstrated the importance of considering environmental factors when exploring individual heart rate, we found no support for heart rate being related to specific spawning behavioral status or secondary sexual characteristics.

Rendimiento Cardíaco del Salmón Rojo Salvaje que Natación Libre durante el Período ReproductivoLos investigadores han conjeturado que la capacidad de obtener dominio durante la reproducción está relacionada con la capacidad de un individuo de obtener mejor la energía requerida para los comportamientos reproductivos y desarrollar características sexuales secundarias, presumiblemente a través de un mejor rendimiento fisiológico. Sin embargo, los estudios que prueban esta idea son limitados. Usando Salmón rojo (Oncorhynchus nerka), exploramos la relación entre la frecuencia cardíaca y el comportamiento de dominación durante el desove. Predijimos que el estado reproductivo de un individuo y los requisitos de energía asociados con el dominio pueden evaluarse relacionando la frecuencia cardíaca de rutina con los cambios en el estado de desove a lo largo del tiempo (es decir, cambios entre la agregación, la subordinación y el dominio). Por lo tanto, utilizamos la frecuencia cardíaca de rutina como un proxy del gasto energético relativo. La frecuencia cardíaca aumentó con la temperatura, como se esperaba, y fue más alta durante el día que por la noche, un patrón conocido que se hizo menos pronunciado a medida que avanzaba el período de desove. La frecuencia cardíaca de rutina no difirió entre sexos y la frecuencia cardíaca promedio de la población no difirió entre los comportamientos reproductivos. A nivel individual, la frecuencia cardíaca no cambió a medida que el comportamiento cambió de un estado a otro (i.e., dominación vs. agregación). No se observaron otras tendencias entre la frecuencia cardíaca y el sexo de rutina, las características sexuales secundarias, la duración de la supervivencia o el éxito del desove (solo para hembras). Por lo tanto, si bien nuestro estudio reveló la complejidad de las relaciones entre el rendimiento cardíaco y los comportamientos reproductivos en el Salmón rojo y demostró la importancia de considerar los factores ambientales al explorar la frecuencia cardíaca individual, no encontramos respaldo para la frecuencia cardíaca relacionada con el estado conductual de desove específico o características sexuales secundarias.Translated to Spanish by J. Heras (herasj01@gmail.com).

Desempenho Cardíaco de Natação Livre em Salmão Sockeye Selvagem durante o Período ReprodutivoOs pesquisadores supuseram que a capacidade de obter dominância durante a reprodução está relacionada à capacidade de um indivíduo em melhor obter e aplicar a energia necessária para comportamentos reprodutivos e desenvolver características sexuais secundárias, presumivelmente por meio de um desempenho fisiológico aprimorado. No entanto, os estudos que testam essa ideia são limitados. Usando salmão sockeye (Oncorhynchus nerka), exploramos a relação entre a frequência cardíaca e o comportamento de dominância durante a desova.Previmos que o estado reprodutivo de um indivíduo e os requisitos de energia associados à dominância podem ser avaliados relacionando a freqüência cardíaca de rotina às mudanças no status de desova ao longo do tempo (ou seja, mudanças entre agregação, subordinação e dominância). Assim, usamos a frequência cardíaca de rotina como um indicador do relativo gasto energético. A frequência cardíaca aumentou com a temperatura, conforme o esperado, e foi maior durante o dia do que à noite, um conhecido padrão de diel que se tornou menos pronunciado à medida que o período de desova progredia. A frequência cardíaca de rotina não diferiu entre os sexos e a frequência cardíaca média da população não diferiu entre os comportamentos reprodutivos. No nível individual, a frequência cardíaca não mudou à medida que o comportamento mudou de um estado para outro (por exemplo, dominância versus agregação). Não foram observadas outras tendências entre freqüência cardíaca de rotina e sexo, características sexuais secundárias, duração da sobrevivência ou sucesso da desova (somente para mulheres). Portanto, embora nosso estudo tenha revelado a complexidade das relações entre desempenho cardíaco e comportamentos reprodutivos em peixes selvagens e demonstrado a importância de considerar fatores ambientais ao explorar a frequência cardíaca individual, não encontramos suporte que frequência cardíaca esteja relacionada ao status comportamental de desova específico ou à características sexuais secundárias.Translated to Portuguese by Diego Vaz (dbistonvaz@vims.edu).

Oxygen uptake in Pacific salmon Oncorhynchus spp.: when ecology and physiology meet.

Over the past several decades, a substantial amount of research has examined how cardiorespiratory physiology supports the diverse activities performed throughout the life cycle of Pacific salmon, genus Oncorhynchus. Pioneering experiments emphasized the importance of aerobic scope in setting the functional thermal tolerance for activity in fishes. Variation in routine metabolism can have important performance and fitness consequences as it is related to dominance, aggression, boldness, territoriality, growth rate, postprandial oxygen consumption, life history, season, time of day, availability of shelter and social interactions. Wild fishes must perform many activities simultaneously (e.g. swim, obtain prey, avoid predators, compete, digest and reproduce) and oxygen delivery is allocated among competing organ systems according to the capacity of the heart to deliver blood. For example, salmonids that are simultaneously swimming and digesting trade-off maximum swimming performance in order to support the oxygen demands of digestion. As adult Pacific salmonids cease feeding in the ocean prior to their home migration, endogenous energy reserves and cardiac capacity are primarily partitioned among the demands for swimming upriver, sexual maturation and spawning behaviours. Furthermore, the upriver spawning migration is under strong selection pressure, given that Pacific salmonids are semelparous (single opportunity to spawn). Consequently, these fishes optimize energy expenditures in a number of ways: strong homing, precise migration timing, choosing forward-assist current paths and exploiting the boundary layer to avoid the strong currents in the middle of the river, using energetically efficient swimming speeds, and recovering rapidly from anaerobic swimming. Upon arrival at the spawning ground, remaining energy can be strategically allocated to the various spawning behaviours. Strong fidelity to natal streams has resulted in reproductively isolated populations that appear to be locally adapted physiologically to their specific environmental conditions. Populations with more challenging migrations have enhanced cardiorespiratory performance. Pacific salmonids are able to maintain aerobic scope across the broad range of temperatures encountered historically during their migration; however, climate change-induced river warming has created lethal conditions for many populations, raising conservation concerns. Despite considerable research examining cardiorespiratory physiology in Pacific salmonids over the last 70 years, critical knowledge gaps are identified.

Facing warm temperatures during migration: cardiac mRNA responses of two adult Oncorhynchus nerka populations to warming and swimming challenges.

The main findings of the current study were that exposing adult sockeye salmon Onchorhynchus nerka to a warm temperature that they regularly encounter during their river migration induced a heat shock response at an mRNA level, and this response was exacerbated with forced swimming. Similar to the heat shock response, increased immune defence-related responses were also observed after warm temperature treatment and with a swimming challenge in two different populations (Chilko and Nechako), but with some important differences. Microarray analyses revealed that 347 genes were differentially expressed between the cold (12-13° C) and warm (18-19° C) treated fish, with stress response (GO:0006950) and response to fungus (GO:0009620) elevated with warm treatment, while expression for genes involved in oxidative phosphorylation (GO:0006119) and electron transport chain (GO:0022900) elevated for cold-treated fish. Analysis of single genes with real-time quantitative PCR revealed that temperature had the most significant effect on mRNA expression levels, with swimming and population having secondary influences. Warm temperature treatment for the Chilko population induced expression of heat shock protein (hsp) 90α, hsp90ß and hsp30 as well as interferon-inducible protein. The Nechako population, which is known to have a narrower thermal tolerance window than the Chilko population, showed even more pronounced stress responses to the warm treatment and there was significant interaction between population and temperature treatment for hsp90ß expression. Moreover, significant interactions were noted between temperature treatment and swimming challenge for hsp90α and hsp30, and while swimming challenge alone increased expression of these hsps, the expression levels were significantly elevated in warm-treated fish swum to exhaustion. In conclusion, it seems that adult O. nerka currently encounter conditions that induce several cellular defence mechanisms during their once-in-the-lifetime migration. As river temperatures continue to increase, it remains to be seen whether or not these cellular defences provide sufficient protection for all O. nerka populations.

Low cardiac and aerobic scope in a coastal population of sockeye salmon Oncorhynchus nerka with a short upriver migration.

This study showed that a coastal population (Harrison) of Fraser River sockeye salmon Oncorhynchus nerka had a lower aerobic and cardiac scope compared with interior populations with more challenging upriver spawning migrations, providing additional support to the idea that Fraser River O. nerka populations have adapted physiologically to their local migratory environment.

Calibrating acoustic acceleration transmitters for estimating energy use by wild adult Pacific salmon.

This study is the first to calibrate acceleration transmitters with energy expenditure using a vertebrate model species. We quantified the relationship between acoustic accelerometer output and oxygen consumption across a range of swim speeds and water temperatures for Harrison River adult sockeye salmon (Oncorhynchus nerka). First, we verified that acceleration transmitters with a sampling frequency of 10 Hz could be used as a proxy for movement in sockeye salmon. Using a mixed effects model, we determined that tailbeat frequency and acceleration were positively correlated (p<0.0001), independent of tag ID. Acceleration (p<0.0001) was positively related to swim speed while fork length (p=0.051) was negatively related to swim speed. Oxygen consumption and accelerometer output (p<0.0001) had a positive linear relationship and were temperature dependent (p<0.0001). There were no differences in swim performance (F(2,12)=1.023, p=0.820) or oxygen consumption (F(1,12)=0.054, p=0.332) between tagged and untagged individuals. Five tagged fish were released into the Fraser River estuary and manually tracked. Of the five fish, three were successfully tracked for 1h. The above relationships were used to determine that the average swim speed was 1.25±0.03 body lengths s(-1) and cost of transport was 3.39±0.17 mg O(2) kg(-1)min(-1), averaged across the three detected fish. Acceleration transmitters can be effectively used to remotely evaluate fine-scale behavior and estimate energy consumption of adult Pacific salmon throughout their homeward spawning migration.

The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka).

The mechanism underlying the decrease in aerobic scope in fish at warm temperatures is not fully understood and is the focus of this research. Our study examined oxygen uptake and delivery in resting, swimming and recovering sockeye salmon while water temperature was acutely increased from 15 degrees C to 24 degrees C in 2 degrees C h(-1) increments. Fish swam at a constant speed during the temperature change. By simultaneously measuring oxygen consumption (M(O(2))), cardiac output (Q) and the blood oxygen status of arterial and venous blood, we were able to determine where in the oxygen cascade a limitation appeared when fish stopped sustained swimming as temperature increased. High temperature fatigue of swimming sockeye salmon was not a result of a failure of either oxygen delivery to the gills or oxygen diffusion at the gills because oxygen partial pressure (P(O(2))) and oxygen content (C(O(2))) in arterial blood did not decrease with increasing temperature, as would be predicted for such limitations. Instead, arterial oxygen delivery (Ta(O(2))) was initially hampered due to a failure to adequately increase Q with increasing temperature. Subsequently, lactate appeared in the blood and venous P(O(2)) remained constant.