DNA in Action: Rapid Application of DNA Variation to Sockeye Salmon Fisheries Management

Commitment to conservation-based management of exploited fish species imposes unprecedented requirements for adaptive, real-time management of biologically and socially complex mixed-stock fisheries such as those conducted for Pacific salmon. Stock identification is a key component of the management process, with population-specific timing and abundance information often incorporated into management decisions. By using both microsatellite and major histocompatibility complex genetic variation, we achieved highly accurate estimates of stock composition for Fraser River sockeye salmon. Over a 2-month period in 2002, we analyzed 9300 returning Fraser River sockeye salmon sampled in mixed-stock fisheries, and provided stock composition estimates to fishery managers within 9–30 h of sample delivery. Stock-specific exploitation targets governed by conservation concerns were achieved in this fishery.     

生理学与基因组学:走向系统生物学

近十年来,生理学与基因组学达到了空前的融合。尽管生理基因组学还是一个非常年轻的研究领域,系统生物学概念的引入必将推进生理基因组学达到全新的水平。本文概要地叙述了这个令人振奋的生理科学的新时代给生理学家带来的机遇和挑战,并以我们自己近十年来的经验为例,讨论了怎样通过扩展和延伸生理学与基因组学的结合,从而对生物学得到系统的理解。     

Dead fish swimming: a review of research on the early migration and high premature mortality in adult Fraser River sockeye salmon Oncorhynchus nerka

Adult sockeye salmon Oncorhynchus nerka destined for the Fraser River, British Columbia are some of the most economically important populations but changes in the timing of their homeward migration have led to management challenges and conservation concerns. After a directed migration from the open ocean to the coast, this group historically would mill just off shore for 3-6 weeks prior to migrating up the Fraser River. This milling behaviour changed abruptly in 1995 and thereafter, decreasing to only a few days in some years (termed early migration), with dramatic consequences that have necessitated risk-averse management strategies. Early migrating fish consistently suffer extremely high mortality (exceeding 90% in some years) during freshwater migration and on spawning grounds prior to spawning. This synthesis examines multidisciplinary, collaborative research aimed at understanding what triggers early migration, why it results in high mortality, and how fisheries managers can utilize these scientific results. Tissue analyses from thousands of O. nerka captured along their migration trajectory from ocean to spawning grounds, including hundreds that were tracked with biotelemetry, have revealed that early migrants are more reproductively advanced and ill-prepared for osmoregulatory transition upon their entry into fresh water. Gene array profiles indicate that many early migrants are also immunocompromised and stressed, carrying a genomic profile consistent with a viral infection. The causes of these physiological changes are still under investigation. Early migration brings O. nerka into the river when it is 3-6° C warmer than historical norms, which for some late-run populations approaches or exceeds their critical maxima leading to the collapse of metabolic and cardiac scope, and mortality. As peak spawning dates have not changed, the surviving early migrants tend to mill in warm lakes near to spawning areas. These results in the accumulation of many more thermal units and longer exposures to freshwater diseases and parasites compared to fish that delay freshwater entry by milling in the cool ocean environment. Experiments have confirmed that thermally driven processes are a primary cause of mortality for early-entry migrants. The Fraser River late-run O. nerka early migration phenomenon illustrates the complex links that exist between salmonid physiology, behaviour and environment and the pivotal role that water temperature can have on population-specific migration survival.     

Atlantic salmon (Salmo salar L.) genetics in the 21st century: taking leaps forward in aquaculture and biological understanding

Atlantic salmon (Salmo salar L.) is among the most iconic and economically important fish species and was the first member of Salmonidae to have a high‐quality reference genome assembly published. Advances in genomics have become increasingly central to the genetic improvement of farmed Atlantic salmon as well as conservation of wild salmon stocks. The salmon genome has also been pivotal in shaping our understanding of the evolutionary and functional consequences arising from an ancestral whole‐genome duplication event characterising all Salmonidae members. Here, we provide a review of the current status of Atlantic salmon genetics and genomics, focussed on progress made from genome‐wide research aimed at improving aquaculture production and enhancing understanding of salmonid ecology, physiology and evolution. We present our views on the future direction of salmon genomics, including the role of emerging technologies (e.g. genome editing) in elucidating genetic features that underpin functional variation in traits of commercial and evolutionary importance.     

Adult spawners: A critical period for subarctic Chinook salmon in a changing climate

Concurrent, distribution-wide abundance declines of some Pacific salmon species, including Chinook salmon (Oncorhynchus tshawytscha), highlights the need to understand how vulnerability at different life stages to climate stressors affects population dynamics and fisheries sustainability. Yukon River Chinook salmon stocks are among the largest subarctic populations, near the northernmost extent of the species range. Existing research suggests that Yukon River Chinook salmon population dynamics are largely driven by factors occurring between the adult spawner life stage and their offspring's first summer at sea (second year post-hatching). However, specific mechanisms sustaining chronic poor productivity are unknown, and there is a tremendous sense of urgency to understand causes, as declines of these stocks have taken a serious toll on commercial, recreational, and indigenous subsistence fisheries. Therefore, we leveraged multiple existing datasets spanning parent and juvenile stages of life history in freshwater and marine habitats. We analyzed environmental data in association with the production of offspring that survive to the marine juvenile stage (juveniles per spawner). These analyses suggest more than 45% of the variability in the production of juvenile Chinook salmon is associated with river temperatures or water discharge levels during the parent spawning migration. Over the past two decades, parents that experienced warmer water temperatures and lower discharge in the mainstem Yukon River produced fewer juveniles per spawning adult. We propose the adult spawner life stage as a critical period regulating population dynamics. We also propose a conceptual model that can explain associations between population dynamics and climate stressors using independent data focused on marine nutrition and freshwater heat stress. It is sobering to consider that some of the northernmost Pacific salmon habitats may already be unfavorable to these cold-water species. Our findings have immediate implications, given the common assumption that northern ranges of Pacific salmon offer refugia from climate stressors.     

Injuries from Non-Retention in Gillnet Fisheries Suppress Reproductive Maturation in Escaped Fish

Exploitation of fisheries resources has unintended consequences, not only in the bycatch and discard of non-target organisms, but also in damage to targeted fish that are injured by gear but not landed (non-retention). Delayed mortality due to non-retention represents lost reproductive potential in exploited stocks, while not contributing to harvest. Our study examined the physiological mechanisms by which delayed mortality occurs and the extent to which injuries related to disentanglement from commercial gear compromise reproductive success in spawning stocks of Pacific salmon (Oncorhynchus spp.). We found evidence for elevated stress in fish injured via non-retention in gillnet fisheries. Plasma cortisol levels correlated with the severity of disentanglement injury and were elevated in fish that developed infections related to disentanglement injuries. We also analyzed sex steroid concentrations in females (estradiol-17β and 17,20β-dihydroxy-4-pregnen-3-one) to determine whether non-retention impairs reproductive potential in escaped individuals. We demonstrate evidence for delayed or inhibited maturation in fish with disentanglement injuries. These findings have important implications for effective conservation and management of exploited fish stocks and suggest means to improve spawning success in such stocks if retention in commercial fisheries is improved and incidental mortality reduced.     

Persistent leatherback turtle migrations present opportunities for conservation

Effective transboundary conservation of highly migratory marine animals requires international management cooperation as well as clear scientific information about habitat use by these species. Populations of leatherback turtles (Dermochelys coriacea) in the eastern Pacific have declined by >90% during the past two decades, primarily due to unsustainable egg harvest and fisheries bycatch mortality. While research and conservation efforts on nesting beaches are ongoing, relatively little is known about this population of leatherbacks' oceanic habitat use and migration pathways. We present the largest multi-year (2004-2005, 2005-2006, and 2007) satellite tracking dataset (12,095 cumulative satellite tracking days) collected for leatherback turtles. Forty-six females were electronically tagged during three field seasons at Playa Grande, Costa Rica, the largest extant nesting colony in the eastern Pacific. After completing nesting, the turtles headed southward, traversing the dynamic equatorial currents with rapid, directed movements. In contrast to the highly varied dispersal patterns seen in many other sea turtle populations, leatherbacks from Playa Grande traveled within a persistent migration corridor from Costa Rica, past the equator, and into the South Pacific Gyre, a vast, low-energy, low-productivity region. We describe the predictable effects of ocean currents on a leatherback migration corridor and characterize long-distance movements by the turtles in the eastern South Pacific. These data from high seas habitats will also elucidate potential areas for mitigating fisheries bycatch interactions. These findings directly inform existing multinational conservation frameworks and provide immediate regions in the migration corridor where conservation can be implemented. We identify high seas locations for focusing future conservation efforts within the leatherback dispersal zone in the South Pacific Gyre.     

Insights on the concept of indicator populations derived from parentage‐based tagging in a large‐scale coho salmon application in British Columbia,Canada

For Pacific salmon, the key fisheries management goal in British Columbia (BC) is to maintain and restore healthy and diverse Pacific salmon populations, making conservation of salmon biodiversity the highest priority for resource management decision‐making. Salmon status assessments are often conducted on coded‐wire‐tagged subsets of indicator populations based on assumptions of little differentiation within or among proximal populations. In the current study of southern BC coho salmon (Oncorhynchus kisutch) populations, parentage‐based tagging (PBT) analysis provided novel information on migration and life‐history patterns to test the assumptions of biological homogeneity over limited (generally < 100 km) geographic distances and, potentially, to inform management of fisheries and hatchery broodstocks. Heterogeneity for location and timing of fishery captures, family productivity, and exploitation rate was observed over small geographic scales, within regions that are, or might be expected to be, within the area encompassed by a single‐tagged indicator population. These results provide little support for the suggestion that information gained from tagged indicator populations is representative of marine distribution, productivity, and exploitation patterns of proximal populations.     

Competing conservation objectives for predators and prey: estimating killer whale prey requirements for Chinook salmon

Ecosystem-based management (EBM) of marine resources attempts to conserve interacting species. In contrast to single-species fisheries management, EBM aims to identify and resolve conflicting objectives for different species. Such a conflict may be emerging in the northeastern Pacific for southern resident killer whales (Orcinus orca) and their primary prey, Chinook salmon (Oncorhynchus tshawytscha). Both species have at-risk conservation status and transboundary (Canada-US) ranges. We modeled individual killer whale prey requirements from feeding and growth records of captive killer whales and morphometric data from historic live-capture fishery and whaling records worldwide. The models, combined with caloric value of salmon, and demographic and diet data for wild killer whales, allow us to predict salmon quantities needed to maintain and recover this killer whale population, which numbered 87 individuals in 2009. Our analyses provide new information on cost of lactation and new parameter estimates for other killer whale populations globally. Prey requirements of southern resident killer whales are difficult to reconcile with fisheries and conservation objectives for Chinook salmon, because the number of fish required is large relative to annual returns and fishery catches. For instance, a U.S. recovery goal (2.3% annual population growth of killer whales over 28 years) implies a 75% increase in energetic requirements. Reducing salmon fisheries may serve as a temporary mitigation measure to allow time for management actions to improve salmon productivity to take effect. As ecosystem-based fishery management becomes more prevalent, trade-offs between conservation objectives for predators and prey will become increasingly necessary. Our approach offers scenarios to compare relative influence of various sources of uncertainty on the resulting consumption estimates to prioritise future research efforts, and a general approach for assessing the extent of conflict between conservation objectives for threatened or protected wildlife where the interaction between affected species can be quantified.     

Sharing the water column: physiological mechanisms underlying species-specific habitat use in tunas

Tuna species support some of the world’s largest commercial and recreational fisheries. Their extensive migratory patterns expose them to multiple national and international fisheries and fishery management regimes. Several prized species have become the focus of global conservation efforts and there is a growing worldwide interest in establishing optimal strategies for sustainable tuna fisheries. Although this task has proven to be very challenging, it has taken on a new sense of urgency in the face of the potential effects of global climate change. A better understanding of the interactions between environmental conditions and tuna physiology and how they affect tuna behavior will offer population and stock assessment modelers and fisheries biologists a more mechanistic understanding of tuna distribution patterns and may help predict changes in both geographic and depth-related movement patterns. Indeed, physiological data comprise a growing component of multi-trait analysis approaches to species conservation. Our review aims to summarize what is known about differences among tuna species in distribution patterns, tolerances to environmental conditions, and physiological characteristics that correlate with the capacity to inhabit cooler (deeper, higher latitude) and even hypoxic waters. To achieve this goal, we discuss how these physiological traits are associated with habitat partitioning within the three-dimensional oceanic environment and with niche expansion into cooler and hypoxic waters. We also point out areas where additional research is needed to predict more accurately how future changes in oceanographic conditions will affect the distributions and movement patterns of tunas and their availability to fisheries.     

Hatching Knowledge: A Case Study on the Hybridization of Local Ecological Knowledge and Scientific Knowledge in Small-Scale Atlantic Salmon (<Emphasis Type="Italic">Salmo salar</Emphasis>) Cultivation in Norway

We investigate drivers of hybridization of local ecological knowledge (LEK) and scientific knowledge (SK) in small-scale Atlantic salmon (Salmo salar) fisheries in western Norway through a case study from the Ørsta River. We find three primary drivers of knowledge hybridization in local fishing groups as part of wild Atlantic salmon cultivation activities: facilitating intergenerational knowledge exchange, coping with regulatory change, and improving the perceived validity of local knowledge sets. We also identify three challenges to knowledge hybridization, and discuss how both drivers and challenges relate to once complementary SK and LEK sets that have diverged as SK has become more technical and complex. We examine the processes by which LEK and SK develop, evolve, and are used to facilitate wild salmon conservation in these fisheries and discuss the role hatcheries can play adapting and utilizing large-scale SK and salmon policy to the local environment through hybridization processes. We conclude with recommendations as to how reframing managerial views on hatcheries as facilitators of knowledge production and transfer may improve both the accessibility of SK to local communities and the integration of LEK into Norwegian wild salmon management.     

Sex and proximity to reproductive maturity influence the survival, final maturation, and blood physiology of Pacific salmon when exposed to high temperature during a simulated migration

Some Pacific salmon populations have been experiencing increasingly warmer river temperatures during their once-in-a-lifetime spawning migration, which has been associated with en route and prespawn mortality. The mechanisms underlying such temperature-mediated mortality are poorly understood. Wild adult pink (Oncorhynchus gorbuscha) and sockeye (Oncorhynchus nerka) salmon were used in this study. The objectives were to investigate the effects of elevated water temperature on mortality, final maturation, and blood properties under controlled conditions that simulated a "cool" (13°C) and "warm" (19°C) freshwater spawning migration. After 10 d at 13°C, observed mortality was 50%-80% in all groups, which suggested that there was likely some mortality associated with handling and confinement. Observed mortality after 10 d at 19°C was higher, reaching ≥98% in male pink salmon and female pink and sockeye salmon. Thus, male sockeye salmon were the most thermally tolerant (54% observed mortality). Model selection supported the temperature- and sex-specific mortality patterns. The pink salmon were closer to reproductive maturation and farther along the senescence trajectory than sockeye salmon, which likely influenced their survival and physiological responses throughout the experiment. Females of both species held at 19°C had reduced plasma sex steroids compared with those held at 13°C, and female pink salmon were less likely to become fully mature at 19° than at 13°C. Male and female sockeye salmon held at 19°C had higher plasma chloride and osmolality than those held at 13°C, indicative of a thermally related stress response. These findings suggest that sex differences and proximity to reproductive maturity must be considered when predicting thermal tolerance and the magnitude of en route and prespawn mortality for Pacific salmon.     

The future is now: Amplicon sequencing and sequence capture usher in the conservation genomics era

The genomics revolution has initiated a new era of population genetics where genome‐wide data are frequently used to understand complex patterns of population structure and selection. However, the application of genomic tools to inform management and conservation has been somewhat rare outside a few well studied species. Fortunately, two recently developed approaches, amplicon sequencing and sequence capture, have the potential to significantly advance the field of conservation genomics. Here, amplicon sequencing refers to highly multiplexed PCR followed by high‐throughput sequencing (e.g., GTseq), and sequence capture refers to using capture probes to isolate loci from reduced‐representation libraries (e.g., Rapture). Both approaches allow sequencing of thousands of individuals at relatively low costs, do not require any specialized equipment for library preparation, and generate data that can be analyzed without sophisticated computational infrastructure. Here, we discuss the advantages and disadvantages of each method and provide a decision framework for geneticists who are looking to integrate these methods into their research programme. While it will always be important to consider the specifics of the biological question and system, we believe that amplicon sequencing is best suited for projects aiming to genotype <500 loci on many individuals (>1,500) or for species where continued monitoring is anticipated (e.g., long‐term pedigrees). Sequence capture, on the other hand, is best applied to projects including fewer individuals or where >500 loci are required. Both of these techniques should smooth the transition from traditional genetic techniques to genomics, helping to usher in the conservation genomics era.     

Interaction between hatchery and wild Pacific salmon in the Far East of Russia: A review

We review studies of interactions between hatchery and wild Pacific salmon in the Russian Far East. This includes the role of hatchery practices that result in premature migration to the sea and increased mortality, and data on feeding and territorial competition between juveniles of hatchery and wild origin. In the course of downstream migration many juvenile hatchery salmon are eliminated by wild salmon predation. During the marine period, Japanese hatchery chum salmon (Oncorhynchus keta) distribution overlaps the distribution of Russian wild salmon. Consequently, replacement of wild populations by hatchery fishes, as a result of abundant juvenile hatchery releases combined with extensive poaching in spawning grounds, is apparent in some Russian rivers. Interactions between the populations occur in all habitats. The importance of conservation of wild salmon populations requires a more detailed study of the consequences of interactions between natural and artificially reared fishes.     

Natal origin of Namibian grey whale implies new distance record for in-water migration

We use genomics to identify the natal origin of a grey whale found in the South Atlantic, at least 20 000 km from the species core range (halfway around the world). The data indicate an origin in the North Pacific, possibly from the endangered western North Pacific population, thought to include only approximately 200 individuals. This contributes to our understanding of Atlantic sightings of this species known primarily from the North Pacific, and could have conservation implications if grey whales have the potential for essentially global dispersion. More broadly, documenting and understanding rare extreme migration events have potential implications for the understanding of how a species may be able to respond to global change.     

Conservation physiology for applied management of marine fish: an overview with perspectives on the role and value of telemetry

Physiological studies focus on the responses of cells, tissues and individuals to stressors, usually in laboratory situations. Conservation and management, on the other hand, focus on populations. The field of conservation physiology addresses the question of how abiotic drivers of physiological responses at the level of the individual alter requirements for successful conservation and management of populations. To achieve this, impacts of physiological effects at the individual level need to be scaled to impacts on population dynamics, which requires consideration of ecology. Successfully realizing the potential of conservation physiology requires interdisciplinary studies incorporating physiology and ecology, and requires that a constructive dialogue develops between these traditionally disparate fields. To encourage this dialogue, we consider the increasingly explicit incorporation of physiology into ecological models applied to marine fish conservation and management. Conservation physiology is further challenged as the physiology of an individual revealed under laboratory conditions is unlikely to reflect realized responses to the complex variable stressors to which it is exposed in the wild. Telemetry technology offers the capability to record an animal's behaviour while simultaneously recording environmental variables to which it is exposed. We consider how the emerging insights from telemetry can strengthen the incorporation of physiology into ecology.     

Transmission dynamics of parasitic sea lice from farm to wild salmon

Marine salmon farming has been correlated with parasitic sea lice infestations and concurrent declines of wild salmonids. Here, we report a quantitative analysis of how a single salmon farm altered the natural transmission dynamics of sea lice to juvenile Pacific salmon. We studied infections of sea lice (Lepeophtheirus salmonis and Caligus clemensi) on juvenile pink salmon (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) as they passed an isolated salmon farm during their seaward migration down two long and narrow corridors. Our calculations suggest the infection pressure imposed by the farm was four orders of magnitude greater than ambient levels, resulting in a maximum infection pressure near the farm that was 73 times greater than ambient levels and exceeded ambient levels for 30 km along the two wild salmon migration corridors. The farm-produced cohort of lice parasitizing the wild juvenile hosts reached reproductive maturity and produced a second generation of lice that re-infected the juvenile salmon. This raises the infection pressure from the farm by an additional order of magnitude, with a composite infection pressure that exceeds ambient levels for 75 km of the two migration routes. Amplified sea lice infestations due to salmon farms are a potential limiting factor to wild salmonid conservation.     

Watershed‐scale climate influences productivity of Chinook salmon populations across southcentral Alaska

The ecosystems supporting Pacific salmon (Oncorhynchus spp.) are changing rapidly as a result of climate change and habitat alteration. Understanding how—and how consistently—salmon populations respond to changes at regional and watershed scales has major implications for fisheries management and habitat conservation. Chinook salmon (O. tshawytscha) populations across Alaska have declined over the past decade, resulting in fisheries closures and prolonged impacts to local communities. These declines are associated with large‐scale climate drivers, but uncertainty remains about the role of local conditions (e.g., precipitation, streamflow, and stream temperature) that vary among the watersheds where salmon spawn and rear. We estimated the effects of these and other environmental indicators on the productivity of 15 Chinook salmon populations in the Cook Inlet basin, southcentral Alaska, using a hierarchical Bayesian stock‐recruitment model. Salmon spawning during 2003–2007 produced 57% fewer recruits than the previous long‐term average, leading to declines in adult returns beginning in 2008. These declines were explained in part by density dependence, with reduced population productivity following years of high spawning abundance. Across all populations, productivity declined with increased precipitation during the fall spawning and early incubation period and increased with above‐average precipitation during juvenile rearing. Above‐average stream temperatures during spawning and rearing had variable effects, with negative relationships in many warmer streams and positive relationships in some colder streams. Productivity was also associated with regional indices of streamflow and ocean conditions, with high variability among populations. The cumulative effects of adverse conditions in freshwater, including high spawning abundance, heavy fall rains, and hot, dry summers may have contributed to the recent population declines across the region. Identifying both coherent and differential responses to environmental change underscores the importance of targeted, watershed‐specific monitoring and conservation efforts for maintaining resilient salmon runs in a warming world.     

Building strong relationships between conservation genetics and primary industry leads to mutually beneficial genomic advances

Several reviews in the past decade have heralded the benefits of embracing high‐throughput sequencing technologies to inform conservation policy and the management of threatened species, but few have offered practical advice on how to expedite the transition from conservation genetics to conservation genomics. Here, we argue that an effective and efficient way to navigate this transition is to capitalize on emerging synergies between conservation genetics and primary industry (e.g., agriculture, fisheries, forestry and horticulture). Here, we demonstrate how building strong relationships between conservation geneticists and primary industry scientists is leading to mutually‐beneficial outcomes for both disciplines. Based on our collective experience as collaborative New Zealand‐based scientists, we also provide insight for forging these cross‐sector relationships.     

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.