Anadromy and the marine migrations of Pacific salmon and trout: Rounsefell revisited

Anadromy is a defining trait in salmonid fishes but it is expressed to different extents among the species in the family, as reviewed in a classic paper by Rounsefell (1958). The present paper re-examines the subject, assessing the degree of anadromy within the genus Oncorhynchus, using Rounsefell’s six criteria: extent of migrations at sea, duration of stay at sea, state of maturity attained at sea, spawning habits and habitats, post-spawning mortality, and occurrence of freshwater forms of the species. The genus ranges from pink salmon (O. gorbuscha), the most fully anadromous species in the family, to entirely non-anadromous species closely related to rainbow trout (O. mykiss), including Mexican golden trout (O. chrysogaster), Gila and Apache trout (O. gilae), and sub-species of cutthroat trout (O. clarki). This paper provides updated information on anadromy and marine migration patterns, emphasizing the iteroparous species, cutthroat (O. clarki) and rainbow (O. mykiss) trout. These two species display widely ranging patterns of anadromy, including truly “landlocked” populations and residents with easy access to the sea. Anadromous rainbow trout (known as steelhead) populations also vary greatly in their distribution at sea, incidence of repeat spawning, and associated traits. We conclude, as did Rounsefell, that anadromy is not a single trait with two conditions (anadromous or non-anadromous). Rather, it reflects a suite of life history traits that are expressed as points along continua for each species and population. Further research is needed in the marine ecology of all species but especially trout, as they are less well known but apparently more variable in patterns of anadromy and life history than salmon species.     

Natural Colonization and Establishment of a Chinook Salmon, <Emphasis Type="Italic">Oncorhynchus tshawytscha</Emphasis>, Population in the Santa Cruz River,an Atlantic Basin of Patagonia

Synopsis We report the finding of an established population of exotic Chinook salmon spawning in headwaters of the Santa Cruz River system (Argentina), the first for this species in an Atlantic basin of South America. Spawning takes place in the Caterina River, a small tributary of Lake Argentino, located 488.5 km from the ocean. Anadromy was verified by correspondence of N and C stable isotope ratios with those of fish captured by bottom-trawlers in the ocean and those of anadromous rainbow trout from the same river basin. The scale patterns of most fish examined were consistent with a stream-type life cycle (i.e., seaward migration by juveniles after a full year in fresh water). Two potential origins were identified for this population: in situ introductions of fish imported directly from the USA in the early 20th century or fish from two ranching experiments conducted in southern Chile during the 1980s. In the latter case, colonization would have proceeded through the Strait of Magellan, helped by prevailing eastward currents.     

Retention of a chromosomal inversion from an anadromous ancestor provides the genetic basis for alternative freshwater ecotypes in rainbow trout

Migratory behaviour patterns in animals are controlled by a complex genetic architecture. Rainbow trout (Oncorhynchus mykiss) is a salmonid fish that spawns in streams but exhibits three primary life history pathways: stream‐resident (fluvial), lake‐migrant (adfluvial) and ocean‐migrant (anadromous). Previous studies examining fluvial and anadromous O. mykiss have identified several genes associated with life history divergence including the presence of an inversion complex within chromosome 5 (Omy05) that appears to maintain a suite of linked genes controlling migratory behaviour. However, adfluvial trout are migratory without being anadromous, and the genetic basis for this life history has not been investigated from evolutionary perspectives. We sampled wild, native nonanadromous rainbow trout occupying connected stream and lake habitats in a southwest Alaskan watershed to determine whether these fish exhibit genetic divergence between fluvial and adfluvial ecotypes, and whether that divergence parallels that documented in fluvial and anadromous O. mykiss. Data from restriction site‐associated DNA (RAD) sequencing revealed an association between frequencies of both the Omy05 inversion complex and other single nucleotide polymorphisms (SNPs) with habitat type (stream or lake), supporting the genetic divergence of fluvial and adfluvial individuals in sympatry. The presence of a genetic basis for migration into lakes, analogous to that documented for anadromy, indicates that the adfluvial ecotype must be recognized separately from the fluvial form of O. mykiss even though neither is anadromous. These results highlight the genetic architecture underlying migration and the importance of chromosomal inversions in promoting and sustaining intraspecific diversity.     

Experimental sea ranching of brook trout, Salvelinus fontinalis Mitchill

An experiment to induce anadromy in a population of wild brook trout, Salvelinus fontinalis , was conducted near Sept-Iles, Quebec, in 1978–1979. Brook trout were captured from the Matamek River, tagged and transported to the Matamek River estuary during late spring and early summer, and allowed free movement between an impassable waterfall 0.7 km upstream and the sea. Fish were recaptured in autumn as they returned to fresh water. Over two years, 34.0% of the released fish were recaptured. Best returns were in the 2+ and 3+ age classes with 38.0 and 62.1% recaptured, respectively. Straying of transplanted fish appeared to be <1%. All age classes included sea run brook trout (sea trout) but the largest percentages of sea trout occurred in older fish. Growth was better in sea trout than in fish which did not develop anadromy, presumably a function of an increased food supply at sea. Severe tagging effects stunted growth and probably suppressed anadromy, especially among younger fish. Sexual characteristics of recaptured fish indicated suppressed maturation of gonads in sea trout compared to fish remaining in fresh water and there was a shift to a larger percentage of females in the sea trout. Comparisons between our results and data on other anadromous Salvelinus species underscore the potential for sea-ranching of trout and char as a moderate effort, high yield aquaculture technique.     

First summer growth predetermined in anadromous and resident brook charr

Early growth of wild, anadromous and non-anadromous (resident) brook charr Salvelinus fontinalis was compared under controlled laboratory conditions. Offspring were collected as they emerged from natural redds in the Miramichi River, New Brunswick, Canada. Anadromous offspring were initially longer and heavier than residents. Anadromous offspring had lower specific growth rates during their first 2 months post-emergence, but surpassed residents by the third month. Consequently, anadromous offspring remained larger at the end of 3 months and it is concluded that they had a predetermined, maternal and genetic advantage related to body size, rather than an environmentally determined advantage during their first summer of growth. Other studies hypothesize that juvenile development affects life-history strategy adopted as adults, which suggests anadromy in this population may be, at least in part, predetermined by maternal and genetic effects.     

Post-spawn migrations of hatchery-origin Oncorhynchus mykiss kelts in the Central Valley of California

We used acoustic telemetry to study the post-spawn movement of Oncorhynchus mykiss kelts released in April 2005 and 2006 from the Coleman National Fish Hatchery, Anderson, CA. Following release, O. mykiss kelts demonstrated both anadromous and non-anadromous life histories, with some fish alternating life history strategies between years. Anadromy was most common, characterized by a short-term residence near the release site, followed by sustained downstream emigration once initiated. O. mykiss kelts demonstrating anadromy arrived at the Golden Gate Bridge from April to mid-July. Repeat spawning migrations of anadromous O. mykiss kelts began from late-September through October of the year of release. High fidelity back to Battle Creek was observed, occurring from late-September through November. While most O. mykiss kelts were anadromous, at least 10 % remained in freshwater, or residualized. O. mykiss kelts that residualized demonstrated two distinct patterns of movement: 1) residency near the release location, and 2) potamodromy. Overall survival was high with 36 % and 48 % of O. mykiss kelts released making a repeat spawning migration and demonstrating iteroparity in 2005 and 2006, respectively. Increase in body lengths of O. mykiss kelts that returned to the Coleman NFH were significantly greater for anadromous fish, compared to fish that residualized, but survival was higher for fish that residualized. Release of hatchery O. mykiss kelts could result in both positive and negative genetic and ecological effects to hatchery- and naturally-producing salmonids. We believe the benefits of releasing O. mykiss kelts at the Coleman NFH, including increased numbers and size of fish in the recreational fishery and genetic and demographic benefits to the hatchery brood stock outweigh the limited risk to natural populations that would result from predation and competition of the relatively small number of O. mykiss kelts that resided in fresh water.     

Effective population size of steelhead trout: influence of variance in reproductive success, hatchery programs, and genetic compensation between life-history forms

The effective population size is influenced by many biological factors in natural populations. To evaluate their relative importance, we estimated the effective number of breeders per year (Nb) and effective population size per generation (Ne) in anadromous steelhead trout (Oncorhynchus mykiss) in the Hood River, Oregon (USA). Using demographic data and genetic parentage analysis on an almost complete sample of all adults that returned to the river over 15 years (>15,000 individuals), we estimated Nb for 13 run years and Ne for three entire generations. The results are as follows: (i) the ratio of Ne to the estimated census population size (N) was 0.17-0.40, with large variance in reproductive success among individuals being the primary cause of the reduction in Ne/N; (ii) fish from a traditional hatchery program (Htrad: nonlocal, multiple generations in a hatchery) had negative effects on Nb, not only by reducing mean reproductive success but also by increasing variance in reproductive success among breeding parents, whereas no sign of such effects was found in fish from supplementation hatchery programs (Hsupp: local, single generation in a hatchery); and (iii) Nb was relatively stable among run years, despite the widely fluctuating annual run sizes of anadromous adults. We found high levels of reproductive contribution of nonanadromous parents to anadromous offspring when anadromous run size is small, suggesting a genetic compensation between life-history forms (anadromous and nonanadromous). This is the first study showing that reproductive interaction between different life-history forms can buffer the genetic impact of fluctuating census size on Ne.     

Inter-Tributary Movements by Resident Salmonids across a Boreal Riverscape

Stream-dwelling fishes inhabit river networks where resources are distributed heterogeneously across space and time. Current theory emphasizes that fishes often perform large-scale movements among habitat patches for reproduction and seeking refugia, but assumes that fish are relatively sedentary during growth phases of their life cycle. Using stationary passive integrated transponder (PIT)-tag antennas and snorkel surveys, we assessed the individual and population level movement patterns of two species of fish across a network of tributaries within the Wood River basin in southwestern Alaska where summer foraging opportunities vary substantially among streams, seasons, and years. Across two years, Arctic grayling (Thymallus arcticus) and rainbow trout (Oncorhynchus mykiss) exhibited kilometer-scale movements among streams during the summer growing season. Although we monitored movements at a small fraction of all tributaries used by grayling and rainbow trout, approximately 50% of individuals moved among two or more streams separated by at least 7 km within a single summer. Movements were concentrated in June and July, and subsided by early August. The decline in movements coincided with spawning by anadromous sockeye salmon, which offer a high-quality resource pulse of food to resident species. Inter-stream movements may represent prospecting behavior as individuals seek out the most profitable foraging opportunities that are patchily distributed across space and time. Our results highlight that large-scale movements may not only be necessary for individuals to fulfill their life-cycle, but also to exploit heterogeneously spaced trophic resources. Therefore, habitat fragmentation and homogenization may have strong, but currently undescribed, ecological effects on the access to critical food resources in stream-dwelling fish populations.     

Stable isotope profiles of partially migratory salmonid populations in Atlantic rivers of Patagonia

In the present study, profiles of stable isotope composition were characterized for two species with partially migratory populations in rivers along the latitudinal gradient of Patagonia, brown trout Salmo trutta and rainbow trout Oncorhynchus mykiss . The effects of factors ( e.g. ontogeny of fishes, location, species and fasting) that may influence the stable isotope analysis (SIA) were evaluated, as was SIA evaluated as a tool to assign individual fish to their corresponding ecotype. Anadromous fishes exhibited enriched δ¹⁵N (15·2 ± 1·0‰; mean ± s . d .) and δ¹³C (−19·2 ± 1·3‰) relative to resident fishes'δ¹⁵N (8·8 ± 1·1‰) and δ¹³C (−23·2 ± 2·5‰). For both species, the difference in δ¹⁵N was larger between resident (range 6·8–10·7‰) and anadromous (range 14·3–17·8‰) fishes than that in δ¹³C. Values of δ¹³C, while not as dramatically contrasting in rainbow trout, provided a powerful anadromy marker for brown trout in the region. Increases were found in both δ¹⁵N and δ¹³C during the spawning migration of anadromous rainbow trout, most likely due to fasting. Differences in stable isotopes between location, size and species were found, suggesting different stable isotopes base levels in freshwater environments and different trophic levels and feeding location of anadromous populations. The SIA was demonstrated as a powerful tool for ecotype discrimination in Patagonian Rivers, overriding any effect of sampling location, size or species.     

A genetically distinct wild redband trout (<Emphasis Type="Italic">Oncorhynchus mykiss gairdneri</Emphasis>) population in Crane Prairie Reservoir,Oregon, persists despite extensive stocking of hatchery rainbow trout (<Emphasis Type="Italic">O. m. irideus</Emphasis>)

Crane Prairie Reservoir in the upper Deschutes River Basin has historically supported a wild population of migratory Deschutes River redband trout. Owing to its status as a premier destination for recreational angling in Oregon, the reservoir has been stocked with domesticated hatchery rainbow trout since 1955. In recent years the wild redband trout population has experienced a substantial decline. Effects on productivity related to genetic interaction with naturally spawning hatchery-origin fish (fitness risks) have not been determined. The species Oncorhynchus mykiss has been characterized with substantial genetic diversity throughout the Deschutes River Basin that further heightens the challenge of identifying specific conservation needs of wild populations. A conservation plan for Crane Prairie wild redband trout requires a better understanding of the natural reproductive success of out-of-basin hatchery trout in the reservoir tributaries, and the similarity between Crane Prairie redband trout with other extant redband trout populations in the basin. Using a suite of 17 microsatellite nuclear DNA markers, we evaluated the genetic structure among Crane Prairie Reservoir redband trout, hatchery rainbow trout, and two adjacent populations of redband trout from within the Upper Deschutes River Basin. We observed significant heterogeneity between the hatchery and wild Crane Prairie populations that may reflect differences in life histories, differential productivity and assortative mating. The genetic distinctions observed among the three redband trout populations suggest restricted gene flow and genetic drift within the upper basin. Temporally stratified sampling and larger numbers of samples will be necessary to confirm these conclusions.     

Does life-history variability in salmonids affect habitat use by juveniles? A comparison among streams open and closed to anadromy

1. Migratory and resident forms of salmonids coexist in many river systems. Although such coexistence is widespread, little is known about its ecological basis and no studies have compared the habitat use of premigratory juveniles and residents. 2. We employed a comparative approach to explore the differential habitat use of juvenile anadromous and resident brook trout. This required the investigation of habitat use in streams closed to anadromy, containing only resident brook trout Salvelinus fontinalis ('resident-only' streams) and streams open to anadromy, containing coexisting Atlantic salmon Salmo salar and anadromous and resident brook trout ('migrant-resident' streams). 3. We demonstrate that fast habitats (riffles) are occupied more frequently in streams with migratory brook trout relative to riffle habitats of streams with only resident brook trout. In contrast, occupation of slow current velocities (pools) was observed in both migrant-resident and resident-only streams as both stream types contain resident brook trout. The net effect is a wider distribution of occupied habitats (pool and riffles) in migrant-resident streams relative to resident-only streams, resulting in few, if any, unused habitats. 4. These results are consistent with previously reported bioenergetic, morphological and stable isotope differences observed between anadromous and resident brook trout. 5. Our findings suggest that a link exists between juvenile habitat use, metabolic costs and life-history strategies.     

Hypoosmoregulation in an anadromous teleost: influence of sex and maturation

Salinity tolerance and hypoosmoregulatory ability of anadromous brook trout (Salvelinus fontinalis) were investigated in relation to sex and state of maturation. Seawater survival of mature males was significantly poorer than that of females or immature males. Lowered salinity tolerance of adult males became acute during the autumn photoperiod (normal spawning period) when the gonadosomatic index was high. Plasma [Cl-], [Mg2+], osmolarity and hematocrit were significantly higher in mature males after transfer to seawater, relative to mature females. It is postulated that reduced adult male hypoosmoregulatory ability explains skewed sex ratios in anadromous brook trout populations and may limit the extent of brook trout anadromy.     

Variation of vertebral number in juvenile Oncorhynchus mykiss in relation to upstream distance from the ocean

Vertebral counts in fishes are set early in development by a complex interaction of genetic and environmental factors. Recently, R. M. McDowall showed that vertebral counts can differ between diadromous and non-diadromous galaxiids, and suggested similar life history-based variation might also occur in the closely related Salmonidae. We examined variation in vertebral counts of juvenile rainbow trout, Oncorhynchus mykiss, from within a single large basin where anadromous and non-anadromous forms co-occur. Juveniles were collected at 29 sites within the Klamath River basin using a nested sampling design. Mean vertebral counts varied among regions, among complexes within regions, and among sites within complexes. Regression showed that mean vertebral counts decreased with increasing distance from the ocean. This decrease could not be explained by differences in temperature within the basin during early development. However, the decrease is consistent with the expectation that non-anadromous forms have fewer vertebrae and are more common at sites distant from the ocean, and suggests that further study of the relationship between vertebral counts and life history form in O. mykiss is warranted.

Maintenance of a small anadromous subpopulation of brown trout (Salmo trutta L.) by straying

1. Microsatellite and isozyme loci variation were used to study structure and dynamics of a brown trout (Salmo trutta) population heavily affected by damming. The downstream area accessible for spawning was drastically reduced to a stream 1 km long influenced by regulated discharge. 2. Stocking of hatchery‐reared juveniles failed and the population is entirely supported by anadromous adults from neighbouring populations. 3. Temporal genetic stability is reported here. Some punctual between‐river genetic differences are likely because of different contribution from each neighbouring river through years. 4. High anadromy‐mediated gene flow produces a lack of genetic substructure in the region. The role of anadromous brown trout on maintenance of endangered small populations is emphasised.     

Who are the missing parents? Grandparentage analysis identifies multiple sources of gene flow into a wild population

In order to increase the size of declining salmonid populations, supplementation programmes intentionally release fish raised in hatcheries into the wild. Because hatchery-born fish often have lower fitness than wild-born fish, estimating rates of gene flow from hatcheries into wild populations is essential for predicting the fitness cost to wild populations. Steelhead trout (Oncorhynchus mykiss) have both freshwater resident and anadromous (ocean-going) life history forms, known as rainbow trout and steelhead, respectively. Juvenile hatchery steelhead that 'residualize' (become residents rather than go to sea as intended) provide a previously unmeasured route for gene flow from hatchery into wild populations. We apply a combination of parentage and grandparentage methods to a three-generation pedigree of steelhead from the Hood River, Oregon, to identify the missing parents of anadromous fish. For fish with only one anadromous parent, 83% were identified as having a resident father while 17% were identified as having a resident mother. Additionally, we documented that resident hatchery males produced more offspring with wild anadromous females than with hatchery anadromous females. One explanation is the high fitness cost associated with matings between two hatchery fish. After accounting for all of the possible matings involving steelhead, we find that only 1% of steelhead genes come from residualized hatchery fish, while 20% of steelhead genes come from wild residents. A further 23% of anadromous steelhead genes come from matings between two resident parents. If these matings mirror the proportion of matings between residualized hatchery fish and anadromous partners, then closer to 40% of all steelhead genes come from wild trout each generation. These results suggest that wild resident fish contribute substantially to endangered steelhead 'populations' and highlight the need for conservation and management efforts to fully account for interconnected Oncorhynchus mykiss life histories.     

Life-history effects of migratory costs in anadromous brown trout

Mean size of sexually mature anadromous brown trout (sea trout) Salmo trutta in south-east Norway increased significantly with migratory distance ( D ) between the feeding area at sea and the spawning area in fresh water, from 32 cm for those spawning close to the river mouth to 43 cm at the spawning grounds 40 km inland. This was largely due to an increased size of the smallest anadromous spawners with increasing D . The raised mean size of the long-distance migrants is paralleled by an increased age at sexual maturity. Body mass at the same length of sea trout decreased with D in fresh water, meaning that the fish moving far inland was slimmer than those spawning near the coast. Gonadal mass of first-time spawning anadromous males declined significantly with D , and the fecundity and the ratio of fecundity over mean mass of the individual eggs adjusted for variation in fish mass, increased with D . There was no clear relationship between the ratio of anadromous to resident fish and D , probably because more variables than D , influence this relationship in the study streams.     

The formation of non-anadromous populations of Atlantic salmon, Salmon salar L., in Europe

Comparison of the different populations of non-anadromous Atlantic salmon in Europe has revealed some common traits. The non-anadromous populations probably became isolated from the anadromous salmon populations during a period of rapid land-upheaval after the last ice age, about 10 000 years ago. The oceanic temperature in the eastern part of the Atlantic was especially low in this period. This probably diminished the advantage gained from the anadromous habit. During this period the low temperatures in the rivers probably increased the frequency of females which matured without migrating seawards. A large number of individuals in the different populations seems to have been favourable for the formation and survival of such races. The occurrence of a lake in such a river system would probably ease the transition to non-anadromous behaviour, because the salmon would not then be forced to adjust its entire life-history when isolated (the salmon could spawn in the river in the usual manner and the smolts then migrate downstream into lakes). Larger lakes would also seem to infer problems for the navigation of the smolts towards the outlet. The only known exception is the river-living land-locked salmon population found in the River Namsen, Norway.
The factors mentioned above have led to an increase in the probability of occurrence and thriving of mature females without a sea migration or to a decrease in the competitive advantage of anadromous behaviour. The above mentioned similarities can explain the seemingly casual distribution of the non-anadromous populations of Atlantic salmon in Europe.     

Population dynamics and harvesting of semelparous species with phenotypic and genotypic variability in reproductive age

We study the evolution of polymorphic life histories in anadromous semelparous salmon and the effects of harvesting. We derive dynamic phenotypic and genetic ESS models for describing the evolutionary dynamics. We show in our deterministic analysis that polymorphisms are not possible in a panmictic random mating population. Instead, genetic or behavioral polymorphisms may be observed in populations with assortative mating systems. Positive assortative mating may be supported and generated by behavioral and phenotypic traits like male mate choice, spawning ground selection by phenotype, or within-river homing-migration-distance by size. In the case of an evolutionarily stable dimorphism, the ESS is characterized by a reproductive ideal free distribution such that at an equilibrium the individuals are indifferent from the fitness point of view between the two life histories of early and late reproduction. Different strategy models - that is, phenotypic and genetic ESS models - yield identical behavioral predictions and, consequently, genetics does not seem to play an important role in the present model. An evolutionary response to increased fishing mortality is obvious and may have resource management implications. High sea fishing mortalities drive the populations toward early spawning. Thus it is possible that unselective harvesting at sea may eliminate, depending on the biological system, behavioral polymorphisms or genetic heterozygozity and drive the population to a monomorphic one. If within-river homing migration distances depend on the size of fish, unselective harvesting at sea, or selective harvesting of spawning runs in rivers, may reduce local population sizes on spawning grounds high up rivers. Finally, harvesting in a population may cause a switch in a dominant life-history strategy in a population so that anticipated sustainable yields cannot be realized in practice.     

THE VISUAL SYSTEMS OF EURYHALINE FISHES

1. The retinas of all marine fishes so far examined except the Labridae, and of all terrestrial vertebrates contain the rhodopsin system alone; those of fresh water fishes the porphyropsin system alone. In the present paper the visual systems of a number of euryhaline fishes are examined—fishes capable of existence in a wide range of salinities, though usually restricted in spawning either to the sea (catadromous) or to fresh water (anadromous). 2. The retinas of the anadromous salmonids (brook trout, rainbow trout, and chinook salmon) contain mixtures of the rhodopsin and porphyropsin systems, predominantly the latter. The retinas of the catadromous eel and the killifish also contain mixtures of both systems, but in reverse proportions. The retinas of the anadromous white perch and alewife contain the porphyropsin system alone. 3. There is therefore an extensive parallelism between the salinity relations of these animals and the composition of their visual systems. All of them possess predominantly or exclusively the visual system commonly associated with the environment in which the fish spawns. 4. These patterns are fixed genetically, and are to a first approximation independent of the history of the individual. They may represent transitional stages in the evolutionary migration of fishes to and from the sea. The presence of both types of visual system in the retinas of some euryhaline fishes incidentally satisfies one formal requirement of two-component color vision.