Pacific salmon migrations and homing: mechanisms and adaptive significance

Pacific salmon are noted for their lengthy foraging migrations and for their precise homing ability. Extensive sampling has documented the general migratory patterns of the major populations, but many basic aspects of their marine ecology are still poorly understood. Their life history pattern has been interpreted as an adaptation to exploit the higher productivity of the marine environment over that in fresh water. The adaptive significance of homing is implied by the specializations of populations for their natal habitat and the competitive superiority of locally adapted populations over transplants from other rivers. However, the establishment of new populations by strays and the levels of gene flow between natural populations have only recently received much attention. Research on salmon migrations has also focused on the mechanisms that guide homing at sea and in fresh water. While salmon have highly developed sensory systems, the ways in which inputs are integrated to guide migration through diverse and complex habitats are still being investigated.     

Dendritic cell migration and lymphocyte homing imprinting

For an effective adaptive immune response to occur, dendritic cells (DC), which are the most efficient antigen-presenting cells, must be able to sample the peripheral microenvironment and migrate towards secondary lymphoid organs (SLO) where they activate naive lymphocytes. Upon activation, lymphocytes proliferate and acquire the capacity to migrate to extralymphoid compartments. Although the molecular mechanisms controlling lymphocyte homing to lymphoid and to some extralymphoid tissues have been described in significant detail, it is much less clear how DC migration is controlled. Do DC obey similar adhesion cues that lymphocytes do, or do they have their own "zip codes"? This is relevant from a therapeutic standpoint because effective DC-based vaccines should be able to reach the appropriate tissues in order to generate protective immune responses. Here, we discuss some of the mechanisms used by DC to reach their target tissues. Once DC arrive at their destination, they are exposed to the tissue microenvironment, which likely modulates their functional properties in a tissue-specific fashion. This local DC "education" is probably responsible among other things; for the acquisition of tissue-specific homing imprinting capacity by which DC instruct lymphocytes to migrate to specific tissues. Finally, we discuss how dysregulation of these signals may play a key role in disease.     

Expression of the calcitonin gene during migration of the Pacific salmon, Oncorhynchus gorbuscha

Plasma calcitonin levels increase during reproduction in female salmon. Whether these changes in circulating levels of the hormone are due to increased secretion and or increased biosynthesis is not established. We measured total and poly A+ RNAs and calcitonin content of ultimobranchial bodies of male and female pink salmon during the different stages of the reproductive cycle. Calcitonin mRNAs were analysed by hybridization of northern and dot blots with a specific probe for salmon calcitonin. Dot blot autoradiography indicated that female animals had higher levels of CT mRNA than males and these values were correlated with plasma calcitonin levels. In conclusion, sexual hormones still to be identified, are probably implicated in the expression of the calcitonin gene in females during the reproductive cycle.     

Detection of infection and susceptibility of different Pacific salmon stocks (Oncorhynchus spp.) to the haemoflagellate Cryptobia salmositica

The haematocrit centrifugation technique, modified by keeping the haematocrit tubes cold (between 1 and 10 C), was sensitive for detecting light infections of Cryptobia salmositica (as few as 75 flagellates per ml of blood). In wet mount preparations, infections lighter than 7.5 X 10(3) flagellates per ml of blood could not be detected consistently. Different Pacific salmon stocks from British Columbia demonstrated differences in susceptibility to C. salmositica in experimental studies using laboratory reared juvenile fish. Oncorhynchus keta and Oncorhynchus tshawytscha from the Big Qualicum River stocks (Vancouver Island), and Oncorhynchus nerka from the Fulton River stock (Skeena River system), were all equally susceptible and suffered high mortalities at low exposures (100 flagellates in 0.1 ml physiological saline inoculated intraperitoneally per fish). Oncorhynchus nerka from the Weaver Creek stock (Fraser River system) was the most resistant with no mortalities even at exposures of 10(6) flagellates (in 0.1 ml physiological saline) per fish. Oncorhynchus kisutch seemed to be slightly less resistant than the Weaver Creek O. nerka, but fewer than 16% of the inoculated fish died. Oncorhynchus kisutch from the Big Qualicum River seemed to be slightly more resistant than O. kisutch from the Capilano River stock (a coastal river near Vancouver), with fewer mortalities and lighter infections when the experiments were terminated. Differences in susceptibility are believed to be associated with innate, genetically transmitted resistance.     

Evolutionary-physiological aspects of adaptation of the Pacific salmon fry of the Oncorhynchus genus to migration to the sea water

A complex of adaptive changes occurring in the Pacific salmon fry in the process of migration to the sea is described, including behavior, ion content in carcasses, and morphological changes in Stannius bodies, gill epithelium, and nephron tubular epithelium. Participating in experiments with transfer from fresh water into a two-layer aquarium (the lower layer - sea water, the upper layer - fresh water) were smolts of chum salmon and underyearlings of masu salmon as well as the trachurus and leiurus forms of the three-spined stickleback Casterosteus aculeatus. All fish, regardless of their salt preference, at once after placement into the two-layer aquarium, occupied the sea water zone, at the very bottom of the aquarium. After 1 h, there started brief excursions of masu salmon and chum salmon to the upper, fresh water layer; however, both forms of the three-spined stickleback did not participate in these excursions. After 12 h, the chum salmon settled down in the lower, sea water layer, while the masu salmon - in the upper, fresh water layer. Both forms of the three-spined stickleback never left the sea water layer and felt quite comfortably on the aquarium bottom. It seems that the high tolerance of the both stickleback forms to wide salinity limits allows them to choose the convenient position regardless of the water salt composition. By analyzing the material obtained for three years (2001-2003) on structure and functions of the gill epithelium chloride cells (CC), we have come to the conclusion that the fresh water fry of two salmon species, chum and masu salmons, caught at the same time and practically in the same water reservoirs can be divided into three groups. The underyearlings of the masu salmon as a rule are characterized by the thickened epithelium of secondary gill lamellae, but by a very small number of CC. In smolts of chum salmon, on the contrary, the epithelium is sufficiently thin, but enriched in the CC that demonstrate an active structure in the very beginning of migration to sea. However, with approaching the sea (and with an increase of terms of migration) the CC activity drops, but their amount does not change. And only after migration to the sea the CC activity rises again, although their amount seems to remain unchanged. The described peculiarities of behavior and of the ion composition regulation in the migrating salmon fry confirm the hypothesis that the salmons evolutionized in fresh water, that the Oncorhynchus genus appeared in large spaces of saltish waters, such as the Japan Sea at the period of the early Pleistocene, and that learning of fry of the Oncorhynchus genus (for instance, of O. gorbuscha and O. keta) is the most specialized in the salmons migrating to the sea, whereas the fresh water species of chars (Salvelinus) and of trouts (Salmo) are more primitive.     

Fecundity and egg size variation in North American Pacific salmon (Oncorhynchus)

We examined regional and latitudinal variation in fecundity and egg weight for five species of Pacific salmon ( Oncorhynchus ) along the Pacific coast of North America. Data were examined for 24 chum salmon, 15 pink salmon, 34 sockeye salmon, 44 chinook salmon, and 40 coho salmon populations from published sources, unpublished Canadian hatchery records, our own laboratory investigations, and other unpublished sources. Substantial regional variation in fecundity and egg weight was observed, with salmon on the Queen Charlotte Islands and Vancouver Island in British Columbia generally having lower fecundity and larger egg size than nearby mainland populations. The relative distance of freshwater migration to the spawning grounds generally had a marked effect on both fecundity and egg size, with populations spawning in the upper portions in the drainages of large rivers like the Fraser River in British Columbia having reduced fecundity and egg size compared with coastal spawning populations. Fecundity was generally higher and egg size generally lower in more northern populations of sockeye, chinook, and coho salmon compared with southern ones. We suggest that egg size tends to be lower in northern populations of some species as a result of increased fecundity due to their older ages at maturity and a limited amount of energy that can be expended on egg production.     

Metabolic pathways of carotenoids in chum salmon Oncorhynchus keta during spawning migration

1. Based on the contents and individual composition of carotenoids in the muscle, serum and ovaries of chum salmon during spawning migration, the reductive metabolism of astaxanthin to zeaxanthin was presumed to take place in the muscle of both male and female. 2. The metabolic rates of zeaxanthin and 4-keto-zeaxanthin in female serum were much faster than those in male serum.     

Timing games in the reproductive phenology of female pacific salmon (Oncorhynchus spp.)

We use a game-theoretic framework to investigate the reproductive phenology of female kokanee (Oncorhynchus nerka). As in the other semelparous species of Pacific salmon, females construct nests in gravel, spawn with males, bury their fertilized eggs, and defend their nest sites until they die several days later. Later-breeding females may reuse previous nest sites, and their digging behavior is thought to subject previously buried eggs to mortality. Using game-theoretic models, we show that females can reduce this risk by allocating resources to longevity (the period between arrival and death) as opposed to eggs. Waiting before territory settlement is also expected if it allows females to conserve energy and delay senescence. The models demonstrate how these costs and benefits interact to select for a seasonal decline in longevity, a well-known phenomenon in the salmonid literature, and a seasonal decline in wait duration. Both of these predictions were supported in a field study of kokanee. Female state of reproductive maturity was the most important proximate factor causing variation in longevity and wait duration. With more than 30% of territories being reused, dig-up is likely an important selective force in this population.     

Physiological impact of acute molybdenum exposure in juvenile kokanee salmon (Oncorhynchus nerka)

A series of experiments were conducted to determine the physiological impact of acute sublethal molybdenum exposure to juvenile kokanee salmon (Oncorhynchus nerka Kennerlyi). Molybdenum was found to be relatively non-toxic to kokanee as the 96 h LC(50) was greater than 2,000 mg Mo l(-1). Exposure to either 25 or 250 mg Mo x l(-1) for 7 days was found to stimulate a significant 1.6- to 1.7-fold increase in ventilation which was later characterized to be dose-dependent between 5 and 250 mg Mo l(-1). Acute sublethal molybdenum exposure was found to have little or no impact on kokanee oxygen consumption at rest or immediately following a bout of forced activity or on physiological indicators of stress such as plasma lactate, sodium and cortisol. Despite these findings, prior exposure to 25 or 250 mg Mo l(-1) resulted in post-exercise loss of equilibrium and exercise-induced delayed mortality that were not observed in controls. Molybdenum accumulation in gill and liver of kokanee was also characterized. The findings of this study suggest that despite the non-toxic nature of molybdenum, acute sublethal exposure to this metal has physiological consequences to those fish exposed even for only a brief period. Further studies are needed to more fully elucidate the metabolism and mode of action of this metal in fish.     

Kinship analysis of Pacific salmon: insights into mating, homing, and timing of reproduction

Multilocus microsatellite genotypes were used to infer kinship and relatedness in two species of Pacific salmon from three populations in Washington State. Even in the absence of direct genetic data from parents, clustering of individuals according to allele sharing and reconstruction of parental genotypes allowed resolution of full- and half-sib relationships among 135 chinook salmon (Oncorhynchus tshawytscha) sampled as preemergent juveniles from 14 redds in the Dungeness River. Inferred reproductive behaviors included single-pair matings, polyandry in which females mated with two to three males at a single redd, polygyny in which males mated with two females at different redds, use of two redds by a single female, and use of one redd site by two females. Greater average relatedness (rxy) in the upper reach of the Dungeness River implied within-reach homing of returning adults. In steelhead trout (O. mykiss), the frequency of related pairs (dyads) of mature individuals that migrated up Snow Creek less than a week apart was greater than expected for randomly chosen dyads, as was the frequency of steelhead dyads that were spawned on the same day in the Forks Creek hatchery. These results imply a heritable basis for upstream migration date and maturation date in steelhead trout.     

Behavioural thermoregulation and homing by spring chinook salmon, Oncorhynchus tshawytscha (Walbaum), in the Yakima River

Temperature-sensitive radio transmitters were employed to study the patterns of behavioural thermoregulation, habitat preference and movement of 19 adult spring chinook salmon, Oncurhynchus tshawytscha (Walbaum), in the Yakima River. During the 4 months prior to spawning, fish maintained an average internal temperature 2.5°C below ambient river temperature. This represented a 12 to 20% decrease in basal metabolic demand or a saving of 17.3 to 29.9 calkg⁻¹ h⁻¹. Fish were most commonly associated with islands, pools, and rock out-croppings along stream banks. Homing behaviour appeared to be modified to optimize temperature regimes and energy conservation. As the time of spawning approached, fish left thermal refuges and migrated to spawning grounds upstream and downstream of refuge areas. Although spring chinook salmon residing within cool-water refuges may be capable of mitigating sub-lethal temperature effects, cool-water areas need to be abundant and available to the fish. The availability of suitable thermal refuges and appropriate holding habitat within mainstem rivers may affect long-term population survival.     

Chemosensory responses of juvenile Coho salmon, Oncorhynchus kisutch, Dolly Varden, Salvelinus malma, and sculpins (Cottus spp.) to eggs and other tissues from adult Pacific salmon

The carcasses of semelparous Pacific salmon (Oncorhynchus spp.) provide nutrients that enter aquatic ecosystems by various pathways, including direct consumption of tissue by fishes. Salmonids and other species frequently eat eggs and other tissues from dead salmon but the roles of vision and olfaction are unclear, as is the relative attraction to different tissues. Accordingly, we conducted a series of in situ experiments using minnow traps in two natural streams in Alaska to test the relative roles of chemosensory and visual cues in attraction of fishes to eggs from adult Pacific salmon, and then compared catch rates of traps baited with eggs, muscle, liver, and testis. Experiments indicated that chemical traces were necessary and sufficient to attract juvenile Dolly Varden (Salvelinus malma), coho salmon (Oncorhynchus kisutch), and sculpins (Cottus spp.) into traps. Combining both sites, 70 salmonids and 19 sculpins were trapped using visual and chemical cues, and 53 and 21, respectively, for traps with only chemical cues. Traps with only the sight of eggs caught no salmonids and only 5 sculpins, comparable to empty control traps. In addition, eggs were markedly more attractive than the other tissues, trapping 68?% of the salmonids and 69?% of the sculpins, compared to 14?% and 15?% for muscle tissue, 12?% and 11?% for liver, and 6?% and 5?% for the testis. Visual cues undoubtedly play a role in egg consumption in streams, but these experiments indicated a very important role of chemical traces in attracting fish to the vicinity of the eggs, and selective attraction of eggs over other salmon tissues.     

Morpho-ecological patterns and feeding of coho salmon Oncorhynchus kisutch fry in the period of downstream migration

The principal patterns of feeding of downstream-migrant and coastal young of the year of coho salmon are considered. The so-called potential downstream migrants and residents, which differ in size and feeding patterns, were distinguished among coastal fry. It is assumed that identification of particular coastal specimens to phenotypic groups of downstream migrants or nonmigrants of young of the year of coho salmon may be determined even in the daytime by such parameters as the body length, feeding intensity, and food spectrum.     

Plasma insulin levels during the spawning migration of the pink salmon, Oncorhynchus gorbuscha

Plasma insulin concentration was measured by homologous radioimmunoassay in male and female pink salmon. Oncorhynchus gorbuscha , during spawning migration in the Fraser and Thompson Rivers, British Columbia. Although the fish ceased feeding prior to entering fresh water, plasma levels of insulin remained stable (males) or even elevated (females) during the final stages of oogenesis and spermatogenesis, decreasing thereafter. Mean concentrations ranged from 0–69 to 1.24 ng ml⁻¹ in males and from 0.33 to 0.88 ng ml⁻¹ in females. At all stages in the anadromous migration where a significant difference in plasma insulin levels between the sexes was observed, males had higher concentrations than females.