The role of spatial structure in at-risk metapopulation recoveries.

Metapopulations are often managed as a single contiguous population despite the spatial structure underlying their local and regional dynamics. Disturbances from human activities can also be spatially structured with mortality impacts concentrated to just a few local populations among the aggregate. Scale transitions between local and regional processes can generate emergent properties whereby the whole system can fail to recover as quickly as expected for an equivalent single population. Here, we draw on theory and empirical case studies to ask: what is the consequence of spatially structured ecological and disturbance processes on metapopulation recoveries? We suggest that exploring this question could help address knowledge gaps for managing metapopulations including: Why do some metapopulations recover quickly while others remain collapsed? And, what risks are unaccounted for when metapopulations are managed at aggregate scales? First, we used model simulations to examine how scale transitions among ecological and disturbance conditions interact to generate emergent metapopulation recovery outcomes. In general, we found that the spatial structure of disturbance was a strong determinant of recovery outcomes. Specifically, disturbances that unevenly impacted local populations consistently generated the slowest recoveries and highest conservation risks. Ecological conditions that dampened metapopulation recoveries included low dispersal, variable local demography, sparsely connected habitat networks, and spatially and temporally correlated stochastic processes. Second, we illustrate the unexpected challenges of managing metapopulations by examining the recoveries of three USA federally listed endangered species: Florida Everglade snail kites, California and Alaska sea otters, and Snake River Chinook salmon. Overall, our results show the pivotal role of spatial structure in metapopulation recoveries whereby the interplay between local and regional processes shapes the resilience of the whole system. With this understanding, we provide guidelines for resource managers tasked with conserving and managing metapopulations and identify opportunities for research to support the application of metapopulation theory to real-world challenges.

Changing estuaries and impacts on juvenile salmon: A systematic review.

Estuaries are productive ecosystems providing important habitat for a diversity of species, yet they also experience intense levels of anthropogenic development. To inform decision-making, it is essential to understand the pathways of impacts of particular human activities, especially those that affect species such as salmon, which have high ecological, social-cultural and economic values. Salmon systems provide an opportunity to build from the substantial body of research on responses to estuary developments and take stock of what is known. We conducted a systematic English-language literature review on the responses of juvenile salmon to anthropogenic activities in estuaries and nearshore areas asking: what has been studied, where are the major knowledge gaps and how do stressors affect salmon? We found a substantial body of research (n = 167 studies; 1,369 comparative tests) to help understand responses of juvenile salmon to 24 activities and their 14 stressors. Across studies, 82% of the research was conducted in the eastern Pacific (Oregon and Washington, USA and British Columbia, Canada) showing a limited geographical scope. Using a semiquantitative approach to summarize the literature, including a weight-of-evidence metric, we found a range of results from low to moderate-high confidence in the consequences of the stressors. For example, we found moderate-high confidence in the negative impacts of pollutants and sea lice and moderate confidence in negative impacts from connectivity loss and changes in flow. Our results suggest that overall, multiple anthropogenic activities cause negative impacts across ecological scales. However, our results also reveal knowledge gaps resulting from minimal research on particular species (e.g. sockeye salmon), regions (e.g. Atlantic) or stressors (e.g. entrainment) that would be expedient areas for future research. With estuaries acting as a nexus of biological and societal importance and hotspots of ongoing development, the insights gained here can contribute to informed decision-making.

Examining the relationships between egg cortisol and oxidative stress in developing wild sockeye salmon (Oncorhynchus nerka).

Maternally-derived hormones in oocytes, such as glucocorticoids (GCs), play a crucial role in embryo development in oviparous taxa. In fishes, maternal stressor exposure increases circulating and egg cortisol levels, the primary GC in fishes, as well as induces oxidative stress. Elevated egg cortisol levels modify offspring traits but whether maternal oxidative stress correlates with circulating and egg cortisol levels, and whether maternal/egg cortisol levels correlate with offspring oxidative stress have yet to be determined. The objective of this study was to examine the relationships among maternal and egg cortisol, and maternal and offspring oxidative stress to provide insight into the potential intergenerational effects of stressor exposure in sockeye salmon (Oncorhynchus nerka). Antioxidant concentration and oxidative stress were measured in maternal tissues (plasma, brain, heart and liver) as well as offspring developmental stages (pre-fertilization, 24h post-fertilization, eyed, and hatch), and were compared to both naturally-occurring and experimentally-elevated (via cortisol egg bath) levels of cortisol in eggs. Oxygen radical absorptive capacity of tissues from maternal sockeye salmon was measured spectrophotometrically and was not correlated with maternal or egg cortisol concentrations. Also, naturally-occurring and experimentally-elevated cortisol levels in eggs (to mimic maternal stress) did not affect oxidative stress or antioxidant capacity of the offspring. We conclude that the metrics of maternal stress examined in sockeye salmon (i.e., maternal/egg cortisol, maternal oxidative stress) are independent of each other, and that egg cortisol content does not influence offspring oxidative stress.

Is winter worse for stressed fish? The consequences of exogenous cortisol manipulation on over-winter survival and condition of juvenile largemouth bass.

Over-winter mortality is an important selective force for warm-water fish (e.g., centrarchids) that live in temperate habitats. Inherent challenges faced by fish during winter may be compounded by additional stressors that activate the hypothalamic-pituitary-interrenal axis, either before or during winter, leading to negative sub-lethal impacts on fish health and condition, and possibly reducing chance of survival. We used experimental cortisol manipulation to test the hypothesis that juvenile largemouth bass (Micropterus salmoides) exposed to semi-chronic elevation in cortisol prior to winter would experience higher levels of over-winter mortality, physiological alterations and impaired immune status relative to control and sham-treated bass. Over-winter survival in experimental ponds was high, averaging 83%, and did not differ among treatment groups. Over the study period, bass exhibited an average increase in mass of 19.4%, as well as a slight increase in Fulton's condition factor, but neither measure differed among groups. Hepatosomatic index in cortisol-treated bass was 23% lower than in control fish, suggesting lower energy status, but white muscle lipid content was similar across all groups. Lastly, there was no difference in spleen somatic index or parasite load among treatment groups, indicating no long-term immune impairment related to our cortisol manipulation. The current study adds to a growing body of literature on glucocorticoid manipulations where field-based findings are not consistent with laboratory-based conceptual understanding of multiple stressors. This suggests that field conditions may provide fish with opportunities to mitigate negative effects of some stressors.

Are there intergenerational and population-specific effects of oxidative stress in sockeye salmon (Oncorhynchus nerka)?

Intergenerational effects of stress have been reported in a wide range of taxa; however, few researchers have examined the intergenerational consequences of oxidative stress. Oxidative stress occurs in living organisms when reactive oxygen species remain unquenched by antioxidant defense systems and become detrimental to cells. In fish, it is unknown how maternal oxidative stress and antioxidant capacity influence offspring quality. The semelparous, migratory life history of Pacific salmon (Oncorhynchus spp.) provides a unique opportunity to explore intergenerational effects of oxidative stress. This study examined the effects of population origin on maternal and developing offspring oxidative stress and antioxidant capacity, and elucidated intergenerational relationships among populations of sockeye salmon (Oncorhynchus nerka) with varying migration effort. For three geographically distinct populations of Fraser River sockeye salmon (British Columbia, Canada), antioxidant capacity and oxidative stress were measured in adult female plasma, heart, brain, and liver, as well as in developing offspring until time of emergence. Maternal and offspring oxidative stress and antioxidant capacity varied among populations but patterns were not consistent across tissue/developmental stage. Furthermore, maternal oxidative stress and antioxidant capacity did not affect offspring oxidative stress and antioxidant capacity across any of the developmental stages or populations sampled. Our results revealed that offspring develop their endogenous antioxidant systems at varying rates across populations; however, this variability is overcome by the time of emergence. While offspring may be relying on maternally derived antioxidants in the initial stages of development, they rapidly develop their own antioxidant systems (mainly glutathione) during later stages of development.

Physiological condition infers habitat choice in juvenile sockeye salmon.

The amount of time that juvenile salmon remain in an estuary varies among and within populations, with some individuals passing through their estuary in hours while others remain in the estuary for several months. Underlying differences in individual physiological condition, such as body size, stored energy and osmoregulatory function, could drive individual variation in the selection of estuary habitat. Here we investigated the role of variation in physiological condition on the selection of estuarine and ocean habitat by sockeye salmon (Oncorhynchus nerka) smolts intercepted at the initiation of their 650-km downstream migration from Chilko Lake, Fraser River, British Columbia (BC). Behavioural salinity preference experiments were conducted on unfed smolts held in fresh water at three time intervals during their downstream migration period, representing the stage of migration at lake-exit, and the expected timing for estuary-entry and ocean-entry (0, 1 and 3 weeks after lake-exit, respectively). In general, salinity preference behaviour varied across the three time periods consistent with expected transition from river to estuary to ocean. Further, individual physiological condition did influence habitat choice. Smolt condition factor (K) and energy density were positively correlated with salinity preference behaviour in the estuary and ocean outmigration stages, but not at lake-exit. Our results suggest that smolt physiological condition upon reaching the estuary could influence migratory behaviour and habitat selection. This provides evidence on the temporally dependent interplay of physiology, behaviour and migration in wild juvenile Pacific salmon, with juvenile rearing conditions influencing smolt energetic status, which in turn influences habitat choice during downstream migration. The implication for the conservation of migratory species is that the relative importance of stopover habitats may vary as a function of initial condition.

Estimating phenology and phenological shifts with hierarchical modeling.

Climate-driven changes to phenology are some of the most prevalent climate change impacts, yet there is no commonly accepted approach to modeling phenological shifts. Here, we present a hierarchical modeling framework for estimating intra-annual patterns in phenology (e.g., peak phenological expression) and analyzing interannual rates of change in peak phenology. Our approach allows for the estimation of multiple sources of uncertainty, including observation error (e.g., imperfect observations of intra-annual patterns in phenology like peak flowering date) and variation in phenological processes (e.g., uncertainty in the rate of change in annual peak phenological expression). Covariates may be included as predictors of annual peaks or interannual variability in phenological responses. We demonstrate the use of our hierarchical modeling framework in two migratory species-juvenile chum salmon and Swainson's thrush. We acknowledge that the complexity of hierarchical models can be difficult to implement from scratch and present an R package that can be used to model peak dates and range (number of days between 25th- and 75th-quartile dates), as well as a rate of change in peak phenology. Increasing precision, calculating uncertainty, and allowing for imperfect data sets when estimating phenological shifts should help ecologists understand how organisms respond to climate change.

Phenological shifts and mismatch with marine productivity vary among Pacific salmon species and populations.

Global climate change is shifting the timing of life-cycle events, sometimes resulting in phenological mismatches between predators and prey. Phenological shifts and subsequent mismatches may be consistent across populations, or they could vary unpredictably across populations within the same species. For anadromous Pacific salmon (Oncorhynchus spp.), juveniles from thousands of locally adapted populations migrate from diverse freshwater habitats to the Pacific Ocean every year. Both the timing of freshwater migration and ocean arrival, relative to nearshore prey (phenological match/mismatch), can control marine survival and population dynamics. Here we examined phenological change of 66 populations across six anadromous Pacific salmon species throughout their range in western North America with the longest time series spanning 1951-2019. We show that different salmon species have different rates of phenological change but that there was substantial within-species variation that was not correlated with changing environmental conditions or geographic patterns. Moreover, outmigration phenologies have not tracked shifts in the timing of marine primary productivity, potentially increasing the frequency of future phenological mismatches. Understanding population responses to mismatches with prey are an important part of characterizing overall population-specific climate vulnerability.

Oxidative stress associated with paternal care in smallmouth bass (Micropterus dolomieu).

In species that provide parental care, care for offspring is often accompanied by an increase in locomotor activity and a decrease in feeding opportunities which can negatively impact endogenous energy reserves. Depletion of parental energy stores and declines in nutritional condition can cause physiological disturbances, such as an imbalance between free radical production and available antioxidants, known as oxidative stress. Using the teleost smallmouth bass (Micropterus dolomieu) as a model, we tested if the energetic challenge associated with sole paternal care was associated with oxidative stress. Blood samples from parental males were collected throughout parental care, during egg, embryo, and larval stages of offspring development, and assayed for both antioxidant capacity and oxidative damage. A reduction in oxygen radical absorbance capacity was observed during the parental care period, indicating a decrease in resistance to oxidative stress. Although no change was observed in the reduced:total thiol ratio, a significant increase in the concentration of both oxidized and total thiols occurred during the parental care period. No increase in the oxidative stress markers 8-hydroxy-2-deoxyguanosine, protein carbonyls and lipid peroxides was observed. We concluded that oxidative stress did not occur as a result of parental care in the male smallmouth bass. This study provides evidence that participation in energetically taxing activities, such as parental care, can result in a decrease in antioxidant resources, but may not always result in oxidative stress.

Limits on performance and survival of juvenile sockeye salmon (Oncorhynchus nerka) during food deprivation: a laboratory-based study.

Long-distance migrations can be energetically demanding and can represent phases of high mortality. Understanding relationships between body condition and migratory performance can help illuminate the challenges and vulnerabilities of migratory species. Juvenile anadromous sockeye salmon (Oncorhynchus nerka) may migrate over 1000 km from their freshwater nursery habitats to estuary and ocean feeding grounds. During the period corresponding to the seaward migration of sockeye salmon, we held smolts in the laboratory to ask the following: (i) Does non-feeding migration duration influence prolonged swim performance and survival? (ii) What are the relationships between individual body condition and swim performance and survival? Wild sockeye salmon were intercepted during their migration and held without food for up to 61 days to represent the non-feeding freshwater migration and the extremes of poor estuary habitat. We conducted 40 sets of prolonged swim trials on 319 fish from 3 treatment groups that represented entrance to the marine environment on (i) an average,(ii) a delayed and (iii) a severely delayed migration schedule. Experimentally controlled freshwater migration duration did not impact swim performance or survival. Swim performance decreased concomitant with condition factor, where smolts with a Fulton's condition factor of <0.69 were less likely (<50% probability) to complete the swim test (90 min swim test, at ~0.50 m/s). Survival of salmon smolts in the laboratory was less likely at energy densities of less than 3.47 MJ/kg. Swim performance decreased much sooner than survival, suggesting that swim performance, and therefore condition factor, may be a good indicator of survival of migratory smolts, as fish with reduced swim performance will likely be predated. These two relationships, one more ecologically relevant and one more clinical, help reveal the limits of long-distance migration for juvenile salmon and can be used to determine population-specific starvation risk associated with various freshwater and marine habitat conditions.

A physiological comparison of three techniques for reviving sockeye salmon exposed to a severe capture stressor during upriver migration.

Capture of fish in commercial and recreational fisheries causes disruption to their physiological homeostasis and can result in delayed mortality for fish that are released. For fish that are severely impaired, it may be desirable to attempt revival prior to release to reduce the likelihood of post-release mortality. In this study, male sockeye salmon (Oncorhynchus nerka) undergoing their upriver migration were used to examine short-term physiological changes during the following three revival treatments after beach seine capture and air exposure: a pump-powered recovery box that provided ram ventilation at one of two water flow rates; and a cylindrical, in-river recovery bag, which ensured that fish were oriented into the river flow. Beach seine capture followed by a 3 min air exposure resulted in severe impairment of reflexes such that fish could not maintain positive orientation or properly ventilate. All three revival treatments resulted in significant reductions in reflex impairment within 15 min, with full recovery of reflex responses observed within 60-120 min. For most variables measured, including plasma lactate, cortisol and osmolality, there were no significant differences among revival treatments. There was some evidence for impaired recovery in the low-flow recovery box, in the form of higher haematocrit and plasma sodium. These data mirror published recovery profiles for a recovery box study in the marine environment where a survival benefit occurred, suggesting that the methods tested here are viable options for reviving salmon caught in freshwater. Importantly, with most of the benefit to animal vitality accrued in the first 15 min, prolonging recovery when fish become vigorous may not provide added benefit because the confinement itself is likely to serve as a stressor.

Facing the river gauntlet: understanding the effects of fisheries capture and water temperature on the physiology of coho salmon.

An improved understanding of bycatch mortality can be achieved by complementing field studies with laboratory experiments that use physiological assessments. This study examined the effects of water temperature and the duration of net entanglement on physiological disturbance and recovery in coho salmon (Oncorhynchus kisutch) after release from a simulated beach seine capture. Heart rate was monitored using implanted electrocardiogram biologgers that allowed fish to swim freely before and after release. A subset of fish was recovered in respirometers to monitor metabolic recovery, and separate groups of fish were sacrificed at different times to assess blood and white muscle biochemistry. One hour after release, fish had elevated lactate in muscle and blood plasma, depleted tissue energy stores, and altered osmoregulatory status, particularly in warmer (15 vs. 10°C) and longer (15 vs. 2 min) capture treatments. A significant effect of entanglement duration on blood and muscle metabolites remained after 4 h. Oxygen consumption rate recovered to baseline within 7-10 h. However, recovery of heart rate to routine levels was longer and more variable, with most fish taking over 10 h, and 33% of fish failing to recover within 24 h. There were no significant treatment effects on either oxygen consumption or heart rate recovery. Our results indicate that fishers should minimize handling time for bycatch and maximize oxygen supply during crowding, especially when temperatures are elevated. Physiological data, such as those presented here, can be used to understand mechanisms that underlie bycatch impairment and mortality, and thus inform best practices that ensure the welfare and conservation of affected species.

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.

Oxidative stress in Pacific salmon (Oncorhynchus spp.) during spawning migration.

The energetic and physiological challenges of spawning migrations in semelparous Pacific salmon (Oncorhynchus spp.) have been well characterized. However, the accompanying costs associated with oxidative stress during this nonfeeding migration and the potential connection to senescence have not been explored. Oxidative stress is caused by an imbalance between free radical production and absorption, leading to irreparable cellular damage that accumulates over time and contributes to senescence. The objective of this study was to determine whether oxidative stress occurs during migration between river entrance and spawning for maturing pink salmon (Oncorhynchus gorbuscha), a semelparous species. Samples of plasma, liver, heart, brain, red muscle, and white muscle were collected from individual pink salmon at both the beginning and the end of the freshwater migration and then assayed for antioxidant capacity as well as for oxidative DNA damage. Antioxidant capacity and DNA damage changed between sites on a tissue-specific basis, demonstrating that oxidative stress may be experienced differentially between tissues. Consistent with our prediction, DNA damage was higher and antioxidant capacity lower in plasma (an integrative measure of body condition) and heart tissue at the spawning grounds compared with river entrance. The increased oxidative stress of these tissues is correlated with the senescence and deterioration associated with a semelparous reproductive strategy. However, similar changes were not seen in liver, red muscle, or white muscle. More surprisingly, the antioxidant capacity was higher and DNA damage was lower in the brains of spawning migrants at the spawning grounds than at river entrance. The latter results highlight the importance of tissue-specific variability in understanding the role that oxidative stress may play in spawning migration success.

Sex-specific consequences of experimental cortisol elevation in pre-reproductive wild largemouth bass.

Experimental implants were used to investigate the effect of elevated cortisol (the primary stress hormone in teleost fish) on energetic and physiological condition prior to reproduction in male and female largemouth bass (Micropterus salmoides). Fish were wild-caught from lakes in Illinois, and held in experimental ponds for the duration of the study. Between 9 and 13 days after cortisol treatment, and immediately prior to the start of the reproductive period, treated and control animals were sampled. Females exhibited lower muscle lipid content, lower liver glycogen content, and higher hepatosomatic indices than males, regardless of treatment. Also, cortisol-treated females had higher hepatosomatic indices and lower final mass than control females, whereas males showed no differences between treatment groups. Finally, cortisol-treated females had higher gonadal cortisol concentrations than control females. In general, we found evidence of reduced energetic stores in female fish relative to male fish, likely due to timing differences in the allocation of resources during reproduction between males and females. Perhaps driven by the difference in energetic reserves, our data further suggest that females are more sensitive than males to elevated cortisol during the period immediately prior to reproduction.

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

The live release of wild adult Pacific salmon (Oncorhynchus spp.) following capture is a management tactic often used in commercial, aboriginal, and recreational fisheries. Fisheries capture and handling can be both exhausting and stressful to fish, which can limit their ability to swim and survive after release. As a result, researchers have assessed methods intended to improve post-release survival by assisting the flow of water over the gills of fish prior to release. Such approaches use recovery bags or boxes that direct water over the gills of restrained fish. This study evaluated a method of assisting ventilation that mimics one often employed by recreational anglers (i.e. holding fish facing into a current). Under laboratory conditions, wild Fraser River sockeye salmon (Oncorhynchus nerka) either received manual ventilation assistance for 1 min using a jet of water focused at the mouth or were left to recover unassisted following a capture-and-release simulation. A control group consisted of fish that were not exposed to the simulation or ventilation assistance. The experiment was conducted at 16 and 21°C, average and peak summer water temperatures for the Fraser River, and fish survival was monitored for 33 days. At 21°C, all fish perished within 3 days after treatment in all experimental groups, highlighting the consequences of handling adult sockeye salmon during elevated migration temperatures. Survival was higher at 16°C, with fish surviving on average 15-20 days after treatment. At 16°C, the capture-and-release simulation and ventilation assistance did not affect the survival of males; however, female survival was poor after the ventilation assistance compared with the unassisted and control groups. Our results suggest that the method of ventilation assistance tested in this study may not enhance the post-release survival of adult Fraser River sockeye salmon migrating in fresh water.