Matthew T. Casselman

Using maximum heart rate as a rapid screening tool to determine optimum temperature for aerobic scope in Pacific salmon Oncorhynchus spp.

The mean ±s.e. optimum temperature (T(opt)) for aerobic scope in juvenile coho salmon Oncorhynchus kisutch was determined to be 17·0 ± 0·7° C. The repeated measures protocol took 3 weeks to complete the T(opt) determination using 12 fish tested at five temperatures separated by 2° C increments. This experiment also demonstrated that the T(opt) was associated with maximum heart rate (f(H)) failing to maintain a Q(10) -related increase with temperature. When maximum f(H) was produced in anaesthetized fish with pharmacological stimulation and f(H) measured from electrocardiogram recordings during acute warming, the Arrhenius break temperature (ABT) for Q(10) discontinuities in maximum f(H) (mean ±s.e. = 17·1 ± 0·5° C for 15 ppm clove oil and 16·5 ± 0·2° C for 50 ppm MS-222) was statistically indistinguishable from the T(opt) measured using aerobic scope. Such a determination took only 3 days rather than 3 weeks. Therefore, it is proposed that determining ABT for discontinuities in maximum f(H) in anaesthetized fish presents itself as a valuable, high-throughput screening tool to assess T(opt) in fishes, a metric that has become recognized as being extremely valuable in fish biology and fisheries management.

Burst Swimming in Areas of High Flow: Delayed Consequences of Anaerobiosis in Wild Adult Sockeye Salmon

Wild riverine fishes are known to rely on burst swimming to traverse hydraulically challenging reaches, and yet there has been little investigation as to whether swimming anaerobically in areas of high flow can lead to delayed mortality. Using acoustic accelerometer transmitters, we estimated the anaerobic activity of anadromous adult sockeye salmon (Oncorhynchus nerka) in the tailrace of a diversion dam in British Columbia, Canada, and its effects on the remaining 50 km of their freshwater spawning migration. Consistent with our hypothesis, migrants that elicited burst swimming behaviors in high flows were more likely to succumb to mortality following dam passage. Females swam with more anaerobic effort compared to males, providing a mechanism for the female-biased migration mortality observed in this watershed. Alterations to dam operations prevented the release of hypolimnetic water from an upstream lake, exposing some migrants to supraoptimal, near-lethal water temperatures (i.e., 24°C) that inhibited their ability to locate, enter, and ascend a vertical-slot fishway. Findings from this study have shown delayed post–dam passage survival consequences of high-flow-induced burst swimming in sockeye salmon. We highlight the need for studies to investigate whether dams can impose other carryover effects on wild aquatic animals.

Immune response genes and pathogen presence predict migration survival in wild salmon smolts

We present the first data to link physiological responses and pathogen presence with subsequent fate during migration of wild salmonid smolts. We tagged and non‐lethally sampled gill tissue from sockeye salmon (Oncorhynchus nerka) smolts as they left their nursery lake (Chilko Lake, BC, Canada) to compare gene expression profiles and freshwater pathogen loads with migration success over the first ~1150 km of their migration to the North Pacific Ocean using acoustic telemetry. Fifteen per cent of smolts were never detected again after release, and these fish had gene expression profiles consistent with an immune response to one or more viral pathogens compared with fish that survived their freshwater migration. Among the significantly upregulated genes of the fish that were never detected postrelease were MX (interferon‐induced GTP‐binding protein Mx) and STAT1 (signal transducer and activator of transcription 1‐alpha/beta), which are characteristic of a type I interferon response to viral pathogens. The most commonly detected pathogen in the smolts leaving the nursery lake was infectious haematopoietic necrosis virus (IHNV). Collectively, these data show that some of the fish assumed to have died after leaving the nursery lake appeared to be responding to one or more viral pathogens and had elevated stress levels that could have contributed to some of the mortality shortly after release. We present the first evidence that changes in gene expression may be predictive of some of the freshwater migration mortality in wild salmonid smolts.

Optimum Temperature in Juvenile Salmonids: Connecting Subcellular Indicators to Tissue Function and Whole-Organism Thermal Optimum

Temperature affects processes at all levels of biological organization, but it is unclear whether processes at different levels have similar thermal optima (Topt). Here, we compare the Topt for aerobic scope, a whole-organism measure of performance, with both the Arrhenius breakpoint temperature for maximum heart rate (HR-ABT), a measure of tissue level performance, and the temperature at which AMP-activated protein kinase (AMPK) is phosphorylated in the heart, an indicator of an increase in dependence on anaerobic energy metabolism at the cellular level in juvenile rainbow trout Oncorhynchus mykiss. The Topt for aerobic scope was 19°C, with aerobic scope being maintained at ≥90% of maximum (termed a “Topt window”) from 16.5° to 20.5°C. HR-ABT occurred at , while the profile of AMPK phosphorylation started to change from baseline at 19°C, suggesting that these processes have similar thermal sensitivities as a fish is warmed to Topt. The effects of temperature on AMPK phosphorylation were also measured in coho salmon Oncorhynchus kisutch hearts and compared with previously published values for HR-ABT and aerobic scope Topt. AMPK phosphorylation in coho hearts began to change at temperatures above 17°C, which again is comparable with the published Topt for aerobic scope (17°C) and HR-ABT () in these individuals. Thus, the thermal sensitivity of these subcellular, tissue, and whole-organism functions are highly correlated in both rainbow trout and coho salmon and may depend on each other.

Tracking wild sockeye salmon smolts to the ocean reveals distinct regions of nocturnal movement and high mortality

Few estimates of migration rates or descriptions of behavior or survival exist for wild populations of out-migrating Pacific salmon smolts from natal freshwater rearing areas to the ocean. Using acoustic transmitters and fixed receiver arrays across four years (2010-2013), we tracked the migration of > 1850 wild sockeye salmon (Oncorhynchus nerka) smolts from Chilko Lake, British Columbia, to the coastal Pacific Ocean (> 1000 km distance). Cumulative survival to the ocean ranged 3-10% among years, although this may be slightly underestimated due to technical limitations at the final receiver array. Distinct spatial patterns in both behavior and survival were observed through all years. In small, clear, upper-river reaches, downstream migration largely occurred at night at speeds up to 50 km/d and coincided with poor survival. Among years, only 57-78% of smolts survived the first 80 km. Parallel laboratory experiments revealed excellent short-term survival and unhindered swimming performance of dummy-tagged smolts, suggesting that predators rather than tagging effects were responsible for the initial high mortality of acoustic-tagged smolts. Migration speeds increased in the Fraser River mainstem (~220 km/d in some years), diel movement patterns ceased, and smolt survival generally exceeded 90% in this segment. Marine movement rates and survival were variable across years, with among-year segment-specific survival being the most variable and lowest (19-61%) during the final (and longest, 240 km) marine migration segment. Osmoregulatory preparedness was not expected to influence marine survival, as smolts could maintain normal levels of plasma chloride when experimentally exposed to saltwater (30 ppt) immediately upon commencing their migration from Chilko Lake. Transportation of smolts downstream generally increased survival to the farthest marine array. The act of tagging may have affected smolts in the marine environment in some years as dummy-tagged fish had poorer survival than control fish when transitioned to saltwater in laboratory-based experiments. Current fisheries models for forecasting the number of adult sockeye returning to spawn have been inaccurate in recent years and generally do not incorporate juvenile or smolt survival information. Our results highlight significant potential for early migration conditions to influence adult recruitment.

Association between swimming performance, cardiorespiratory morphometry, and thermal tolerance in Atlantic salmon (Salmo salar L.)

This experiment tested the hypothesis that swimming performance in Atlantic salmon (Salmo salar) parr is connected to cardiorespiratory performance and morphology, as well as maximum heart rate (fHmax) related measures of thermal tolerance. Moreover, it was hypothesized that the cardiorespiratory differences between poor and strong swimmers will be retained in a later life stage, i.e., 15 weeks post-smoltification and seawater transfer. This experiment screened a population of 3,200 parr (11.2 ± 0.25 g) for their swimming performance, classifying them as poor and good swimmers based on their critical swimming speeds (4.4±0.1 body length s-1 and >6.8±0.1 body length s-1, respectively). Compared with poor performing parr, good swimmers had a significantly thicker compact myocardium (by 23.7%) and taller gill secondary lamellae (by 16.2%). In contrast, there was no significant difference in maximum oxygen consumption between the two groups as assessed using a ‘chase’ protocol, and the relationship between heart rate specific measures of thermal tolerance and swim performance was variable. For example, three measures did not differ between the two groups, whereas the Arrhenius breakpoint temperature for fHmax and fHmax were higher and lower, respectively, in the poor swimmers. Importantly, the identified morphological and fHmax differences at the parr stage persisted after 15 weeks of common garden rearing in seawater, and they were associated with an increase in relative ventricular mass and a small, but significant, improvement in growth rate. Therefore, it seems that an early assessment of swimming performance can effectively screen for morphological capacities related to oxygen supply and growth rate, but less so for heart rate related measures of thermal tolerance.

Aerobic scope increases throughout an ecologically relevant temperature range in coho salmon

ABSTRACT Aerobic scope (AS) has been proposed as a functional measurement that can be used to make predictions about the thermal niche of aquatic ectotherms and hence potential fitness outcomes under future warming scenarios. Some salmonid species and populations, for example, have been reported to exhibit different thermal profiles for their AS curves such that AS peaks around the modal river temperature encountered during the upriver spawning migration, suggesting species- and population-level adaptations to river temperature regimes. Interestingly, some other salmonid species and populations have been reported to exhibit AS curves that maintain an upwards trajectory throughout the ecologically relevant temperature range rather than peaking at a modal temperature. To shed further light on this apparent dichotomy, we used adult coho salmon (Oncorhynchus kisutch) to test the prediction that peak AS coincides with population-specific, historically experienced river temperatures. We assessed AS at 10 and 15°C, which represent a typical river migration temperature and the upper limit of the historically experienced temperature range, respectively. We also examined published data on AS in juvenile coho salmon in relation to new temperature data measured from their freshwater rearing environments. In both cases, AS was either maintained or increased modestly throughout the range of ecologically relevant temperatures. In light of existing evidence and the new data presented here, we suggest that when attempting to understand thermal optima for Pacific salmon and other species across life stages, AS is a useful metric of oxygen transport capacity but other thermally sensitive physiological indices of performance and fitness should be considered in concert. Summary: Coho salmon do not conform to existing predictions about the temperature dependence of aerobic scope in Pacific salmon.