Size variability of juvenile Atlantic salmon: links to environmental conditions

Climate change models predict a 2 to 6° C increase in air temperature within the next 100 years in the Maritime Provinces of eastern Canada. Higher air temperatures are expected to contribute to increased water temperatures, alterations in stream flow conditions, and ultimately reductions in fish growth. Mean annual size-at-age of juvenile Atlantic salmon Salmo salar decreased in the Northwest Miramichi and Southwest Miramichi Rivers between 1971–1999. Lengths-at-age of juveniles were significantly correlated between the two rivers. For Atlantic salmon parr, stronger associations between inter-cohort fork length ( L _F) than intra-cohort L _F were observed, suggesting that environmental conditions in the current year of growth have the more significant effects on size of age 2 year parr than conditions encountered the previous year by age 1 year parr of the same cohort. Fork lengths of parr were significantly and negatively associated with spring air and water temperatures. In the Miramichi River, increases in air and water temperature as predicted from climate change models may adversely affect growth of juvenile Atlantic salmon parr, reducing the overall productivity of the Atlantic salmon populations in this region.     

The effects of prior residence on behavior and growth rates in juvenile Atlantic salmon (Salmo salar)

It is well documented that prior residence confers advantagesin territorial disputes, but its impact on other aspects ofbehavior and fitness is less understood. We tested how priorresidence influences the subsequent feeding behavior and growthperformance of dispersing Atlantic salmon fry (Salmo salar)using experimental manipulations of residence in a seminaturalstream tank. In replicated trials, groups of seven "primary"fish were released into the stream tank 3 days ahead of seven"secondary" fish. Standardized behavioral observations were madeon each fish over the following 14 days, after which all fishwere removed and measured. Primaries and secondaries were initiallythe same size and body condition and exhibited the same degreeof site fidelity. However, primaries darted higher into thewater column to intercept prey items, fed at a higher rate,and subsequently grew faster. Larger fish (in terms of body length)tended to be more dominant, and dominants grew faster than subordinates.However, there was no difference in dominance between primaries andsecondaries. These results suggest that the well-documentedadvantage of early-emerging salmon fry over late-emerging frycannot be completely attributed to intrinsic differences andthat the advantage is partly mediated via a prior residenceeffect. Furthermore, prior residents gain foraging advantageswithout necessarily becoming more dominant.     

Temperature, light intensity and plasma melatonin levels in juvenile Atlantic salmon

Plasma melatonin synthesis in juvenile Atlantic salmon Salmo salar decreased with increasing light intensity. Melatonin profiles reflected accurately the photoperiod under which the salmon were maintained. Groups maintained at 12°C showed significantly higher ( P < 0·01) levels of dark phase plasma melatonin compared with the groups maintained at 4°C.     

Influence of growth and temperature on strontium deposition in the otoliths of Atlantic salmon

Sr : Ca ratios measured in the otoliths of sea‐caged Atlantic salmon Salmo salar showed distinct seasonal peaks that were unrelated to water temperature and somatic growth, suggesting other factors have a greater influence on strontium deposition. Atlantic salmon remained in the sea‐cages for two seasons, or equivalent to two‐seawinter fish in the wild and were subjected to seasonally varying temperatures. Water temperature appeared to be inversely related to the Sr : Ca ratios, but this relationship was statistically not significant. Furthermore, water temperature could not explain the distinct increase in the strontium during the second year. The intensity of the Sr peaks increased in the second season while average winter water temperatures were consistent between years. Additionally, strontium deposition in the otoliths was unrelated to somatic growth. Somatic growth, as evidenced by circuli spacings on the scales, was largely invariant and therefore could not explain the observed peaks. Though not explicitly measured, the data are consistent with the notion that strontium deposition is a function of maturity state in Atlantic salmon.     

Oxygen consumption, ammonia excretion and protein use in response to thermal changes in juvenile Atlantic salmon Salmo salar

Experiments were designed to examine the effects of various temperature challenges on oxygen consumption and ammonia excretion rates and protein utilization in juvenile Atlantic salmon Salmo salar . Fish acclimated to 15° C were acutely and abruptly exposed to either 20 or 25° C for a period of 3 h. To simulate a more environmentally relevant temperature challenge, a third group of fish was exposed to a gradual increase in temperature from 15 to 20° C over a period of 3 h ( c. 1·7° C h⁻¹). Oxygen consumption and ammonia excretion rates were monitored before, during and after the temperature shift. From the ammonia excretion and oxygen consumption rates, protein utilization rates were calculated. Acute temperature changes (15–20° C or 15–25° C) caused large and immediate increases in the oxygen consumption rates. When the temperature was gradually changed ( i.e. 1·7° C h⁻¹), however, the rates of oxygen consumption and ammonia excretion were only marginally altered. When fish were exposed to warmer temperatures ( i.e. 15–20° C or 15–25° C) protein use generally remained at pre-exposure (15° C) levels. A rapid transfer back to 15° C (20–15° C or 25–15° C) generally increased protein use in S. salar . These results indicate that both the magnitude and the rate of temperature change are important in describing the physiological response in juvenile salmonids.     

Genetic variation in immune parameters and associations to survival in Atlantic salmon

Lysozyme activity, haemolytic activity, total level of IgM, and levels of antibodies against A-layer from Aeromonas salmonicida and O-antigen from Vibrio salmonicida , respectively, were determined in 77 full-sib groups of Atlantic salmon in order to evaluate their possible use as immune parameters for indirect selection to improve disease resistance. Fish from parallel full-sib groups had previously been challenged with Aeromonas salmonicida (causing furunculosis), Renibacterium salmoninarum (causing bacterial kidney disease, BKD) and Vibrio salmonicida (causing cold-water vibriosis). Heritabilities were estimated for each of the immune parameters and correlations between the least square means of the full-sib groups for the different immune parameters and survival rates in the parallel full-sib groups were determined. A significant genetic variation in lysozyme activity was found, as well as an apparent genetic association between low lysozyme activity and high survival rates. Low heritabilities and low univariate correlations with survival in the full-sib groups were estimated for all of the other immune parameters. An analysis of the multivariate associations between the full-sib mean values of the complete set of immune parameters, and survival rates in the parallel full-sib groups in each of the challenge tests, revealed that, at low levels of lysozyme activity and with low antibody titres against V. salmonicida O-antigen, increased IgM levels seemed to increase survival from furunculosis.     

Chondroid bone and secondary cartilage contribute to apical dentary growth in juvenile Atlantic salmon

The microstructure and tissue composition of the dentary bone in Atlantic salmon salmo salar parr were examined using a variety of histological and whole‐mount techniques. Proximally, the dentary is composed of typical cellular lamellar bone with Sharpey's fibres extending dorsally, proximally and ventrally. Meckel's cartilage is located medially through the entire length of the dentary, and degrades distally resulting in a short transitional zone between hyaline cartilage and connective tissue. At the distal tip of the dentary, isogenic clusters of chondrocytes of periosteal origin were observed secreting small amounts of pericellular cartilage matrix within the bone matrix. These characteristics are highly indicative of secondary chondrogenesis, and suggest that the apical part of the dentary bone in Atlantic salmon does not grow via 'pure' intramembranous ossification, but rather via a modified mode of periosteal ossification involving secondary cartilage and chondroid bone. Furthermore, the unusual mode of gender‐related dentary growth (kype formation) in adult male Atlantic salmon could be the continuation of a general mode of salmonid apical dentary growth.     

Behavioural influences on life-history variation in juvenile Atlantic salmon,Salmo salar

Synopsis Juvenile Atlantic salmon emigrate from the river in a given year as a consequence of a physiological decision influencing appetite and growth during the previous summer. The direction of the decision depends on developmental performance exceeding a genetically determined threshold at that time, and that performance is governed by environmental opportunity. The animal's foraging efficiency (ability to avoid predators, and to compete) determines how well that opportunity is used. Those fish which maintained relatively high growth after July preferred higher stream flows, and were more likely to hide than to flee from a predator. Predator vigilance reduced intake, and ability to discriminate edible particles. Early competitive ability depended on fierceness rather than size, and ultimate large size was a consequence of dominant status. Initial status among high ranking individuals (but not among low ones) predicted the likelihood of maintaining growth in late summer. Size by July was the better predictor for low ranked fish. The influence of high status on life-history variation depends on how much it suppresses the growth of those lower in the hierarchy. Invited review     

The influence of life-history strategy on lipid metabolism in overwintering juvenile Atlantic salmon

From November to May, the lipid mass in the viscera and carcass of juvenile Atlantic salmon Salmo salar that were undergoing smolt transformation prior to seaward migration ('early migrants') were significantly greater than those of their siblings that would delay migration for at least a further year. During winter (November-February), the depletion of lipid associated with the viscera was significantly greater in early migrants, whilst lipid depletion in the remaining carcass was greater in delayed migrants. Early migrants continued to deplete both lipid compartments in spring (February-May), whereas delayed migrants depleted visceral lipid but replenished carcass lipid over the same period. Fatty acid accumulation rates (a measure of storage lipid synthesis rates) were two to six times greater in visceral than in carcass lipid throughout the study, suggesting that lipid turnover is much more rapid in the viscera. There were no differences in fatty acid accumulation rates between migrant groups in November, despite the much lower food consumption rate of delayed migrants at that time, suggesting that these fish allocated a larger proportion of their nutritional resources to lipid synthesis. In the carcass lipid of early migrants, and in both the visceral and carcass lipid of delayed migrants, the fatty acid accumulation rate was negatively correlated with lipid mass. Fatty acid accumulation rates increased from November to February in both visceral and carcass lipid in the two migrant groups. The fatty acid accumulation rate in carcass lipid was significantly higher in delayed migrants than in early migrants in February, but not in May. These results support the hypothesis that life history strategies involving rapid growth will result in a relatively low allocation of resources to lipid reserves.     

Genetic changes in an Atlantic salmon population resulting from escaped juvenile farm salmon

The study was undertaken on three adjacent rivers in NW Ireland, on one of which an Atlantic salmon Salmo salar freshwater juvenile rearing unit is situated. Two markers which distinguished farm and wild populations were used. An Ava II-B RFLP in the ND1 region of mtDNA was at a frequency of 0.58 in the farm strain but absent in the wild populations. Allele E at minisatellite locus Ssa- A45/2/l was at a frequency of 0.91 in farm samples, but at a maximum of 0.41 in the populations in the two rivers adjacent to the one with the juvenile rearing unit. The farm strain showed a significant reduction in mean heterozygosity (0.281 ± 0.057), over three minisatellite loci examined, compared to wild samples (0.532 ± 0.063). The occurrence of farm genotypes and the independent occurrence of mtDNA and minisatellite markers in several parr samples from the river indicated that escaped juvenile salmon completed their life cycle, bred and interbred with native fish, upon their return to the river. Escaped fish homed accurately, as adults, to the site of escape, i.e. the area adjacent to the hatchery outflow in the upstream part of the river. Breeding of males in the lower part of the river was also indicated but this could have been due to mature male parr which had moved downstream. The return of adults of farm origin to the river to breed was indicated by the presence of the Ava II-B haplotype in adults netted in the estuary.     

Genetic studies on serum transferrins in Atlantic salmon

Published and unpublished data on genetic variation at the transferrin locus ( TF *) in Atlantic salmon from rivers in eastern North America sampled from 1968 to 1970 were reanalysed and compared with data for samples collected in 1998 from nine of the same rivers. Genetic differentiation among rivers was highly significant as was spatial differentiation among tributary samples within the Miramichi River system, the largest rivers studied. Comparison of allele frequencies in rivers also sampled in 1998 show no overall evidence of significant genetic change after 30 years, spanning 9 generations. The results strongly support the stability of the patterns of spatial genetic differentiation and support the occurrence in Atlantic salmon of reproductive isolation among rivers and among tributaries within large river systems.     

Monthly indices of the post-smolt growth of Atlantic salmon from the Drammen River, Norway

Indices of the monthly post-smolt growth of three maturity groups of Atlantic salmon Salmo salar from the Drammen River in Norway were examined. Scale samples were collected from 1983 to 2003, providing a retrospective growth history for 2854 individuals. Overall post-smolt growth of all three maturity groups decreased throughout the study period. When the post-smolt year was segmented into 8 monthly indices, there was a significant decline in growth during the fourth and fifth month, typically months of maximum growth. The pre-fishery abundance of one and two sea-winter fish from Norway also showed a decline throughout the study period and was positively correlated to the post-smolt growth of fish returning to the Drammen River. Freshwater growth was negatively correlated to the pre-fishery abundance, thus indicating that factors affecting post-smolt growth during the fourth and fifth months at sea may be responsible for declining return numbers in Norway.     

Genetic variation in Atlantic salmon, Salmo salar L., within the Tamar catchment in south-west England

Electrophoretic analysis of enzymes in 383 juvenile Atlantic salmon, Salmo salar L., within the Tamar catchment (south-west England) revealed significant genetic differences at the IDHP-3* locus between the three tributaries studied. Aspects of temporal and spatial variation, and management policy within catchments, are discussed.     

Time series covering up to four decades reveals major changes and drivers of marine growth and proportion of repeat spawners in an Atlantic salmon population

1. Wild Atlantic salmon populations have declined in many regions and are affected by diverse natural and anthropogenic factors. To facilitate management guidelines, precise knowledge of mechanisms driving population changes in demographics and life history traits is needed.
2. Our analyses were conducted on (a) age and growth data from scales of salmon caught by angling in the river Etneelva, Norway, covering smolt year classes from 1980 to 2018, (b) extensive sampling of the whole spawning run in the fish trap from 2013 onwards, and (c) time series of sea surface temperature, zooplankton biomass, and salmon lice infestation intensity.
3. Marine growth during the first year at sea displayed a distinct stepwise decline across the four decades. Simultaneously, the population shifted from predominantly 1SW to 2SW salmon, and the proportion of repeat spawners increased from 3 to 7%. The latter observation is most evident in females and likely due to decreased marine exploitation. Female repeat spawners tended to be less catchable than males by anglers.
4. Depending on the time period analyzed, marine growth rate during the first year at sea was both positively and negatively associated with sea surface temperature. Zooplankton biomass was positively associated with growth, while salmon lice infestation intensity was negatively associated with growth.
5. Collectively, these results are likely to be linked with both changes in oceanic conditions and harvest regimes. Our conflicting results regarding the influence of sea surface temperature on marine growth are likely to be caused by long‐term increases in temperature, which may have triggered (or coincided with) ecosystem shifts creating generally poorer growth conditions over time, but within shorter datasets warmer years gave generally higher growth. We encourage management authorities to expand the use of permanently monitored reference rivers with complete trapping facilities, like the river Etneelva, generating valuable long‐term data for future analyses.

     

Marine post-smolt growth and age at maturity of Atlantic salmon

The annual variation in sea-age of maturation for a hatchery dependent stock of Atlantic salmon was compared to variation in post-smolt growth as evidenced by circuli spacing patterns. The proportion of returns of 1-seawinter (1 SW) and 2 SW salmon and the fraction of the smolt year class or cohort that maturated as 1 SW fish, were compared to seasonal growth indices determined from circuli spacing on the scales of smolt class survivors returning as 1 SW and 2 SW spawners. Using image processing techniques, we extracted inter-circuli distances from scales from 2244 recaptured fish. Spacing data for the first year at sea were collected and then expressed as seasonal growth indices for the spring period, when post-smolts first enter the ocean; the summer, when growth appears maximal; and winter, when growth appears to be at a minimum. In general, circuli spacings were wider for 1 SW than for the 2 SW returns of the same smolt cohort. The 1 SW fraction was significantly and positively correlated with late summer growth, suggesting that growth during this season is pivotal in determining the proportion of a smolt class that matures early.     

Seasonal variation in trypsin activity in juvenile Atlantic salmon upper and lower modal groups

Juvenile salmon in their first year of growth showed a bimodal distribution of body lengths by December. For experimental purposes samples of fish from the upper 2% of body lengths were taken as representing the upper modal group (UMG), whilst fish from the bottom 5% of body lengths were taken to represent the lower modal group (LMG). The population of fish from which the samples were taken were fed ad libitum from December to July. During the winter months to March, neither group increased in weight. Growth resumed between March and July. The LMG fish had a very low food intake, as indicated by the relative weight of digesta in the stomach, in the winter months. However, following resumption of feeding, the relative weight of stomach digesta of the LMG fish exceeded that of the UMG fish between May and July. The activity of trypsin in the intestinal digesta followed a similar pattern, the LMG fish showing a higher trypsin activity in the spring months. Starvation of UMG fish for 5 days in winter resulted in accumulation of trypsin in the pancreatic tissues, whilst injection of the trypsin releasing hormone cholecystokinin (CCK) into starving UMG fish resulted in reduction of trypsin in the secretory tissues. CCK also caused reduction of trypsin in the pancreatic tissues of LMG fish, suggesting that the pancreas of this group is potentially fully functional during the winter period. Ultrastructure studies of the pancreatic acinar cells showed evidence for lower secretory activity in the LMG fish, as indicated by smaller numbers of zymogen granules, less well developed Golgi systems and a smaller number of active secreting cells. It appears that trypsin secretion by the pancreas in LMG fish is at a low level during the winter, in response to the reduced amounts of food passing through the gut, which is ultimately controlled by changes in food intake, lowered metabolic level and lowered appetite levels.     

Prey selection by experienced and naive juvenile Atlantic salmon

Both in foraging groups and in a sequential prey encounter context, learning had a visible effect on the pattern of selection for three live prey types ( Ecdyonurus larvae, Hydropsyche larvae, and Gammarus ) by juvenile Atlantic salmon Salmo salar . Compared to wild-caught fish, naive, hatchery-reared fish that had not been exposed to natural prey ate Hydropsyche larvae in a remarkably low proportion, and consumed a higher proportion of Gammarus. Ecdyonurus experienced a high and rather steady predation rate across the experience gradient, but after a short period of experience with live prey the consumption rate for Hydropsyche increased drastically, and that of Gammarus decreased, matching the selection pattern exhibited by wild fish. Individual fish offered prey in a sequential encounter context increased consumption rates of all the prey types as they gained experience, but the improvement was higher for the prey that were less consumed initially. Fish became more selective as they approached satiation, conforming to the prediction of optimal foraging theory that higher predator's energy requirements, as well as low food availability, result in reduced selectivity. The results also suggest that fish from distinct populations can differ in the degree of diet selectivity according to their energetic requirements for growth. The fast learning response of Atlantic salmon parr towards novel prey probably allows fish to maintain a high foraging efficiency when faced with frequent changes in the availability of different prey types.     

Genetic variation at enzyme loci in the southernmost European populations of Atlantic salmon

Genetic variation was studied at 8 allozyme loci in six severely endangered wild Spanish populations of Salmo salar located at the southernmost geographical limit of European Atlantic salmon. Low levels of variation were detected and no significant deviations from Hardy–Weinberg equilibrium were found.