The effects of depth and salinity on juvenile Chinook salmon Oncorhynchus tshawytscha (Walbaum) habitat choice in an artificial estuary

The energetic cost for juvenile Chinook salmon Oncorhynchus tshawytscha to forage in habitats of different salinity and depth was quantified using a behavioural titration based on ideal free distribution theory. When given a choice between freshwater habitats of different depths (>0·83 or <0·83 m), a greater proportion of fish used the deeper habitat. When the deeper habitat was saltwater, the proportion of fish using it increased. When food was added to both the shallow freshwater and deep saline habitats, however, fish distribution returned to that observed when both habitats were fresh water. This indicates that the preference for deep saline habitats during the stratified phase was driven by some benefit associated with residency in deeper water, rather than salinity. The low perceived cost of low salinity might be in part due to the fish's ability to minimize this cost by only making brief forays into the alternate freshwater habitat. When the food ration delivered to the more costly, shallow habitat was 50% greater than that delivered to the less costly, deep habitat, fish distributed themselves equally between the two habitats, presumably because of equal net benefits. This study demonstrates that juvenile Chinook salmon prefer deep saline habitat to shallow freshwater habitats but will make brief forays into the freshwater habitat if food availability is sufficiently high.     

Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator

1. Non‐native predators might inflict proportionally higher mortality on prey that have no previous experience of them, compared to species that have coexisted with the predator for some time. 2. We tested whether juvenile Chinook salmon (Oncorhynchus tshawytscha) were less able to recognise a non‐native than a native predator, by investigating behavioural responses to the chemical cues of the invasive smallmouth bass (Micropterus dolomieu) and the native northern pikeminnow (Ptychocheilus oregonensis) in both laboratory and field experiments. 3. Laboratory results demonstrated strong innate antipredator responses of individual juvenile Chinook salmon to northern pikeminnow; fish spent 70% of time motionless and exhibited 100% greater panic response than in controls. By contrast, antipredator responses to the chemical cues of smallmouth bass did not differ from controls. 4. These results were supported by similar differences in recognition of these predator odours by groups of juvenile Chinook salmon in fully natural conditions, though responses reflected a greater range of antipredator behaviours by individuals. In field trials, responses to northern pikeminnow odour resulted in increased flight or absence, reductions in swimming and foraging, and increased time spent near the substratum, compared to smallmouth bass odour. 5. Given that survival of juvenile fish is facilitated by predator recognition, our results support the hypothesis that naivety may be an important factor determining the effect of non‐native predators on prey populations. Efforts to manage the effect of native and non‐native predators may benefit by considering complex behavioural interactions, such as these at the individual and group levels.     

Changes in habitat availability for outmigrating juvenile salmon (Oncorhynchus spp.) following estuary restoration

The restoration of the Nisqually River Delta (Washington, U.S.A.) represents one of the largest efforts toward reestablishing the ecosystem function and resilience of modified habitat in the Puget Sound, particularly for anadromous salmonid species. The opportunity for outmigrating salmon to access and benefit from the expansion of available tidal habitat can be quantified by several physical attributes, which are related to the ecological and physiological responses of juvenile salmon. We monitored a variety of physical parameters to measure changes in opportunity potential from historic, pre‐restoration, and post‐restoration habitat conditions at several sites across the delta. These parameters included channel morphology, water quality, tidal elevation, and landscape connectivity. We conducted fish catch surveys across the delta to determine if salmon was utilizing restored estuary habitat. Overall major channel area increased 42% and major channel length increased 131% from pre‐ to post‐restoration conditions. Furthermore, the results of our tidal inundation model indicated that major channels were accessible up to 75% of the time, as opposed to 30% pre‐restoration. Outmigrating salmon utilized this newly accessible habitat as quickly as 1 year post‐restoration. The presence of salmon in restored tidal channels confirmed rapid post‐restoration increases in opportunity potential on the delta despite habitat quality differences between restored and reference sites.     

Using otolith chemical and structural analysis to investigate reservoir habitat use by juvenile Chinook salmon Oncorhynchus tshawytscha

Isotopic composition of ⁸⁷Sr:⁸⁶Sr and natural elemental tracers (Sr, Ba, Mg, Mn and Ca) were quantified from otoliths in juvenile and adult Chinook salmon Oncorhynchus tshawytscha to assess the ability of otolith microchemistry and microstructure to reconstruct juvenile O. tshawytscha rearing habitat and growth. Daily increments were measured to assess relative growth between natal rearing habitats. Otolith microchemistry was able to resolve juvenile habitat use between reservoir and natal tributary rearing habitats (within headwater basins), but not among catchments. Results suggest that 90% (n = 18) of sampled non‐hatchery adults returning to the Middle Fork Willamette River were reared in a reservoir and 10% (n = 2) in natal tributary habitat upstream from the reservoir. Juveniles collected in reservoirs had higher growth rates than juveniles reared in natal streams. The results demonstrate the utility of otolith microchemistry and microstructure to distinguish among rearing habitats, including habitats in highly altered systems.     

Behavioural thermoregulation by subyearling fall (autumn) Chinook salmon Oncorhynchus tshawytscha in a reservoir

This study investigated behavioural thermoregulation by subyearling fall (autumn) Chinook salmon Oncorhynchus tshawytscha in a reservoir on the Snake River, Washington, U.S.A. During the summer, temperatures in the reservoir varied from 23° C on the surface to 11° C at 14 m depth. Subyearlings implanted with temperature-sensing radio transmitters were released at the surface at temperatures >20° C during three blocks of time in summer 2004. Vertical profiles were taken to measure temperature and depth use as the fish moved downstream over an average of 5·6–7·2 h and 6·0–13·8 km. The majority of the subyearlings maintained average body temperatures that differed from average vertical profile temperatures during most of the time they were tracked. The mean proportion of the time subyearlings tracked within the 16–20° C temperature range was larger than the proportion of time this range was available, which confirmed temperature selection opposed to random use. The subyearlings selected a depth and temperature combination that allowed them to increase their exposure to temperatures of 16–20° C when temperatures <16 and >20° C were available at lower and higher positions in the water column. A portion of the subyearlings that selected a temperature c. 17·0° C during the day, moved into warmer water at night coincident with an increase in downstream movement rate. Though subyearlings used temperatures outside of the 16–20° C range part of the time, behavioural thermoregulation probably reduced the effects of intermittent exposure to suboptimal temperatures. By doing so, it might enhance growth opportunity and life-history diversity in the population of subyearlings studied.     

Environmental adaptation in Chinook salmon (Oncorhynchus tshawytscha) throughout their North American range

Landscape genomics is a rapidly growing field with recent advances in both genotyping efficiency and statistical analyses that provide insight towards local adaptation of populations under varying environmental and selective pressure. Chinook salmon (Oncorhynchus tshawytscha) are a broadly distributed Pacific salmon species, occupying a diversity of habitats throughout the northeastern Pacific with pronounced variation in environmental and climate features but little is understood regarding local adaptation in this species. We used a multivariate method, redundancy analysis (RDA), to identify polygenic correlations between 19 703 SNP loci and a suite of environmental variables in 46 collections of Chinook salmon (1956 total individuals) distributed throughout much of its North American range. Models in RDA were conducted on both rangewide and regional scales by hierarchical partitioning of the populations into three distinct genetic lineages. Our results indicate that between 5.8 and 21.8% of genomic variation can be accounted for by environmental features, and 566 putatively adaptive loci were identified as targets of environmental adaptation. The most influential drivers of adaptive divergence included precipitation in the driest quarter of the year (Rangewide and North Coastal Lineage, anova P = 0.002 and 0.01, respectively), precipitation in the wettest quarter of the year (Interior Columbia River Stream‐Type Lineage, anova P = 0.03), variation in mean diurnal range in temperature (South Coastal Lineage, anova P = 0.005), and migration distance (Rangewide, anova P = 0.001). Our results indicate that environmental features are strong drivers of adaptive genomic divergence in this species, and provide a foundation to investigate how Chinook salmon might respond to global environmental change.     

Juvenile growth and aggression in diploid and triploid Chinook salmon Oncorhynchus tshawytscha (Walbaum)

Multilocus heterozygosity, aggressive and feeding behaviour, plasma cortisol levels and growth rate were evaluated among three groups of juvenile Chinook salmon Oncorhynchus tshawytscha : diploid, triploid and mixed groups of diploid and triploid fish. There was no difference between diploid and triploid fish in measurements of heterozygosity calculated using seven microsatellite loci, and these measurements did not correlate with performance measurements including feeding rate and growth rate. Aggression trials that examined small groups of fish revealed that after 4 days together in tanks, triploid fish were significantly less aggressive during feeding than diploid fish or fish in mixed groups. At the end of the trials, however, plasma cortisol levels did not differ among the three groups. Thirty-day growth trials in duplicate tanks of 60 fish revealed no difference in growth rate among diploid, triploid and mixed groups, but plasma cortisol levels were significantly lower in triploid fish than in either diploid fish or the mixed fish. Overall, independent of the above differences in aggressive behaviour and cortisol levels, these results suggest similar performance in diploid and triploid Chinook salmon, and thus provide support for the viability of triploid Chinook salmon culture in commercial aquaculture.     

An integrated linkage map reveals candidate genes underlying adaptive variation in Chinook salmon (Oncorhynchus tshawytscha)

Salmonids are an important cultural and ecological resource exhibiting near worldwide distribution between their native and introduced range. Previous research has generated linkage maps and genomic resources for several species as well as genome assemblies for two species. We first leveraged improvements in mapping and genotyping methods to create a dense linkage map for Chinook salmon Oncorhynchus tshawytscha by assembling family data from different sources. We successfully mapped 14 620 SNP loci including 2336 paralogs in subtelomeric regions. This improved map was then used as a foundation to integrate genomic resources for gene annotation and population genomic analyses. We anchored a total of 286 scaffolds from the Atlantic salmon genome to the linkage map to provide a framework for the placement 11 728 Chinook salmon ESTs. Previously identified thermotolerance QTL were found to colocalize with several candidate genes including HSP70, a gene known to be involved in thermal response, as well as its inhibitor. Multiple regions of the genome with elevated divergence between populations were also identified, and annotation of ESTs in these regions identified candidate genes for fitness related traits such as stress response, growth and behaviour. Collectively, these results demonstrate the utility of combining genomic resources with linkage maps to enhance evolutionary inferences.     

Distribution of the invasive New Zealand mudsnail (Potamopyrgus antipodarum) in the Columbia River Estuary and its first recorded occurrence in the diet of juvenile Chinook salmon (Oncorhynchus tshawytscha)

Estuaries play an important role as nurseries and migration corridors for Chinook salmon and other fishes. The invasive New Zealand mudsnail, Potamopyrgus antipodarum (Gray, 1843), has been noted in the Columbia River Estuary and other estuaries in the western USA, yet no studies have addressed the estuarine impacts of this invader. Our data show P. antipodarum is currently found in five peripheral bays and many tributaries of the Columbia River Estuary, where it can constitute a major portion of the benthic invertebrate biomass and where it co-occurs with native amphipod species. We review the history of the P. antipodarum invasion in the Columbia River Estuary and discuss potential impacts on estuarine food webs. We also report the first occurrence of P. antipodarum in the diet of juvenile Chinook salmon from the Columbia River Estuary. Although present in Chinook diets at very low frequencies, our observations of P. antipodarum in Chinook gut contents may represent early stages of food web change due to the establishment of dense estuarine snail populations. Additional research is needed to determine the effects of P. antipodarum on benthic resources, native benthic invertebrates, and benthic predators. We encourage biologists working in western USA estuaries to be alert to the possibility of encountering P. antipodarum in benthic habitats and predator diets.

Using parentage analysis to estimate rates of straying and homing in Chinook salmon (Oncorhynchus tshawytscha)

We used parentage analysis based on microsatellite genotypes to measure rates of homing and straying of Chinook salmon (Oncorhynchus tshawytscha) among five major spawning tributaries within the Wenatchee River, Washington. On the basis of analysis of 2248 natural‐origin and 11594 hatchery‐origin fish, we estimated that the rate of homing to natal tributaries by natural‐origin fish ranged from 0% to 99% depending on the tributary. Hatchery‐origin fish released in one of the five tributaries homed to that tributary at a far lower rate than the natural‐origin fish (71% compared to 96%). For hatchery‐released fish, stray rates based on parentage analysis were consistent with rates estimated using physical tag recoveries. Stray rates among major spawning tributaries were generally higher than stray rates of tagged fish to areas outside of the Wenatchee River watershed. Within the Wenatchee watershed, rates of straying by natural‐origin fish were significantly affected by spawning tributary and by parental origin: progeny of naturally spawning hatchery‐produced fish strayed at significantly higher rates than progeny whose parents were themselves of natural origin. Notably, none of the 170 offspring that were products of mating by two natural‐origin fish strayed from their natal tributary. Indirect estimates of gene flow based on F_ST statistics were correlated with but higher than the estimates from the parentage data. Tributary‐specific estimates of effective population size were also correlated with the number of spawners in each tributary.     

Population differences in Chinook salmon (Oncorhynchus tshawytscha) DNA methylation: Genetic drift and environmental factors

Local adaptation and phenotypic differences among populations have been reported in many species, though most studies focus on either neutral or adaptive genetic differentiation. With the discovery of DNA methylation, questions have arisen about its contribution to individual variation in and among natural populations. Previous studies have identified differences in methylation among populations of organisms, although most to date have been in plants and model animal species. Here we obtained eyed eggs from eight populations of Chinook salmon (Oncorhynchus tshawytscha) and assayed DNA methylation at 23 genes involved in development, immune function, stress response, and metabolism using a gene‐targeted PCR‐based assay for next‐generation sequencing. Evidence for population differences in methylation was found at eight out of 23 gene loci after controlling for developmental timing in each individual. However, we found no correlation between freshwater environmental parameters and methylation variation among populations at those eight genes. A weak correlation was identified between pairwise DNA methylation dissimilarity among populations and pairwise F _ST based on 15 microsatellite loci, indicating weak effects of genetic drift or geographic distance on methylation. The weak correlation was primarily driven by two genes, GTIIBS and Nkef. However, single‐gene Mantel tests comparing methylation and pairwise F _ST were not significant after Bonferroni correction. Thus, population differences in DNA methylation are more likely related to unmeasured oceanic environmental conditions, local adaptation, and/or genetic drift. DNA methylation is an additional mechanism that contributes to among population variation, with potential influences on organism phenotype, adaptive potential, and population resilience.     

Environmental correlates of life-history variation in juvenile chinook salmon, Oncorhynchus tshawytscha (Walbaum)

Throughout its native North Pacific, the chinook salmon, Oncorhynchus tshawytscha (Walbaum), exists as twolife-history types that aredistinguished by the age at which juvenile salmon migrate to sea as smolts. 'Stream-type' chinook migrate seaward after I or more years of feeding in fresh water, whereas 'ocean-type' fish migrate to sea as newly emerged fry or after 2–3 months in fresh water. Stream-type chinook predominate in populations distant from the sea south of 56° N, and in both inland and coastal populations north of this point. By contrast, ocean-type chinook predominate in coastal populations south of 56° N, but are rare in populations in more northerly latitudes. Stream-type populations are associated with areas of low 'growth opportunity' (as measured by temperature and photoperiod regimes) and/or areas distant from the sea compared to ocean-type. Geographic variability in juvenile life history is suggested to result, in part, from environmental modulation of smolting timing via differences in growth opportunity among geo-graphic areas. In addition, differences in migration distance and temperature regime may result in selection for different sizes at migration among populations which, through differences in growth opportunity, might promote geographic variability in age at seaward migration.     

Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha)

Despite growing evidence for parasite-mediated selection on the vertebrate major histocompatibility complex (MHC), little is known about variation in the bacterial parasite community within and among host populations or its influence on MHC evolution. In this study, we characterize variation in the parasitic bacterial community associated with Chinook salmon ( Oncorhynchus tshawytscha ) fry in five populations in British Columbia (BC), Canada across 2 years, and examine whether bacterial infections are a potential source of selection on the MHC. We found an unprecedented diversity of bacteria infecting fry with a total of 55 unique bacteria identified. Bacterial infection rates varied from 9% to 29% among populations and there was a significant isolation by distance relationship in bacterial community phylogenetic similarity across the populations. Spatial variation in the frequency of infections and in the phylogenetic similarity of bacterial communities may result in differential parasite-mediated selection at the MHC across populations. Across all populations, we found evidence of a heterozygote advantage at the MHC class II, which may be a source of balancing selection on this locus. Interestingly, a co-inertia analysis indicated only susceptibility associations between a few of the MHC class I and II alleles and specific bacterial parasites; there was no evidence that any of the alleles provided resistance to the bacteria. Our results reveal a complex bacterial community infecting populations of a fish and underscore the importance of considering the role of multiple pathogens in the evolution of host adaptations.     

Chronic administration of fluoxetine alters locomotor behavior, but does not potentiate the locomotor stimulating effects of CRH in juvenile Chinook salmon (Oncorhynchus tshawytscha)

The present study investigated: 1) the behavioral effects of chronic administration of a serotonin uptake inhibitor (fluoxetine) in juvenile Chinook salmon, Oncorhynchus tshawytscha and, 2) whether chronic administration of fluoxetine alters the behavioral effects of corticotropin-releasing hormone (CRH). Chronic (20 day) treatment with fluoxetine decreased locomotor activity when compared to fish given long-term injections of saline. An intracerebroventricular (i.c.v.) injection of CRH had no effect on locomotor activity following a 20 day intraperitoneal treatment with either saline or fluoxetine. Chronic treatment with fluoxetine also increased the amount of time fish spent near the center of the tank. A similar increase was seen in fish given a chronic intraperitoneal (i.p.) series of saline followed by an acute i.c.v. injection of CRH. However, the effect was not additive when fish were given chronic i.p. injections of fluoxetine followed by an acute i.c.v. injection of CRH. These results provide evidence to support the hypothesis that the serotonergic system is involved in mediating locomotor activity and habitat choice in teleosts.     

Juvenile habitat partitioning and relative productivity in allochronically isolated sockeye salmon (Oncorhynchus nerka)

Allochronic divergence, like spatial isolation, may contribute to population diversity and adaptation, however the challenges for tracking habitat utilization in shared environments are far greater. Adult Klukshu River (Yukon, Canada) sockeye salmon, Oncorhynchus nerka, return as genetically distinct "early" and "late" runs. Early and late adult spawning populations (1999 and 2000) and their subsequent fry (sampled at 7 sites in 2000 and at 8 sites in 2001 throughout Klukshu Lake and River) were genotyped at eight microsatellite loci. Bayesian assignment was used to determine the spatial distribution of early versus late fry; although intermixed, the distribution of fry significantly differed in Klukshu Lake and in the Klukshu River in 2001, based on crosstab analyses. Late-run fry predominated in Klukshu Lake at all sites, while early-run fry were most common in the north and south of Klukshu Lake and in Klukshu River. Early-run spawners had significantly higher relative productivity (early life survival) than late-run fish (2.9 times more fry produced per early-run adult in 2000, and 9.2 times more in 2001). This study demonstrates spatial habitat partitioning and differences in the contribution of allochronically isolated populations to fry abundance, and highlights annual variability that likely contributes to recruitment variation.     

Dung‐associated arthropods influence foraging ecology and habitat selection in Black‐necked Cranes (Grus nigricollis) on the Qinghai–Tibet Plateau

Variation in grassland vegetation structure influences the habitat selection of insectivorous birds. This variation presents a trade‐off for insectivorous predators: Arthropod abundance increases with vegetation height and heterogeneity, but access to arthropod prey items decreases. In contrast, grazing by large herbivores reduces and homogenizes vegetation, decreasing total arthropod abundance and diversity. However, the presence of livestock dung may help counteract the overall reduction in invertebrates by increasing arthropods associated with dung. It is unclear, however, how the presence of arthropod prey in dung contributes to overall habitat selection for insectivorous birds or how dung‐associated arthropods affect trade‐offs between vegetation structure, arthropod abundance, and access to prey. To explore these relationships, we studied habitat selection of the Black‐necked Crane (Grus nigricollis), a large omnivorous bird that breeds on the Qinghai–Tibet Plateau. We assessed the relationships between habitat selection of cranes and vegetation structure, arthropod abundance, and the presence of yak dung. We found that Black‐necked Cranes disproportionately foraged in grassland patches with short sward height, low sward height heterogeneity, and high numbers of dry yak dung, despite these habitats having lower total arthropod abundance. Although total arthropod abundance is lower, these habitats are supplemented with dry yak dung, which are associated with coleopteran larvae, making dung pats an indicator of food resources for breeding Black‐necked Cranes. Coleopteran adults and larvae in yak dung appear to be an important factor influencing the habitat selection of Black‐necked Cranes and should be considered when assessing grassland foraging trade‐offs of insectivorous birds. This research provides new insights into the role of livestock dung in defining foraging habitats and resources for insectivorous predators.     

A latitudinal cline in the Chinook salmon (Oncorhynchus tshawytscha) Clock gene: evidence for selection on PolyQ length variants

A critical seasonal event for anadromous Chinook salmon (Oncorhynchus tshawytscha) is the time at which adults migrate from the ocean to breed in freshwater. We investigated whether allelic variation at the circadian rhythm genes, OtsClock1a and OtsClock1b, underlies genetic control of migration timing among 42 populations in North America. We identified eight length variants of the functionally important polyglutamine repeat motif (PolyQ) of OtsClock1b while OtsClock1a PolyQ was highly conserved. We found evidence of a latitudinal cline in average allele length and frequency of the two most common OtsClock1b alleles. The shorter 335 bp allele increases in frequency with decreasing latitude while the longer 359 bp allele increases in frequency at higher latitudes. Comparison to 13 microsatellite loci showed that 335 and 359 bp deviate significantly from neutral expectations. Furthermore, a hierarchical gene diversity analysis based on OtsClock1b PolyQ variation revealed that run timing explains 40.9 per cent of the overall genetic variance among populations. By contrast, an analysis based on 13 microsatellite loci showed that run timing explains only 13.2 per cent of the overall genetic variance. Our findings suggest that length polymorphisms in OtsClock1b PolyQ may be maintained by selection and reflect an adaptation to ecological factors correlated with latitude, such as the seasonally changing day length.     

Growth estimates from otolith increment widths of juvenile chinook salmon (Oncorhynchus tshawytscha) reared in changing environments

For otolith increments to provide useful estimates of fish growth, otolith growth must covary closely with somatic growth. We reared groups of juvenile chinook salmon ( Oncorhynchus tshawytscha Walbaum) for 70 days, changing ration or temperature during a 20-day treatment period. Restricted rations halted somatic growth, however increment widths decreased gradually; somatic growth was overestimated from increment width. Otolith growth followed changes in water temperature more closely than changes in ration, supporting a hypothesized effect of metabolic rate on otolith growth. Increment growth was only loosely coupled to fish growth rate, and may also be affected by past growth histories. For juvenile fish, increment widths may not be sensitive indicators of short-term changes in growing conditions.     

The effects of paternal reproductive tactic and rearing environment on juvenile variation in growth as mediated through aggression and foraging behaviours of Chinook salmon (Oncorhynchus tshawytscha)

In species with indeterminate growth, differential growth rates can lead to animals adopting alternative reproductive tactics such as sneak–guard phenotypes, which is partially predicted by variation in growth during the juvenile life‐history stage. To investigate sources of growth variation, we examined the independent and joint effects of paternal reproductive tactic (G) and rearing environment (E) on juvenile growth in Chinook salmon (Oncorhynchus tshawytscha), hypothesizing G and E effects are partially mediated through differences in behaviour such as aggressive interactions and resulting foraging behaviours. We created maternal half‐sibling families with one‐half of the female's eggs fertilized by the milt of a sneaker “jack” and the other half by a guarder “hooknose”. At the exogenous feeding stage, each split‐clutch family was then divided again and reared in a rationed diet or growth‐promotion diet environment for approximately 6 months, during which growth parameters were measured. Before saltwater transfer at 9 months of age, social interactions were observed in groups of six fish of various competitor origins. We found ration restricts growth rate and juvenile mass, and evidence of genetic effects on growth depensation, where jack‐sired individuals grew less uniformly over time. These growth‐related differences influenced an individual's level of aggression, with individuals raised on a restricted diet and those whose families experienced greatest growth being most aggressive. These individuals were more likely to feed than not and feed most often. Jack‐sired individuals were additionally aggressive in the absence of food, and when raised on a rationed diet outcompeted others to feed most. These results show how individuals may achieve higher growth rates via intrinsic (G) or induced (E) aggressive behavioural phenotypes, and eventually attain the threshold body size necessary during the saltwater phase to precociously sexually mature and adopt alternative reproductive phenotypes.