Balancing risks and rewards of alternate strategies in the seaward extent, duration and timing of fjord use in contemporary anadromy of brown trout (Salmo trutta).

BACKGROUND: Anadromy comprises a successful life-cycle adaptation for salmonids, with marine migration providing improved feeding opportunities and thus improved growth. These rewards are balanced against costs from increased energy expenditure and mortality risk. Anthropogenic-induced environmental changes that reduce benefits and/or increase costs of migration e.g., aquaculture and hydropower, may therefore result in adaptations disfavouring anadromy. We tagged brown trout (Salmo trutta) smolts (N = 175) and veteran migrants (N = 342), from five adjacent riverine populations located in Sognefjorden, the longest Norwegian fjord-system supporting anadromous brown trout populations (209 km). Over four years, 138 acoustic telemetry receivers were deployed to track migrations of tagged individuals from freshwater and throughout Sognefjorden. Detected movements were used to fit migration models and multi-state mark-recapture models of survival and movement for each life-stage. Seaward migration distance was modelled to examine the fitness consequences from alternate migration strategies, with these models used to simulate the extent of fjord-use by individuals and accompanying growth, fecundity and survival consequences. We compared these findings with mark-recapture data collected prior to aquaculture and hydropower development. RESULTS: The telemetry data revealed that the outermost-fjord region was utilised by all populations albeit by few individuals. However, historical recaptures were located at a greater distance from the river mouth (87.7 ± 70.3 km), when compared to maximum migration distances of present-day counterparts (58.6 ± 54.9 km). River of origin influenced observed migratory behaviour and differential survival was estimated for each population and life-stage. The simulations based on telemetry-data models revealed a 30% and 23% difference in survival among populations for smolts and veteran migrants, respectively. At the individual-level, a long-distance migration strategy was rewarded with enhanced fecundity. However, the main contribution to population-level fecundity was overwhelmingly derived from middle-distance migrants, due to higher mortality rates and limited numbers of long-distant migrants. CONCLUSIONS: We conclude that present-day anadromy is precarious, but potential risk varies considerably between life-stages and populations, even within a single fjord system. Our findings suggest that selection for extended migration is under pressure, we therefore stress the importance of monitoring and management actions to secure genetic variation pertinent to preserve fitness gains of anadromy.

Plerocercoids of the cestode Diphyllobothrium ditremum in brown trout Salmo trutta: substantial increase in infection after establishment of European minnow Phoxinus phoxinus.

This study focuses on plerocercoids of the cestode Diphyllobothrium ditremum in brown trout Salmo trutta from the subalpine lake Øvre Heimdalsvatn in south-central Norway. Salmo trutta was the only fish species in this lake until European minnow Phoxinus phoxinus was registered in 1969. The P. phoxinus population increased substantially in the following years. In contrast with the 1969-1972 period, when plerocercoids of D. ditremum were practically absent in S. trutta, there was a high prevalence and intensity of infection in the 2013 S. trutta samples. Because the life cycle of D. ditremum involves two larval stages, in copepods and salmonids and mature worms in piscivorous birds, such as mergansers and loons, a change in feeding ecology of S. trutta or changes in population densities of copepods, fish or birds might have influenced the infection pattern. No relationships between D. ditremum infection and muscle-tissue δ15 N signature or Hg concentration were found, indicating that infection is not a result of piscivory or cannibalism. Furthermore, consumption of copepods by S. trutta during summer and autumn was low. On the other hand, the number of piscivorous birds has increased, probably due to the presence of P. phoxinus as a new and numerous prey. An increased number of final D. ditremum hosts may have produced a higher output of cestode eggs, resulting in more infected copepods that in turn are consumed by S. trutta. Indirectly, P. phoxinus may therefore have caused the observed increased infection in S. trutta and thereby imposed further negative effects on S. trutta in high mountain areas.

Small larvae in large rivers: observations on downstream movement of European grayling Thymallus thymallus during early life stages.

Behaviour of early life stages of the salmonid European grayling Thymallus thymallus was investigated by assessing the timing of larval downstream movement from spawning areas, the depth at which larvae moved and the distribution of juvenile fish during summer in two large connected river systems in Norway. Trapping of larvae moving downstream and electrofishing surveys revealed that T. thymallus larvae emerging from the spawning gravel moved downstream predominantly during the night, despite light levels sufficient for orientation in the high-latitude study area. Larvae moved in the water mostly at the bottom layer close to the substratum, while drifting debris was caught in all layers of the water column. Few young-of-the-year still resided close to the spawning areas in autumn, suggesting large-scale movement (several km). Together, these observations show that there may be a deliberate, active component to downstream movement of T. thymallus during early life stages. This research signifies the importance of longitudinal connectivity for T. thymallus in Nordic large river systems. Human alterations of flow regimes and the construction of reservoirs for hydropower may not only affect the movement of adult fish, but may already interfere with active movement behaviour of fish during early life stages.

Seawater tolerance and post-smolt migration of wild Atlantic salmon Salmo salar × brown trout S. trutta hybrid smolts.

High levels of hybridization between Atlantic salmon Salmo salar and brown trout Salmo trutta have been reported in the River Driva. This study presents the underlying mechanisms of development of seawater (SW) tolerance and marine migration pattern for S. salar×S. trutta hybrids. Migrating S. salar×S. trutta hybrid smolts caught in the River Driva, Norway (a river containing Gyrodactylus salaris), displayed freshwater (FW) gill Na(+), K(+) -ATPase (NKA) activity levels of 11·8 µmol ADP mg protein h(-1), which were equal to or higher than activity levels observed in S. salar and S. trutta smolts. Following 4 days of SW exposure (salinity 32·3), enzyme activity remained high and plasma ion levels were maintained within the normal physiological range observed in S. salar smolts, indicating no signs of ion perturbations in S. salar×S. trutta hybrids. SW exposure induced an increase in NKA α1b-subunit mRNA levels with a concurrent decrease in α1a levels. Salmo salar×S. trutta post-smolts migrated rapidly through the fjord system, with increasing speed with distance from the river, as is often seen in S. salar smolts. The present findings suggest that S. salar×S. trutta smolts, as judged by the activity and transcription of the NKA system, regulation of plasma ion levels and migration speed more closely resemble S. salar than S. trutta.

Effects of production intensity and production strategies in commercial Atlantic salmon smolt (Salmo salar L.) production on subsequent performance in the early sea stage.

A data set from commercial Atlantic salmon (Salmo salar L.) producers on production intensity and production strategies in smolt tanks (N = 63-94) was obtained during 1999-2006. The effects of production intensity on subsequent fish mortality and growth during the early sea phase (90 days) were examined by principal component analysis and subsequent generalized linear model analysis. Levels of accumulated metabolites (CO(2), total ammonia nitrogen and NH(3)), and information provided by producers (production density (kg fish m(3-1)), specific water use (l kg fish(-1) min(-1)) and oxygen drop (mg l(-1)) from tank inlet to tank outlet), were used as predictor variables. In addition, several other welfare relevant variables such as disease history, temperature during freshwater and sea stage; season (S1) or off-season (S0) smolt production; and the use of seawater addition during the freshwater stage were analyzed. No strong intensity effects on mortality or growth were found. CO(2) levels alone (P < 0.001, R(2) = 0.16), and in combination with specific water use (R(2) = 0.20), had the strongest effect on mortality. In both cases, mortality decreased with increasing density. For growth, the intensity model with the most support (R(2) = 0.17) was O(2) drop, density and their interaction effects, resulting in the best growth at low and high intensity, and poorer growth at intermediate levels. Documented viral disease outbreaks (infectious pancreatic necrosis and two cases of pancreas disease) in the sea phase resulted in significantly higher mortalities at 90 days compared with undiagnosed smolt groups, although mortalities were highly variable in both categories. The temperature difference between the freshwater stage and seawater had a small, but significant, effect on growth with the best growth in groups stocked to warmer seawater (P = 0.04, R(2) = 0.06). S0 and S1 smolt groups did not differ significantly in growth, but the mortality was significantly (P = 0.02) higher in S1 groups. Seawater addition as a categorical variable had no significant effects, but when analyzed within the seawater addition group, intermediate salinities (15-25 ppt) gave the best results on growth (p = 0.04, R(2) = 0.15). Production intensity had small explanatory power on subsequent seawater performance in the analyzed smolt groups. If anything, the analysis shows a beneficial effect of intensive production strategies on subsequent performance. Analysis of the various production strategies indicates better survival of S0 compared with S1 smolt groups, improved growth when stocked in seawater warmer than freshwater, and a negative effect of viral disease outbreaks on survival. The results clearly demonstrate the difficulty of extrapolating results from experimental work on fish welfare and production intensity variables to commercial production. On the other hand, the presented results may simply demonstrate that the traditional fish welfare criteria growth and mortality may not suffice to evaluate welfare consequences of suboptimal water quality or production strategies in the aquaculture industry.

Strong gene flow and lack of stable population structure in the face of rapid adaptation to local temperature in a spring-spawning salmonid, the European grayling (Thymallus thymallus).

Gene flow has the potential to both constrain and facilitate adaptation to local environmental conditions. The early stages of population divergence can be unstable because of fluctuating levels of gene flow. Investigating temporal variation in gene flow during the initial stages of population divergence can therefore provide insights to the role of gene flow in adaptive evolution. Since the recent colonization of Lake Lesjaskogsvatnet in Norway by European grayling (Thymallus thymallus), local populations have been established in over 20 tributaries. Multiple founder events appear to have resulted in reduced neutral variation. Nevertheless, there is evidence for local adaptation in early life-history traits to different temperature regimes. In this study, microsatellite data from almost a decade of sampling were assessed to infer population structuring and its temporal stability. Several alternative analyses indicated that spatial variation explained 2-3 times more of the divergence in the system than temporal variation. Over all samples and years, there was a significant correlation between genetic and geographic distance. However, decomposed pairwise regression analysis revealed differing patterns of genetic structure among local populations and indicated that migration outweighs genetic drift in the majority of populations. In addition, isolation by distance was observable in only three of the six years, and signals of population bottlenecks were observed in the majority of samples. Combined, the results suggest that habitat-specific adaptation in this system has preceded the development of consistent population substructuring in the face of high levels of gene flow from divergent environments.

Sibling-size variation in brown trout Salmo trutta in relation to egg size and stream size.

Sibling-size variation (SSV), estimated as the coefficient of variation of egg size, was investigated for 13 populations of brown trout Salmo trutta. SSV was negatively correlated with mean egg size both at the population and individual levels. After correction for the effect of mean egg size, SSV was also negatively correlated with stream size. These results provide new information about how salmonid SSV can vary at different ecological scales (individual, population and region). The results are discussed in light of competing theories for explaining SSV: (1) the passive effect hypothesis, stating that egg size variation follows passively from selection on egg size and (2) the bet-hedging hypothesis, stating that high SSV is adaptive in unpredictable environments.

A century of life-history evolution in grayling.

Synchronic and allochronic data sets consisting of phenotypic values of various life-history traits from five grayling Thymallus thymallus populations with common ancestors were analysed for the purpose of estimating evolution and divergence rates. The synchronic data contained both juvenile and adult traits from populations that have been segregated for 44-88 years (9-22 generations). The allochronic time series contained growth- and maturation data spanning 95 years (16 generations). Estimated evolution and divergence rates were high compared with other life-history studies on the same temporal scale (0.002-1.008 haldanes, 10-30, 500 darwins). The divergence of adult traits were most probably caused by differential mortalities induced by variation in fishing intensity. For the population with allochronic data, 48 years (eight generations) of intense and consistent size-selective gill-net fishing resulted in a constant reduction in age (-0.33 years pr 10 year) and length (-18mm pr 10 year) at maturity. Length-at-age for ages one to five also decreased during the same period. When gill-net fishing was relaxed, age and length at maturity and length-at-age increased. Divergence rates for juvenile traits derived from a common-garden experiment were high, and standardized selection differentials (s') were high, especially for yolk-sac volume (s' = 2.6). We also document that low divergence rates for juvenile traits were lower between populations having similar spawning/nursery habitats (running water) than populations having relatively different habitats (running water v.s. still water). We suggest that the major part of the observed phenotypic divergence is mostly due to adaptive evolution, although microsatellite data indicate that genetic drift also has occurred.

Genetic lineages and postglacial colonization of grayling (Thymallus thymallus, Salmonidae) in Europe, as revealed by mitochondrial DNA analyses.

In stark contrast to other species within the Salmonidae family, phylogeographic information on European grayling, Thymallus thymallus, is virtually nonexistent. In this paper, we utilized mitochondrial DNA polymerase chain reaction-restriction fragment length polymorphism (mtDNA PCR-RFLP) and sequence variation to infer the postglacial dispersal routes of T. thymallus into and within northern Europe, and to locate geographically, potential evolutionarily distinct populations. Mitochondrial analyses revealed a total of 27 T. thymallus haplotypes which clustered into three distinct lineages. Average pairwise interlineage divergence was four and nine times higher than average intralineage divergence for RFLP and sequence data, respectively. Two European grayling individuals from the easternmost sample in Russia exhibited haplotypes more genetically diverged from any T. thymallus haplotype than T. arcticus haplotype, and suggested that hybridization/introgression zone of these two sister species may extend much further west than previously thought. Geographic division of the lineages was generally very clear with northern Europe comprising of two genetically differentiated areas: (i) Finland, Estonia and north-western Russia; and (ii) central Germany, Poland and western Fennoscandia. Average interpopulation divergence in North European T. thymallus was 10 times higher than that observed in a recent mtDNA study of North American T. arcticus. We conclude that (i) North European T. thymallus populations have survived dramatic Pleistocene temperature oscillations and originate from ancient eastern and central European refugia; (ii) genetic divergence of population groups within northern Europe is substantial and geographically distinct; and (iii) the remainder of Europe harbours additional differentiated assemblages that likely descend from a Danubian refugium. These findings should provide useful information for developing appropriate conservation strategies for European grayling and exemplify a case with a clear need for multinational co-operation for managing and conserving biodiversity.

Permanent impairment in the feeding behavior of grayling (Thymallus thymallus) exposed to methylmercury during embryogenesis.

Embryos of grayling (Thymallus thymallus) were exposed to different concentrations of methylmercury (0.16, 0.8, 4.0 and 20 micrograms Hg l-1) during the first 10 days of development. The exposure resulted in body concentrations in the newly hatched fry of 0.09, 0.27, 0.63 and 3.80 micrograms Hg g-1 wet wt., respectively. A control group had a body concentration of 0.01 microgram Hg g-1. Morphological disturbances were only found in the highest exposure group. Three years later, at a size of 13.8 +/- 0.8 cm, the different groups were tested for sublethal toxicant effects on foraging behavior. In the first series of experiments we tested the foraging efficiency of the fish when kept alone for 5 min in small flow-through aquariums. In the second series of experiments we tested the competitive ability of eight individuals from an exposed group vs. eight individuals from a control group when kept together for 30 min in a 300-1 aquarium. In both experiments live Dapnia magna were used as prey. We found impaired feeding efficiencies and reduced competitive abilities in grayling from the exposed groups which as yolk-fry had Hg concentrations of 0.27 microgram g-1 or more. In the foraging efficiency experiments these groups were 15-24% less efficient as compared to the control group. In the competitive ability experiments the control group caught two to six times as many preys as these exposed groups. Such harmful body concentrations of Hg (> 0.27 microgram g-1) may be found in eggs from piscivorous fishes in lakes receiving diffuse atmospheric depositions of mercury. We suggest such concentrations may have ecological consequences by reducing the fitness of the affected populations.