Glenn Terrence Crossin

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.

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...

MECHANISTIC BASIS OF INDIVIDUAL MORTALITY IN PACIFIC SALMON DURING SPAWNING MIGRATIONS

Reproductive-based migration is a challenging period for many animals, but particularly for Pacific salmonids, which must navigate from the high seas to freshwater natal streams. For the first time, we attempt to answer the question as to why some migratory adult Pacific salmon die en route to spawning grounds. Summer-run sockeye salmon (Oncorhynchus nerka) were used as a model, and the migration behavior of 301 fish was followed by intercepting them in the ocean about 215 km from the mouth of the Fraser River, British Columbia, Canada, and implanting a gastric radio transmitter. Before release, telemetered fish were also bio-sampled, which included drawing a blood sample, collecting a gill biopsy, and quantifying energetic status with a microwave energy meter. We tested the predictions that the fish that died prematurely would be characterized by low energy reserves, advanced reproductive development, elevated indicators of stress, and low osmoregulatory preparedness compared with fish that completed their river migration. Just over half (52.3%) of the sockeye tagged were subsequently detected in the Fraser River. Salmon that failed to enter the river had exhibited indicators of stress (e.g., elevated plasma lactate, glucose, and cortisol). Contrary to our prediction, fish that failed to enter the river tended to have higher gross somatic energy and be larger at the time of sampling in the ocean than fish that successfully entered the river. Of the fish that were detected in the river (i.e., 134 fish excluding fishery removals), 9.7% did not migrate beyond the lower reaches (approximately 250 km from ocean), and a further 14.2% reached the upper reaches but failed to reach natal sub-watersheds, whereas the remainder (76.1%) reached natal sub-watersheds. Of these, fish unsuccessful in the lower reaches tended to have a high plasma osmolality in the ocean, whereas fish failing in the upper reaches had lower levels of reproductive hormones in the ocean.

A Nonlethal, Rapid Method for Assessing the Somatic Energy Content of Migrating Adult Pacific Salmon

Abstract Traditional methods for determining the energy content of fish involve either chemical assays of lipid and protein levels (proximate analyses) or tissue combustion (bomb calorimetry). In studies of migrating Pacific salmon Oncorhynchus spp., entire fish need to be homogenized prior to analysis, as energy reserves are stored along a head-to-tail gradient and change along this gradient depending on the stage of upriver migration. The logistics and costs associated with transporting carcasses to the laboratory can be prohibitive. Also, many populations of Pacific salmon are at risk of extinction, so lethal sampling is often not an option. Few reliable and practical methods exist that enable rapid and nonlethal energy determinations of large fish in the field. We evaluated a handheld microwave energy meter as a means of estimating whole-body energy concentrations. In 2002 and 2003, we collected sockeye salmon O. nerka from several stocks during their coastal and upriver migration through the Fraser R...

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.

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.

Mechanisms Influencing the Timing and Success of Reproductive Migration in a Capital Breeding Semelparous Fish Species, the Sockeye Salmon

Two populations of homing sockeye salmon (Oncorhynchus nerka; Adams and Chilko) were intercepted in the marine approaches around the northern and southern ends of Vancouver Island (British Columbia, Canada) en route to a natal river. More than 500 salmon were nonlethally biopsied for blood plasma, gill filament tips, and gross somatic energy (GSE) and were released with either acoustic or radio transmitters. At the time of capture, GSE, body length, and circulating testosterone ([T]) differed between populations, differences that reflected known life‐history variations. Within‐population analyses showed that in Adams sockeye salmon, plasma glucose ([glu]), lactate ([lactate]), and ion concentrations were higher in the northern approach than in the southern approach, suggesting that the former was more stressful. GSE, [T], and gill Na+,K+‐ATPase activities also differed between the two locales, and each varied significantly with Julian date, suggesting seasonality. Despite these relative geographic differences, the timing of river entry and the ability to reach spawning areas were strongly correlated with energetic, reproductive, and osmoregulatory state. Salmon that delayed river entry and reached spawning areas had relatively high GSE and low [T] and gill ATPase. In contrast, salmon that entered the river directly but that ultimately failed to reach spawning areas had lower GSE and higher [T] and gill ATPase, and they also swam at significantly faster rates (failed fish ∼20.0 km d−1 vs. successful fish ∼15.5 km d−1). Physiologically, salmon that did not enter the river at all but that presumably died in the marine environment exhibited high stress (plasma [glu] and [lactate]) and ionoregulatory measures (plasma [Na+], [Cl−], osmolality).

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.

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.