Michael R. Donaldson

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...

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.

Conservation physiology in practice: how physiological knowledge has improved our ability to sustainably manage Pacific salmon during up-river migration.

Despite growing interest in conservation physiology, practical examples of how physiology has helped to understand or to solve conservation problems remain scarce. Over the past decade, an interdisciplinary research team has used a conservation physiology approach to address topical conservation concerns for Pacific salmon. Here, we review how novel applications of tools such as physiological telemetry, functional genomics and laboratory experiments on cardiorespiratory physiology have shed light on the effect of fisheries capture and release, disease and individual condition, and stock-specific consequences of warming river temperatures, respectively, and discuss how these findings have or have not benefited Pacific salmon management. Overall, physiological tools have provided remarkable insights into the effects of fisheries capture and have helped to enhance techniques for facilitating recovery from fisheries capture. Stock-specific cardiorespiratory thresholds for thermal tolerances have been identified for sockeye salmon and can be used by managers to better predict migration success, representing a rare example that links a physiological scope to fitness in the wild population. Functional genomics approaches have identified physiological signatures predictive of individual migration mortality. Although fisheries managers are primarily concerned with population-level processes, understanding the causes of en route mortality provides a mechanistic explanation and can be used to refine management models. We discuss the challenges that we have overcome, as well as those that we continue to face, in making conservation physiology relevant to managers of Pacific salmon.

Effects of post-capture ventilation assistance and elevated water temperature on sockeye salmon in a simulated capture-and-release experiment

The authors evaluated a method of assisting the ventilation of adult sockeye salmon in an attempt to enhance post-release survival after fisheries capture at moderate and peak water temperatures. Though comparable recovery methods are often used by recreational anglers, the authors found this to be ineffective in enhancing post-release survival.

Individual variation in migration speed of upriver-migrating sockeye salmon in the Fraser River in relation to their physiological and energetic status at marine approach.

Little research has examined individual variation in migration speeds of Pacific salmon (Oncorhynchus spp.) in natural river systems or attempted to link migratory behavior with physiological and energetic status on a large spatial scale in the wild. As a model, we used three stocks of summer‐run sockeye salmon (Oncorhynchus nerka) from the Fraser River watershed, British Columbia, to test the hypothesis that individual variation in migration speed is determined by a combination of environmental factors (i.e., water temperature), intrinsic biological differences (sex and population), and physiological and energetic condition. Before the freshwater portion of the migration, sockeye salmon (Quesnel, Chilcotin, and Nechako stock complexes) were captured in Johnstone Strait (∼215 km from river entry), gastrically implanted with radio transmitters, and sampled for blood, gill tissue, and energetic status before release. Analyses focused solely on individuals that successfully reached natal subwatersheds. Migration speeds were assessed by an extensive radiotelemetry array. Individuals from the stock complex that migrated the longest distance (Nechako) traveled at speeds slower than those of other stock complexes. Females traveled slower than males. An elevated energetic status of fish in the ocean was negatively correlated with migration speed in most river segments. During the transition from the ocean to the river, migration speed was negatively correlated with mean maximum water temperature; however, for the majority of river segments, it was positively correlated with migration speed. Physiological status measured in the ocean did not explain among‐individual variability in river migration speeds. Collectively, these findings suggest that there could be extensive variation in migration behavior among individuals, sexes, and populations and that physiological condition in the ocean explained little of this variation relative to in‐river environmental conditions and energetic status. Interestingly, individual fish generally retained their rank in swimming speed across different segments, except when transiting a challenging canyon midway during the migration.

Consequences of high temperatures and premature mortality on the transcriptome and blood physiology of wild adult sockeye salmon (Oncorhynchus nerka)

Elevated river water temperature in the Fraser River, British Columbia, Canada, has been associated with enhanced mortality of adult sockeye salmon (Oncorhynchus nerka) during their upriver migration to spawning grounds. We undertook a study to assess the effects of elevated water temperatures on the gill transcriptome and blood plasma variables in wild-caught sockeye salmon. Naturally migrating sockeye salmon returning to the Fraser River were collected and held at ecologically relevant temperatures of 14°C and 19°C for seven days, a period representing a significant portion of their upstream migration. After seven days, sockeye salmon held at 19°C stimulated heat shock response genes as well as many genes associated with an immune response when compared with fish held at 14°C. Additionally, fish at 19°C had elevated plasma chloride and lactate, suggestive of a disturbance in osmoregulatory homeostasis and a stress response detectable in the blood plasma. Fish that died prematurely over the course of the holding study were compared with time-matched surviving fish; the former fish were characterized by an upregulation of several transcription factors associated with apoptosis and downregulation of genes involved in immune function and antioxidant activity. Ornithine decarboxylase (ODC1) was the most significantly upregulated gene in dying salmon, which suggests an association with cellular apoptosis. We hypothesize that the observed decrease in plasma ions and increases in plasma cortisol that occur in dying fish may be linked to the increase in ODC1. By highlighting these underlying physiological mechanisms, this study enhances our understanding of the processes involved in premature mortality and temperature stress in Pacific salmon during migration to spawning grounds.

Physiology, Behavior, and Survival of Angled and Air-Exposed Largemouth Bass

Abstract Catch-and-release practices are common in recreational fisheries, yet little is known about the behavior, physiology, and ultimate fate of released fish. We used a combination of radiotelemetry (external attachment) and nonlethal blood sampling (i.e., the blood concentrations of lactate and glucose and plasma concentrations of aspartate aminotransferase (AST), Na+, K+, and Cl−) to assess the relationship between the prerelease physiological status and postrelease behavior and mortality of largemouth bass Micropterus salmoides. The experiments were conducted at two temperatures: approximately 15°C and 21°C. Immediately after capture by standard angling techniques, largemouth bass were exposed to air for 0 to 15 min to assess the consequences of air exposure at two moderate water temperatures. Fish exposed to air for long periods (approximately 10 min or more) had significantly higher concentrations of blood glucose 30 min after air exposure and took significantly longer to regain equilibrium than ...

Making connections in aquatic ecosystems with acoustic telemetry monitoring

Autonomous acoustic telemetry monitoring systems have been deployed in aquatic ecosystems around the globe – from under ice sheets in the Arctic to coral reefs in Australia – to track animals. With tens of thousands of tagged aquatic animals from a range of taxa, vast amounts of data have been generated. As data accumulate, it is useful to reflect on how this information has advanced our understanding of aquatic animals and improved management and conservation. Here we identify knowledge gaps and discuss opportunities to advance aquatic animal science and management using acoustic telemetry monitoring. Current technological and analytical shortfalls still need to be addressed to fully realize the potential of acoustic monitoring. Future interdisciplinary research that relies on transmitter-borne sensors and emphasizes hypothesis testing will amplify the benefits of this technology.

Physiological Responses of Free-Swimming Adult Coho Salmon to Simulated Predator and Fisheries Encounters

The responses of free-swimming adult coho salmon (Oncorhynchus kisutch) to simulated predator and fisheries encounters were assessed by monitoring heart rate (fH) with implanted data loggers and periodically taking caudal blood samples. A 10- or 30-min corralling treatment was conducted to simulate conspecifics being cornered by a predator or corralled by fisheries gear without physical contact. Corralling rapidly doubled fH from ∼31 beats min−1 to a maximum of ∼60 beats min−1, regardless of the duration of the corralling. However, recovery of fH to precorralling levels was significantly faster after the 10-min corralling (7.6 h) than after the 30-min corralling (11.5 h). An exhaustive-exercise treatment (chasing for 3 min, with physical contact) to simulate a predator chasing a fish to exhaustion or a fish becoming exhausted after encountering fisheries gear resulted in increased fH (to 60 beats min−1), plasma lactate, glucose, sodium, osmolality, and cortisol (males only) and a significant decrease in mean corpuscular hemoglobin concentration. Recovery of fH and most blood variables was complete about 16 h after exhaustive exercise and handling. The results illustrate a clear relationship between the intensity of exercise and the duration required for recovery of fH. Changes in fH were significantly correlated with those in plasma lactate, chloride, and sodium at 1 h after the exercise treatment protocols. Thus, measurements of fH may provide an accurate indication of the general physiological response of salmonids to exhaustive exercise in the natural environment.

Limited behavioural thermoregulation by adult upriver-migrating sockeye salmon (Oncorhynchus nerka) in the Lower Fraser River, British Columbia

The objective of this study was to combine radio telemetry with individual thermal loggers to assess the extent to which adult migrating sockeye salmon (Oncorhynchus nerka (Walbaum in Artedi, 1792)) behaviourally thermoregulate during their migration through the Fraser River mainstem, British Columbia. The Fraser mainstem represents a region of the migration route that contains some of the highest mean temperatures encountered by sockeye salmon during their life history. We found that throughout the study area, individual sockeye salmon body temperatures occasionally deviated from ambient temperatures (DT), yet individuals maintained a DT of -1 8C or cooler for only 5% of their migration through the study region. There were moderate mean deviations of DT in two segments that are known to contain thermally stratified waters. In one of the study segments with the greatest DT, mean body temperatures decreased as river temperatures in- creased and DT became increasingly positive with higher river discharge rates, but these relationships were not observed in any of the other study segments. No relationship existed between DT and migration rate. While periodic associations with cool water were evident, mean body temperatures were not significantly different than mean river temperatures throughout the lower Fraser mainstem. This finding raises further conservation concerns for vulnerable Fraser River sock- eye stocks that are predicted to encounter increasing peak summer river temperatures in the coming decades.