Andrew G. Lotto

The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks

SUMMARY Our knowledge of the swimming capabilities and metabolic rates of adult salmon, and particularly the influence of temperature on them, is extremely limited, and yet this information is critical to understanding the remarkable upstream migrations that these fish can make. To remedy this situation, we examined the effects of temperature on swimming performance and metabolic rates of 107 adult fish taken from three stocks of sockeye salmon Oncorhynchus nerka and one stock of coho salmon O. kisutch at various field and laboratory locations, using large, portable, swim tunnels. The salmon stocks were selected because of differences in their ambient water temperature (ranging from 5°C to 20°C) and the total distance of their in-river migrations (ranging from ∼100 km for coastal stocks to ∼1100 km for interior stocks). As anticipated, differences in routine metabolic rate observed among salmon stocks were largely explained by an exponential dependence on ambient water temperature. However, the relationship between water temperature and maximum oxygen consumption (ṀO2max), i.e. the ṀO2 measured at the critical swimming speed (Ucrit), revealed temperature optima for ṀO2max that were stock-specific. These temperature optima were very similar to the average ambient water temperatures for the natal stream of a given stock. Furthermore, at a comparable water temperature, the salmon stocks that experienced a long and energetically costly in-river migration were characterized by a higher ṀO2max, a higher scope for activity, a higher Ucrit and, in some cases, a higher cost of transport, relative to the coastal salmon stocks that experience a short in-river migration. We conclude that high-caliber respirometry can be performed in a field setting and that stock-specific differences in swimming performance of adult salmon may be important for understanding upstream migration energetics and abilities.

Excess post-exercise oxygen consumption in adult sockeye ( Oncorhynchus nerka) and coho (O. kisutch) salmon following critical speed swimming

SUMMARY The present study measured the excess post-exercise oxygen cost (EPOC) following tests at critical swimming speed (Ucrit) in three stocks of adult, wild, Pacific salmon (Oncorhynchus sp.) and used EPOC to estimate the time required to return to their routine level of oxygen consumption (recovery time) and the total oxygen cost of swimming to Ucrit. Following exhaustion at Ucrit, recovery time was 42–78 min, depending upon the fish stock. The recovery times are several-fold shorter than previously reported for juvenile, hatchery-raised salmonids. EPOC varied fivefold among the fish stocks, being greatest for Gates Creek sockeye salmon (O. nerka), which was the salmon stock that had the longest in-river migration, experienced the warmest temperature and achieved the highest maximum oxygen consumption compared with the other salmon stocks that were studied. EPOC was related to Ucrit, which in turn was directly influenced by ambient test temperature. The non-aerobic cost of swimming to Ucrit was estimated to add an additional 21.4–50.5% to the oxygen consumption measured at Ucrit. While these non-aerobic contributions to swimming did not affect the minimum cost of transport, they were up to three times higher than the value used previously for an energetic model of salmon migration in the Fraser River, BC, Canada. As such, the underestimate of non-aerobic swimming costs may require a reevaluation of the importance of how in-river barriers like rapids and bypass facilities at dams, and year-to-year changes in river flows and temperatures, affect energy use and hence migration success.

Exposure to high temperature influences the behaviour, physiology, and survival of sockeye salmon during spawning migration

Since 1996, some populations of Fraser River sockeye salmon (Oncorhynchus nerkaWalbaum in Artedi, 1792) have begun spawning migrations weeks earlier than normal, and most perish en route as a result. We suspect that a high midsummer river temperature is the principal cause of mortality. We intercepted 100 sockeye during normal migration near a spawning stream and measured somatic energy and aspects of plasma biochemistry. Fish were then held at either 10 or 18 8C for 24 days. Before release, fish were biopsied again and implanted with acoustic transmitters. A group of bi- opsied but untreated control salmon were released at the same time. Sixty-two percent (8 of 13) of control salmon and 68% (21 of 31) of 10 8C salmon reached spawning areas. The 18 8C-treated fish were half as successful (35%; 6 of 17). During the holding period, mortality was 2 times higher and levels of Parvicapsula minibicornis(Kent, Whitaker and Dawe, 1997) infection were higher in the 18 8C-treated group than in the 10 8C-treated group. The only physiological dif- ference between treatments was a change in gill Na + ,K + -ATPase activity. This drop correlated negatively with travel times for the 18 8C-treated males. Reproductive-hormone levels and stress measures did not differ between treatments but showed significant correlations with individual travel times.

Developing a Mechanistic Understanding of Fish Migrations by Linking Telemetry with Physiology, Behavior, Genomics and Experimental Biology: An Interdisciplinary Case Study on Adult Fraser River Sockeye Salmon

Abstract Fish migration represents one of the most complex and intriguing biological phenomena in the animal kingdom. How do fish migrate such vast distances? What are the costs and benefits of migration? Some of these fundamental questions have been addressed through the use of telemetry. However, telemetry alone has not and will not yield a complete understanding of the migration biology of fish a or provide solutions to problems such as identifying physical barriers to migration or understanding potential impacts of climate change. Telemetry can be coupled with other tools and techniques to yield new insights into animal biology. Using Fraser River sockeye salmon (Oncorhynchus nerka) as a model, we summarize the advances that we have made in understanding salmonid migration biology through the integration of disciplines (i.e., interdisciplinary research) including physiology, behavior, functional genomics, and experimental biology. We also discuss opportunities for using large-scale telemetry arrays an...

Effect of water temperature, timing, physiological condition, and lake thermal refugia on migrating adult Weaver Creek sockeye salmon (Oncorhynchus nerka)

We coupled physiological biopsy and positional telemetry to examine survival to reach spawning grounds in re- lation to water temperature, timing, physiological condition, and holding location (river or lake) in adult migrating sockeye salmon (Oncorhynchus nerka). We tracked 83 fish across a large temperature range (13.5-21.5 8C), which included record highs. Only early-timed migrants that held in Harrison Lake survived to reach spawning grounds (16%, or n = 4). Normal- timed fish, those that migrated at historically observed times, survived at higher levels if they held in Harrison River (72%, or n = 18). Mortalities were identified on the bottoms of both the lake and river. Hypothetical degree-day (DD) ac- cumulation revealed that early-timed river fish would have greatly surpassed (~800 8C DD) a critical disease threshold value (~500 8C DD). There was no difference in hypothetical DD accumulation between normal-timed river fish and early- timed lake fish. Early-timed sockeye had elevated physiological stress (e.g., plasma lactate, glucose, and hematocrit), which may have contributed to high levels of mortality. By using lakes as thermal refugia, early-timed fish likely reduce rates of disease development and may better recover from physiological stress associated with high encountered tempera- tures.

Physiological Benefits of Being Small in a Changing World: Responses of Coho Salmon (Oncorhynchus kisutch) to an Acute Thermal Challenge and a Simulated Capture Event

Evidence is building to suggest that both chronic and acute warm temperature exposure, as well as other anthropogenic perturbations, may select for small adult fish within a species. To shed light on this phenomenon, we investigated physiological and anatomical attributes associated with size-specific responses to an acute thermal challenge and a fisheries capture simulation (exercise+air exposure) in maturing male coho salmon (Oncorhynchus kisutch). Full-size females were included for a sex-specific comparison. A size-specific response in haematology to an acute thermal challenge (from 7 to 20°C at 3°C h−1) was apparent only for plasma potassium, whereby full-size males exhibited a significant increase in comparison with smaller males (‘jacks’). Full-size females exhibited an elevated blood stress response in comparison with full-size males. Metabolic recovery following exhaustive exercise at 7°C was size-specific, with jacks regaining resting levels of metabolism at 9.3±0.5 h post-exercise in comparison with 12.3±0.4 h for full-size fish of both sexes. Excess post-exercise oxygen consumption scaled with body mass in male fish with an exponent of b = 1.20±0.08. Jacks appeared to regain osmoregulatory homeostasis faster than full-size males, and they had higher ventilation rates at 1 h post-exercise. Peak metabolic rate during post-exercise recovery scaled with body mass with an exponent of b∼1, suggesting that the slower metabolic recovery in large fish was not due to limitations in diffusive or convective oxygen transport, but that large fish simply accumulated a greater ‘oxygen debt’ that took longer to pay back at the size-independent peak metabolic rate of ∼6 mg min−1 kg−1. Post-exercise recovery of plasma testosterone was faster in jacks compared with full-size males, suggesting less impairment of the maturation trajectory of smaller fish. Supporting previous studies, these findings suggest that environmental change and non-lethal fisheries interactions have the potential to select for small individuals within fish populations over time.

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.

Routine and Active Metabolic Rates of Migrating Adult Wild Sockeye Salmon (Oncorhynchus nerka Walbaum) in Seawater and Freshwater

We present the first data on the differences in routine and active metabolic rates for sexually maturing migratory adult sockeye salmon (Oncorhynchus nerka) that were intercepted in the ocean and then held in either seawater or freshwater. Routine and active oxygen uptake rates (Mo2) were significantly higher (27%–72%) in seawater than in freshwater at all swimming speeds except those approaching critical swimming speed. During a 45‐min recovery period, the declining postexercise oxygen uptake remained 58%–73% higher in seawater than in freshwater. When fish performed a second swim test, active metabolic rates again remained 28%–81% higher for fish in seawater except at the critical swimming speed. Despite their differences in metabolic rates, fish in both seawater and freshwater could repeat the swim test and reach a similar maximum oxygen uptake and critical swimming speed as in the first swim test, even without restoring routine metabolic rate between swim tests. Thus, elevated Mo2 related to either being in seawater as opposed to freshwater or not being fully recovered from previous exhaustive exercise did not present itself as a metabolic loading that limited either critical swimming performance or maximum Mo2. The basis for the difference in metabolic rates of migratory sockeye salmon held in seawater and freshwater is uncertain, but it could include differences in states of nutrition, reproduction, and restlessness, as well as ionic differences. Regardless, this study elucidates some of the metabolic costs involved during the migration of adult salmon from seawater to freshwater, which may have applications for fisheries conservation and management models of energy use.

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.

Disentangling the roles of air exposure, gill net injury, and facilitated recovery on the postcapture and release mortality and behavior of adult migratory sockeye salmon (Oncorhynchus nerka) in freshwater.

We sought to improve the understanding of delayed mortality in migrating sockeye salmon (Oncorhynchus nerka) captured and released in freshwater fisheries. Using biotelemetry, blood physiology, and reflex assessments, we evaluated the relative roles of gill net injury and air exposure and investigated whether using a recovery box improved survival. Fish (), captured by beach seine, were allocated to four treatment groups: captured only, air exposed, injured, and injured and air exposed. Only half of the fish in each group were provided with a 15-min facilitated recovery. After treatment, fish were radio-tagged and released to resume their migration. Blood status was assessed in 36 additional untagged fish sampled after the four treatments. Compared with fish sampled immediately on capture, all treatments resulted in elevated plasma lactate and cortisol concentrations. After air exposure, plasma osmolality was elevated and reflexes were significantly impaired relative to the control and injured treatments. Injured fish exhibited reduced short-term migration speed by 3.2 km/d and had a 14.5% reduced survival to subnatal watersheds compared to controls. The 15-min facilitated recovery improved reflex assessment relative to fish released immediately but did not affect survival. We suggest that in sockeye salmon migrating in cool water temperatures (∼13°–16°C), delayed mortality can result from injury and air exposure, perhaps through sublethal stress, and that injury created additive delayed mortality likely via secondary infections.