Female Pacific salmon often experience higher mortality than males during their once-in-a-lifetime up-river spawning migration, particularly when exposed to secondary stressors (e.g. high temperatures). However, the underlying mechanisms remain unknown. One hypothesis is that female Pacific salmon hearts are more oxygen-limited than males and are less able to supply oxygen to the body's tissues during this demanding migration. Notably, female hearts have higher coronary blood flow, which could indicate a greater reliance on this oxygen source. Oxygen limitations can develop from naturally occurring coronary blockages (i.e., coronary arteriosclerosis) found in mature salmon hearts. If female hearts rely more heavily on coronary blood flow but experience similar arteriosclerosis levels as males, they will have disproportionately impaired aerobic performance. To test this hypothesis, we measured resting (RMR) and maximum metabolic rate (MMR), aerobic scope (AS) and acute upper thermal tolerance in coho salmon (Oncorhynchus kisutch) with an intact or artificially blocked coronary oxygen supply. We also assessed venous blood oxygen and chemistry (cortisol, ions, and metabolite concentrations) at different time intervals during recovery from exhaustive exercise. We found that coronary blockage impaired MMR, AS, and the partial pressure of oxygen in venous blood (PvO2) during exercise recovery but did not differ between sexes. Coronary ligation lowered acute upper thermal tolerance by 1.1°C. Though we did not find evidence of enhanced female reliance on coronary supply, our findings highlight the importance of coronary blood supply for mature wild salmon, where migration success may be linked to cardiac performance, particularly during warm water conditions.
Passive integrated transponder (PIT) technology is a leading tool for tracking fish in freshwater systems. PIT is highly applicable for assessing fish passage at anthropogenic infrastructure (e.g., dams and floodgates); however, there are often complications in operating PIT antennas near these structures due to the ambient electromagnetic interference of metal and power-supply equipment. We designed a PIT antenna that is resistant to the effects of ambient electromagnetic interference (AEMI). This design uses lobes with balanced polarity within the antenna to neutralize AEMI within the vicinity of the antenna. This novel PIT antenna provides a more effective and cost-efficient option for researchers tracking fish in environments with high AEMI.
BACKGROUND: Ecological and physical conditions vary with depth in aquatic ecosystems, resulting in gradients of habitat suitability. Although variation in vertical distributions among individuals provides evidence of habitat selection, it has been challenging to disentangle how processes at multiple spatio-temporal scales shape behaviour. METHODS: We collected thousands of observations of depth from > 300 acoustically tagged adult Chinook salmon Oncorhynchus tshawytscha, spanning multiple seasons and years. We used these data to parameterize a machine-learning model to disentangle the influence of spatial, temporal, and dynamic oceanographic variables while accounting for differences in individual condition and maturation stage. RESULTS: The top performing machine learning model used bathymetric depth ratio (i.e., individual depth relative to seafloor depth) as a response. We found that bathymetry, season, maturation stage, and spatial location most strongly influenced Chinook salmon depth. Chinook salmon bathymetric depth ratios were deepest in shallow water, during winter, and for immature individuals. We also identified non-linear interactions among covariates, resulting in spatially-varying effects of zooplankton concentration, lunar cycle, temperature and oxygen concentration. CONCLUSIONS: Our results suggest Chinook salmon vertical habitat use is a function of ecological interactions, not physiological constraints. Temporal and spatial variation in depth distributions could be used to guide management decisions intended to reduce fishery impacts on Chinook salmon. More generally, our findings demonstrate how complex interactions among bathymetry, seasonality, location, and life history stage regulate vertical habitat selection.
Understanding the adaptive potential of populations and species is pivotal for minimizing the loss of biodiversity in this era of rapid climate change. Adaptive potential has been estimated in various ways, including based on levels of standing genetic variation, presence of potentially beneficial alleles, and/or the severity of environmental change. Kokanee salmon, the non-migratory ecotype of sockeye salmon (Oncorhynchus nerka), is culturally and economically important and has already been impacted by the effects of climate change. To assess its climate vulnerability moving forward, we integrated analyses of standing genetic variation, genotype-environment associations, and climate modeling based on sequence and structural genomic variation from 224 whole genomes sampled from 22 lakes in British Columbia and Yukon (Canada). We found that variables for extreme temperatures, particularly warmer temperatures, had the most pervasive signature of selection in the genome and were the strongest predictors of levels of standing variation and of putatively adaptive genomic variation, both sequence and structural. Genomic offset estimates, a measure of climate vulnerability, were significantly correlated with higher increases in extreme warm temperatures, further highlighting the risk of summer heat waves that are predicted to increase in frequency in the future. Levels of standing genetic variation, an important metric for population viability and resilience, were not correlated with genomic offset. Nonetheless, our combined approach highlights the importance of integrating different sources of information and genomic data to formulate more comprehensive and accurate predictions on the vulnerability of populations and species to future climate change.
Stream temperatures are influenced by the amount of solar insolation they receive. Increasing stream temperatures associated with climate warming pose detrimental health risks to freshwater ecosystems. In British Columbia (BC), Canada, timber harvesting along forested streams is managed using riparian buffer zones of varying widths and designations. Within buffer zones, depending on distance from the stream, selective thinning may be permitted or harvest may be forbidden. In this study, we used airborne laser scanning (ALS) point cloud data acquired via a remotely piloted aircraft system (RPAS) to derive forest canopy characteristics that were then used to estimate daily incoming summer and fall solar insolation for five stream reaches in coastal conifer-dominated temperate forests in Vancouver Island, BC, Canada. We then examined empirical relationships between estimated insolation and actual instream temperature measurements. Based on these empirical relationships, the potential effects of timber harvest on instream temperatures were simulated by comparing scenarios of different riparian forest harvest intensities. Our results indicated that modeled solar insolation explained 43-90 % of the variation in observed stream reach temperatures, and furthermore, when a single cold-water stream reach was excluded explained an overall 81 % of variation. Simulated harvesting scenarios generally projected increases in maximum stream reach temperatures 1-2 °C in summer and early fall months. However, in a full clearcut scenario (i.e. where all trees were removed), maximum stream reach temperatures increased as much as 5.8 °C. Our results emphasize the importance of retaining riparian vegetation for the maintenance of habitable temperatures for freshwater-reliant fish with thermal restrictions. In addition, we demonstrate the feasibility of RPAS-based monitoring of stream reach shading and canopy cover, enabling detailed assessment of environmental stressors faced by fish populations under climate warming.
Climatic warming elevates mortality for many salmonid populations during their physically challenging up-river spawning migrations, yet, the mechanisms underlying the increased mortality remain elusive. One hypothesis posits that a cardiac oxygen insufficiency impairs the heart's capacity to pump sufficient oxygen to body tissues to sustain up-river swimming, especially in warm water when oxygen availability declines and cardiac and whole-animal oxygen demand increases. We tested this hypothesis by measuring cardiac and metabolic (cardiorespiratory) performance, and assessing the upper thermal tolerance of coho salmon (Oncorhynchus kisutch) during sustained swimming and acute warming. By surgically ligating the coronary artery, which naturally accumulates arteriosclerotic lesions in migrating salmon, we partially impaired oxygen supply to the heart. Coronary ligation caused drastic cardiac impairment during swimming, even at benign temperatures, and substantially constrained cardiorespiratory performance during swimming and progressive warming compared to sham-operated control fish. Furthermore, upper thermal tolerance during swimming was markedly reduced (by 4.4 °C) following ligation. While the cardiorespiratory capacity of female salmon was generally lower at higher temperatures compared to males, upper thermal tolerance during swimming was similar between sexes within treatment groups. Cardiac oxygen supply is a crucial determinant for the migratory capacity of salmon facing climatic environmental warming.
Oncorhynchus kisutch , Animals , Male , Female , Swimming , Oxygen Consumption , Temperature , Salmon , Oxygen
The early marine life of Pacific salmon is believed to be a critical period limiting population-level survival. Recent evidence suggests that some infectious agents are associated with survival but linkages with underlying physiological mechanisms are lacking. While challenge studies can demonstrate cause and effect relationships between infection and pathological change or mortality, in some cases pathological change may only manifest in the presence of environmental stressors; thus, it is important to gain context from field observations. Herein, we examined physiological correlates with infectious agent loads in Chinook salmon during their first ocean year. We measured physiology at the molecular (gene expression), metabolic (plasma chemistry) and cellular (histopathology) levels. Of 46 assayed infectious agents, 27 were detected, including viruses, bacteria and parasites. This exploratory study identified.a strong molecular response to viral disease and pathological change consistent with jaundice/anemia associated with Piscine orthoreovirus,strong molecular signals of gill inflammation and immune response associated with gill agents `Candidatus Branchiomonas cysticola' and Parvicapsula pseudobranchicola,a general downregulation of gill immune response associated with Parvicapsula minibicornis complementary to that of P. pseudobranchicola.Importantly, our study provides the first evidence that the molecular activation of viral disease response and the lesions observed during the development of the PRV-related disease jaundice/anemia in farmed Chinook salmon are also observed in wild juvenile Chinook salmon.
Climate change is causing large declines in many Pacific salmon populations. In particular, warm rivers are associated with high levels of premature mortality in migrating adults. The Fraser River watershed in British Columbia, Canada, supports some of the largest Chinook salmon (Oncorhynchus tshawytscha) runs in the world. However, the Fraser River is warming at a rate that threatens these populations at critical freshwater life stages. A growing body of literature suggests salmonids are locally adapted to their thermal migratory experience, and thus, population-specific thermal performance information can aid in management decisions. We compared the thermal performance of pre-spawning adult Chinook salmon from two populations, a coastal fall-run from the Chilliwack River (125 km cooler migration) and an interior summer-run from the Shuswap River (565 km warmer migration). We acutely exposed fish to temperatures reflecting current (12°C, 18°C) and future projected temperatures (21°C, 24°C) in the Fraser River and assessed survival, aerobic capacity (resting and maximum metabolic rates, absolute aerobic scope (AAS), muscle and ventricle citrate synthase), anaerobic capacity (muscle and ventricle lactate dehydrogenase) and recovery capacity (post-exercise metabolism, blood physiology, tissue lactate). Chilliwack Chinook salmon performed worse at high temperatures, indicated by elevated mortality, reduced breadth in AAS, enhanced plasma lactate and potassium levels and elevated tissue lactate concentrations compared with Shuswap Chinook salmon. At water temperatures exceeding the upper pejus temperatures (Tpejus, defined here as 80% of maximum AAS) of Chilliwack (18.7°C) and Shuswap (20.2°C) Chinook salmon populations, physiological performance will decline and affect migration and survival to spawn. Our results reveal population differences in pre-spawning Chinook salmon performance across scales of biological organization at ecologically relevant temperatures. Given the rapid warming of rivers, we show that it is critical to consider the intra-specific variation in thermal physiology to assist in the conservation and management of Pacific salmon.
Metabolic scope represents the aerobic energy budget available to an organism to perform non-maintenance activities (e.g., escape a predator, recover from a fisheries interaction, compete for a mate). Conflicting energetic requirements can give rise to ecologically relevant metabolic trade-offs when energy budgeting is constrained. The objective of this study was to investigate how aerobic energy is utilized when individual sockeye salmon (Oncorhynchus nerka) are exposed to multiple acute stressors. To indirectly assess metabolic changes in free-swimming individuals, salmon were implanted with heart rate biologgers. The animals were then exercised to exhaustion or briefly handled as a control, and allowed to recover from this stressor for 48 h. During the first 2 h of the recovery period, individual salmon were exposed to 90 ml of conspecific alarm cues or water as a control. Heart rate was recorded throughout the recovery period. Recovery effort and time was higher in exercised fish, relative to control fish, whereas exposure to an alarm cue had no effect on either of these metrics. Individual routine heart rate was negatively correlated with recovery time and effort. Together, these findings suggest that metabolic energy allocation towards exercise recovery (i.e., an acute stressor; handling, chase, etc.) trumps anti-predator responses in salmon, although individual variation may mediate this effect at the population level.
Animal Migration , Salmon , Animals , Salmon/physiology , Animal Migration/physiology , Fishes , Swimming/physiology , Oxygen Consumption/physiology
Although infectious agents can act as strong population regulators, knowledge of their spatial distributions in wild Pacific salmon is limited, especially in the marine environment. Characterizing pathogen distributions during early marine residence, a period considered a survival bottleneck for Pacific salmon, may reveal where salmon populations are exposed to potentially detrimental pathogens. Using high-throughput qPCR, we determined the prevalence of 56 infectious agents in 5719 Chinook, 2032 Coho and 4062 Sockeye salmon, sampled between 2008 and 2018, in their first year of marine residence along coastal Western Canada. We identified high prevalence clusters, which often shifted geographically with season, for most of the 41 detected agents. A high density of infection clusters was found in the Salish Sea along the east coast of Vancouver Island, an important migration route and residence area for many salmon populations, some experiencing chronically poor marine survival. Maps for each infectious agent taxa showing clusters across all host species are provided. Our novel documentation of salmon pathogen distributions in the marine environment contributes to the ecological knowledge regarding some lesser known pathogens, identifies salmon populations potentially impacted by specific pathogens, and pinpoints priority locations for future research and remediation.
Oncorhynchus , Animals , British Columbia/epidemiology , Salmon
Incorporating host-pathogen(s)-environment axes into management and conservation planning is critical to preserving species in a warming climate. However, the role pathogens play in host stress resilience remains largely unexplored in wild animal populations. We experimentally characterized how independent and cumulative stressors (fisheries handling, high water temperature) and natural infections affected the health and longevity of released wild adult sockeye salmon (Oncorhynchus nerka) in British Columbia, Canada. Returning adults were collected before and after entering the Fraser River, yielding marine- and river-collected groups, respectively (N = 185). Fish were exposed to a mild (seine) or severe (gill net) fishery treatment at collection, and then held in flow-through freshwater tanks for up to four weeks at historical (14°C) or projected migration temperatures (18°C). Using weekly nonlethal gill biopsies and high-throughput qPCR, we quantified loads of up to 46 pathogens with host stress and immune gene expression. Marine-collected fish had less severe infections than river-collected fish, a short migration distance (100 km, 5-7 days) that produced profound infection differences. At 14°C, river-collected fish survived 1-2 weeks less than marine-collected fish. All fish held at 18°C died within 4 weeks unless they experienced minimal handling. Gene expression correlated with infections in river-collected fish, while marine-collected fish were more stressor-responsive. Cumulative stressors were detrimental regardless of infections or collection location, probably due to extreme physiological disturbance. Because river-derived infections correlated with single stressor responses, river entry probably decreases stressor resilience of adult salmon by altering both physiology and pathogen burdens, which redirect host responses toward disease resistance.
Fisheries , Salmon , Animal Migration , Animals , British Columbia , Gene-Environment Interaction , Salmon/genetics
Predation risk for animal migrants can be impacted by physical condition. Although size- or condition-based selection is often observed, observing infection-based predation is rare due to the difficulties in assessing infectious agents in predated samples. We examined predation of outmigrating sockeye salmon (Oncorhynchus nerka) smolts by bull trout (Salvelinus confluentus) in south-central British Columbia, Canada. We used a high-throughput quantitative polymerase chain reaction (qPCR) platform to screen for the presence of 17 infectious agents found in salmon and assess 14 host genes associated with viral responses. In one (2014) of the two years assessed (2014 and 2015), the presence of infectious haematopoietic necrosis virus (IHNv) resulted in 15-26 times greater chance of predation; in 2015 IHNv was absent among all samples, predated or not. Thus, we provide further evidence that infection can impact predation risk in migrants. Some smolts with high IHNv loads also exhibited gene expression profiles consistent with a virus-induced disease state. Nine other infectious agents were observed between the two years, none of which were associated with increased selection by bull trout. In 2014, richness of infectious agents was also associated with greater predation risk. This is a rare demonstration of predator consumption resulting in selection for prey that carry infectious agents. The mechanism by which this selection occurs is not yet determined. By culling infectious agents from migrant populations, fish predators could provide an ecological benefit to prey.
Both laboratory and field respirometry are rapidly growing techniques to determine animal performance thresholds. However, replicating protocols to estimate maximum metabolic rate (MMR) between species, populations, and individuals can be difficult, especially in the field. We therefore evaluated seven different exercise treatments-four laboratory methods involving a swim tunnel (critical swim speed [Ucrit], Ucrit postswim fatigue, maximum swim speed [Umax], and Umax postswim fatigue) and three field-based chasing methods (3-min chase with 1-min air exposure, 3-min chase with no air exposure, and chase to exhaustion)-in adult coho salmon (Oncorhynchus kisutch) as a case study to determine best general practices for measuring and quantifying MMR in fish. We found that all seven methods were highly comparable and that chase treatments represent a valuable field alternative to swim tunnels. Moreover, we caution that the type of test and duration of measurement windows used to calculate MMR can have significant effects on estimates of MMR and statistical power for each approach.
Oncorhynchus kisutch , Oxygen Consumption , Animals , Fishes , Swimming , Fatigue
[This corrects the article DOI: 10.1093/conphys/coz095.].
Co-management is widely seen as a way of improving environmental governance and empowering communities. When successful, co-management enhances the validity and legitimacy of decision-making, while providing stakeholders with influence over processes and outcomes that directly impact them. However, our research with participants in co-management across several cases leads us to argue that many of the individuals who contribute to co-management are subject to significant personal stress arising from both the logistical and social/emotional demands of participation in these processes. We argue that the literature on co-management has touched on this only indirectly, and that personal stress is a major challenge for participants that ought to be integrated into research agendas and addressed by policy-makers. In this article, we review the contours of the personal stress issue as it has appeared in our observations of co-management events and interviews with participants. While these findings are partial and preliminary, we argue that personal stress has theoretical and practical significance to the broader literature and process design. We conclude the article with recommendations for participants, researchers and policy-makers about how to consider and respond to problems of personal stress.
Conservation of Natural Resources , Environmental Policy , Decision Making , Humans , Referral and Consultation
White sturgeon are the largest freshwater fish in North America and are the focus of an intense catch-and-release (C&R) fishery; the effects are largely unknown. We assessed the effect of fight and handling time, water temperature, river discharge rate, and fish size on physiological and reflex impairment responses of wild white sturgeon to angling. Sixty of these fish were tagged with acoustic transmitters to assess survival and post-release behaviour. Survival was high (100%). Water temperature and discharge influenced post-capture blood physiology. Specifically, lactate, chloride, and cortisol concentrations were elevated in individuals fought longer, and captured at higher water temperatures and river discharge. Cortisol was affected by fish size, with lower concentrations found in larger individuals. Only lactate and chloride were positively related to reflex impairment scores. Post-release movements were correlated with physiological state, fight characteristics and the environment. Specifically, higher blood lactate and chloride and those with longer fight times moved shorter distances after release. Contrastingly, higher levels of circulating glucose and potassium, as well as larger fish captured during periods of high discharge moved longer distances. Sturgeon tended to move shorter distances and at slower rates when reflex impairment was high, although reflex impairment in general did not explain a significant proportion of the variance in any movement metric. Our results show intriguing variance in the physiological and behavioural response of individual white sturgeon to C&R angling, with some degree of environmental dependence, and highlights the importance of understanding drivers of such variation when managing fisheries.
Behavior, Animal , Fisheries/standards , Fishes/physiology , Hydrocortisone/metabolism , Mortality/trends , Reflex/physiology , Stress, Physiological , Animals , Human Activities , Humans , Rivers , Temperature , Water Pollutants, Chemical/toxicity
Pacific salmon routinely encounter stressors during their upriver spawning migration, which have the potential to influence offspring through hormonally-mediated maternal effects. To disentangle genetic vs. hormonal effects on offspring swimming performance, we collected gametes from three species of Pacific salmon (Chinook, pink and sockeye) at the end of migration and exposed a subset of eggs from each female to cortisol baths to simulate high levels of maternal stress. Fertilised eggs were reared to fry and put through a series of aerobic swim trials. Results show that exposure to cortisol early in development reduces maximum oxygen consumption while swimming, and decreases aerobic scope in all three species. Resting oxygen consumption did not differ between cortisol and control treatment groups. We also examined several metrics that could influence aerobic performance, and found no differences between treatment groups in haematocrit%, haemoglobin concentration, heart mass, citrate synthase activity or lactate dehydrogenase activity. Though it was not the focus of this study, an interesting discovery was that pink salmon had a higher MO2max and aerobic scope relative to the other species, which was supported by a greater haematocrit, haemoglobin, a larger heart and higher CS activity. Some management and conservation practices for Pacific salmon focus efforts primarily on facilitating adult spawning. However, if deleterious effects of maternal stress acquired prior to spawning persist into the next generation, consideration will need to be given to sub-lethal effects that could be imparted onto offspring from maternal stress.
Early marine survival of juvenile salmon is intimately associated with their physiological condition during smoltification and ocean entry. Smoltification (parr-smolt transformation) is a developmental process that allows salmon to acquire seawater tolerance in preparation for marine living. Traditionally, this developmental process has been monitored using gill Na+/K+-ATPase (NKA) activity or plasma hormones, but gill gene expression offers the possibility of another method. Here, we describe the discovery of candidate genes from gill tissue for staging smoltification using comparisons of microarray studies with particular focus on the commonalities between anadromous Rainbow trout and Sockeye salmon datasets, as well as a literature comparison encompassing more species. A subset of 37 candidate genes mainly from the microarray analyses was used for TaqMan quantitative PCR assay design and their expression patterns were validated using gill samples from four groups, representing three species and two ecotypes: Coho salmon, Sockeye salmon, stream-type Chinook salmon and ocean-type Chinook salmon. The best smoltification biomarkers, as measured by consistent changes across these four groups, were genes involved in ion regulation, oxygen transport and immunity. Smoltification gene expression patterns (using the top 10 biomarkers) were confirmed by significant correlations with NKA activity and were associated with changes in body brightness, caudal fin darkness and caudal peduncle length. We incorporate gene expression patterns of pre-smolt, smolt and de-smolt trials from acute seawater transfers from a companion study to develop a preliminary seawater tolerance classification model for ocean-type Chinook salmon. This work demonstrates the potential of gene expression biomarkers to stage smoltification and classify juveniles as pre-smolt, smolt or de-smolt.
An organism's ability to respond effectively to environmental change is critical to its survival. Yet, life stage and overall condition can dictate tolerance thresholds to heightened environmental stressors, such that stress may not be equally felt across individuals and at all times. Also, the transcriptional responses induced by environmental changes can reflect both generalized responses as well as others that are highly specific to the type of change being experienced. Thus, if transcriptional biomarkers specific to a stressor, even under multi-stressor conditions, can be identified, the biomarkers could then be applied in natural environments to determine when and where an individual experiences such a stressor. Here, we experimentally challenged juvenile Chinook salmon (Oncorhynchus tshawytscha) to validate candidate gill gene expression biomarkers. A sophisticated experimental design manipulated salinity (freshwater, brackish water and seawater), temperature (10, 14 and 18°C) and dissolved oxygen (normoxia and hypoxia) in all 18 possible combinations for 6 days using separate trials for three smolt statuses (pre-smolt, smolt and de-smolt). In addition, changes in juvenile behaviour, plasma variables, gill Na+/K+-ATPase activity, body size, body morphology and skin pigmentation supplemented the gene expression responses. We identified biomarkers specific to salinity and temperature that transcended the multiple stressors, smolt status and mortality (live, dead and moribund). Similar biomarkers for dissolved oxygen were not identified. This work demonstrates the unique power of gene expression biomarkers to identify a specific stressor even under multi-stressor conditions, and we discuss our next steps for hypoxia biomarkers using an RNA-seq study.
Gene Expression/physiology , Genetic Markers/physiology , Salinity , Salmon/physiology , Temperature , Animals , Life History Traits , Oxygen/chemistry , Oxygen/metabolism , Salmon/genetics
Fish vitality can be measured by classifying reflex impairments (i.e., a visual impression of the ability to respond to induced stimuli) and visible injuries. These metrics can predict survival probability following release from fisheries, and monitoring physiological disturbances following capture can help understand mechanisms of mortality. To test the hypothesis that severity of injury and reflex impairment influences the time course of physiological recovery, coho salmon (Oncorhynchus kisutch) were held for up to 84-h following capture by purse seine. We classified reflex impairments and visible dermal injuries, and through repeated blood sampling, assessed metrics indicative of stress, exhaustion, and osmoregulatory disturbances. Reflex-impairments and blood lactate levels suggested fish were exhausted upon capture but recovered after 48â¯h. Conversely, fish with dermal injuries showed disruptions to ion homeostasis that were greater in more severely injured fish and increased over time. While reflex impairments may predict short term post-release mortality, the prolonged physiological disturbances caused by dermal injuries are likely to be responsible for delayed mortality; our results suggest that disruptions to ion homeostasis is a possible mechanism of post-release mortality.
Oncorhynchus kisutch/physiology , Skin/injuries , Animals , Conservation of Natural Resources , Homeostasis , Lactic Acid/blood , Reflex , Stress, Physiological
