Fitness and behavioral correlates of pre-stress and stress-induced plasma cortisol titers in pink salmon (Oncorhynchus gorbuscha) upon arrival at spawning grounds

Semelparous Pacific salmon (Onchorynchus spp.) serve as an excellent model for examining the relationships between life history, behavior and individual variation in glucocorticoid (GC) stress hormone levels because reproductive behaviors are highly variable between individuals and failure to reproduce results in zero fitness. Pink salmon (O. gorbuscha) were intercepted upon arrival at the spawning grounds across three time periods. Pre-stress and stress-induced plasma cortisol concentrations were assessed in relation to behavior, longevity and reproductive success. Results revealed differences between sexes and with arrival time. The study period marked a year of high reproductive success and only nine females (12% of sample) failed to spawn. Female pre-spawn mortalities were characterized by significantly elevated stress-induced cortisol concentrations and decreased longevity as well as pre-stress cortisol above the normal range in pink salmon from the study area. Interestingly, reproductive behaviors were only associated with pre-stress cortisol levels. For females, aggression and mate interaction time were reduced in individuals with elevated pre-stress cortisol concentrations. In males, a similar negative relationship between pre-stress cortisol concentration and mate interaction time was detected. The observed behavioral correlations are likely a factor of social status where dominant individuals, known to have higher reproductive success, are characterized by lower cortisol levels relative to subordinate conspecifics. Findings show both elevated pre-stress and stress-induced cortisol concentrations at arrival to the spawning grounds to be associated with reduced survival.     

The efficacy of field techniques for obtaining and storing blood samples from fishes

Prompted by the dramatic increase in the use of blood analyses in fisheries research and monitoring, this study investigated the efficacy of common field techniques for sampling and storing blood from fishes. Three questions were addressed: (1) Do blood samples taken via rapid caudal puncture (the ‘grab‐and‐stab’ technique) yield similar results for live v. sacrificed groups of fishes? (2) Do rapidly obtained caudal blood samples accurately represent blood properties of fishes prior to capture? (3) Does storage of whole blood in an ice slurry for a working day (8·5 h) modify the properties of the plasma? It was shown that haematocrit, plasma ions, metabolites, stress hormones and sex hormones of caudal blood samples were statistically similar when taken from live v. recently sacrificed groups of adult coho salmon Oncorhynchus kisutch. Moreover, this study confirmed by using paired blood samples from cannulated O. kisutch that blood acquired through the caudal puncture technique (mean ±s.e . 142 ± 26 s after capture) was representative of fish prior to capture. Long‐term (8·5 h) cold storage of sockeye salmon Oncorhynchus nerka whole blood caused significant decreases in plasma potassium and chloride, and a significant increase in plasma glucose. Previous research has suggested that these changes largely result from net movements of ions and molecules between the plasma and erythrocytes, movements that can occur within minutes of storage. Thus, blood samples from fishes should be centrifuged as quickly as practicable in the field for separation of plasma and erythrocytes to prevent potentially misleading data.     

Physiological, energetic and behavioural correlates of successful fishway passage of adult sockeye salmon Oncorhynchus nerka in the Seton River, British Columbia

Electromyogram (EMG) radio telemetry was used in conjunction with physiological biopsy to relate prior physiological condition and subsequent swimming energetics and behaviours to passage success of 13 wild adult sockeye salmon Oncorhynchus nerka at a vertical-slot fishway on the Seton River, British Columbia. At the time of capture, plasma lactate, glucose and cortisol levels indicated that fish were not exhibiting unusually high levels of physiological stress. Very few differences existed between successful and unsuccessful fish in body size, initial plasma physiology and energy state and mean swim speed and energy use during passage. Generally, fish did not employ burst swimming during successful or failed attempts at passage, indicating that failure was probably not related to metabolic acidosis. Plasma Na⁺ concentration was significantly lower in unsuccessful fish ( P < 0·05), which is suggestive of a depressed ionic state or a possible stress component, although values in all fish were within an expected range for migrant adult O. nerka . Nevertheless, six of 13 fish failed to reascend the fishway and remained in the tailrace of the dam for more than a day on average before moving downstream and away from the dam. During this time, fish were observed actively seeking a means of passage, suggesting that there may have been other, undetermined causes of passage failure.     

Physiological and molecular endocrine changes in maturing wild sockeye salmon, <Emphasis Type="Italic">Oncorhynchus nerka</Emphasis>, during ocean and river migration

Maturing adult sockeye salmon Oncorhynchus nerka were intercepted while migrating in the ocean and upstream in freshwater over a combined distance of more than 1,300 km to determine physiological and endocrine changes associated with ionoregulation. Sockeye migrating through seawater and freshwater showed consistent declines in gill Na⁺/K⁺-ATPase (NKA) activity, plasma osmolality and plasma chloride concentration. In contrast, plasma sodium concentration became elevated in seawater as fish approached the river mouth and was then restored after sockeye entered the river. Accompanying the movement from seawater to freshwater was a significant increase in mRNA for the NKA α1a subunit in the gill, with little change in the α1b subunit. Potential endocrine signals stimulating the physiological changes during migration were assessed by measuring plasma cortisol and prolactin (Prl) concentrations and quantifying mRNA extracted from the gill for glucocorticoid receptors 1 and 2 (GR1 and GR2), mineralocorticoid receptor (MR), growth hormone 1 receptor (GH1R), and prolactin receptor (PrlR). Plasma cortisol and prolactin concentrations were high in seawater suggesting a preparatory endocrine signal before freshwater entry. Generally, the mRNA expression for GR1, GR2 and MR declined during migration, most notably after fish entered freshwater. In contrast, PrlR mRNA increased throughout migration, particularly as sockeye approached the spawning grounds. A highly significant association existed between gill PrlR mRNA and gill NKA α1a mRNA. GH1R mRNA also increased significantly, but only after sockeye had migrated beyond tidal influence in the river and then again just before the fish reached the spawning grounds. These findings suggest that cortisol and prolactin stimulate ionoregulation in the gill as sockeye salmon adapt to freshwater.     

Sex and proximity to reproductive maturity influence the survival, final maturation, and blood physiology of Pacific salmon when exposed to high temperature during a simulated migration

Some Pacific salmon populations have been experiencing increasingly warmer river temperatures during their once-in-a-lifetime spawning migration, which has been associated with en route and prespawn mortality. The mechanisms underlying such temperature-mediated mortality are poorly understood. Wild adult pink (Oncorhynchus gorbuscha) and sockeye (Oncorhynchus nerka) salmon were used in this study. The objectives were to investigate the effects of elevated water temperature on mortality, final maturation, and blood properties under controlled conditions that simulated a "cool" (13°C) and "warm" (19°C) freshwater spawning migration. After 10 d at 13°C, observed mortality was 50%-80% in all groups, which suggested that there was likely some mortality associated with handling and confinement. Observed mortality after 10 d at 19°C was higher, reaching ≥98% in male pink salmon and female pink and sockeye salmon. Thus, male sockeye salmon were the most thermally tolerant (54% observed mortality). Model selection supported the temperature- and sex-specific mortality patterns. The pink salmon were closer to reproductive maturation and farther along the senescence trajectory than sockeye salmon, which likely influenced their survival and physiological responses throughout the experiment. Females of both species held at 19°C had reduced plasma sex steroids compared with those held at 13°C, and female pink salmon were less likely to become fully mature at 19° than at 13°C. Male and female sockeye salmon held at 19°C had higher plasma chloride and osmolality than those held at 13°C, indicative of a thermally related stress response. These findings suggest that sex differences and proximity to reproductive maturity must be considered when predicting thermal tolerance and the magnitude of en route and prespawn mortality for Pacific salmon.     

Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations

Concern over global climate change is widespread, but quantifying relationships between temperature change and animal fitness has been a challenge for scientists. Our approach to this challenge was to study migratory Pacific salmon (Oncorhynchus spp.), fish whose lifetime fitness hinges on a once-in-a-lifetime river migration to natal spawning grounds. Here, we suggest that their thermal optimum for aerobic scope is adaptive for river migration at the population level. We base this suggestion on several lines of evidence. The theoretical line of evidence comes from a direct association between the temperature optimum for aerobic metabolic scope and the temperatures historically experienced by three Fraser River salmon populations during their river migration. This close association was then used to predict that the occurrence of a period of anomalously high river temperatures in 2004 led to a complete collapse of aerobic scope during river migration for a portion of one of the sockeye salmon (Oncorhynchus nerka) populations. This prediction was corroborated with empirical data from our biotelemetry studies, which tracked the migration of individual sockeye salmon in the Fraser River and revealed that the success of river migration for the same sockeye population was temperature dependent. Therefore, we suggest that collapse of aerobic scope was an important mechanism to explain the high salmon mortality observed during their migration. Consequently, models based on thermal optima for aerobic scope for ectothermic animals should improve predictions of population fitness under future climate scenarios.     

Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha)

This study was undertaken to provide a comprehensive set of data relevant to disclosing the physiological effects and possible oxygen transport limitations in the Chinook salmon (Oncorhynchus tshawytscha) during an acute temperature change. Fish were instrumented with a blood flow probe around the ventral aorta and catheters in the dorsal aorta and sinus venosus. Water temperature was progressively increased from 13 degrees C in steps of 4 degrees C up to 25 degrees C. Cardiac output increased from 29 to 56 ml.min(-1).kg(-1) between 13 and 25 degrees C through an increase in heart rate (58 to 105 beats/min). Systemic vascular resistance was reduced, causing a stable dorsal aortic blood pressure, yet central venous blood pressure increased significantly at 25 degrees C. Oxygen consumption rate increased from 3.4 to 8.7 mg.min(-1).kg(-1) during the temperature increase, although there were signs of anaerobic respiration at 25 degrees C in the form of increased blood lactate and decreased pH. Arterial oxygen partial pressure was maintained during the heat stress, although venous oxygen partial pressure (Pv(O(2))) and venous oxygen content were significantly reduced. Cardiac arrhythmias were prominent in three of the largest fish (>4 kg) at 25 degrees C. Given the switch to anaerobic metabolism and the observation of cardiac arrhythmias at 25 degrees C, we propose that the cascade of venous oxygen depletion results in a threshold value for Pv(O(2)) of around 1 kPa. At this point, the oxygen supply to systemic and cardiac tissues is compromised, such that the oxygen-deprived and acidotic myocardium becomes arrhythmic, and blood perfusion through the gills and to the tissues becomes compromised.     

Altering the Binding Properties of PRDM9 Partially Restores Fertility across the Species Boundary

Sterility or subfertility of male hybrid offspring is commonly observed. This phenomenon contributes to reproductive barriers between the parental populations, an early step in the process of speciation. One frequent cause of such infertility is a failure of proper chromosome pairing during male meiosis. In subspecies of the house mouse, the likelihood of successful chromosome synapsis is improved by the binding of the histone methyltransferase PRDM9 to both chromosome homologs at matching positions. Using genetic manipulation, we altered PRDM9 binding to occur more often at matched sites, and find that chromosome pairing defects can be rescued, not only in an intersubspecific cross, but also between distinct species. Using different engineered variants, we demonstrate a quantitative link between the degree of matched homolog binding, chromosome synapsis, and rescue of fertility in hybrids between Mus musculus and Mus spretus. The resulting partial restoration of fertility reveals additional mechanisms at play that act to lock-in the reproductive isolation between these two species.     

The effects of experimental energy depletion on the physiological condition and survival of adult sockeye salmon (<Emphasis Type="Italic">Oncorhynchus nerka</Emphasis>) during spawning migration

In 2005 and 2006, adult sockeye salmon (Oncorhynchus nerka) were captured en route to spawning grounds and placed in either a slow (∼ 0.1 m·s⁻¹) or fast (∼0.4 m·s⁻¹) water velocity treatment for 18 days in order to assess how migrational energy depletion during the final stages of maturation affected physiological condition and survival. Fish in the fast treatment utilized more energy than the slow treatment in 2005 (0.91 MJ kg⁻¹ vs. 0.43 MJ kg⁻¹; P = 0.010), and 2006 (0.72 MJ kg⁻¹ vs. 0.37 MJ kg⁻¹; P = 0.021). Non-treatment fish captured upon arrival at spawning grounds showed energy levels intermediate to the two treatments in 2005 and lower than both in 2006, suggesting that energy use during the treatments were within levels normally experienced by this population. No differences in survival were found between treatments (P > 0.05), although females had lower survival than males in both years (both P < 0.01). After 18 days, surviving fish from the fast treatment showed signs of elevated physiological stress relative to fish from the slow treatment. Specifically, plasma osmolality was lower in fast fish in 2005 (P < 0.001), as was plasma chloride in both years (both P < 0.02). In 2006, plasma lactate was higher (P = 0.014) in fast fish. Within the ranges of energetic depletion that were examined here, a more energy-intensive migration can have a substantial influence on the physiological condition and stress of adult sockeye salmon, but not on survival.