Comparative developmental biology of pink salmon, Oncorhynchus gorbuscha, in southern British Columbia

Eggs and alevins from 21 families of pink salmon, Oncorhynchus gorbuscha , from five odd-year broodline stocks spawning in southern British Columbia were incubated under controlled water temperatures of 4° C, 8° C and 12° C. There were significant differences in egg survival among stocks and among families within stocks at all incubation temperatures, but the differences were greatest at 4° C. Alevin survival was at least 97% for each stock at each temperature. The most northern spawning stocks had higher egg survival at 4° C than did the others. Hatching time of the alevins and emergence time of the fry were similar for all five stocks. Alevins hatching at 8° C were longer than those hatching at 4°C or 12°C, but there were no stock differences in alevin length or tissue weight. Stocks with larger eggs produced alevins of greater total weight and more yolk. Emergent fry from Vancouver Island stocks had the greatest tissue weight at 12° C, but Fraser River fry were heaviest at 8° C. There were significant differences among families within stocks for alevin and fry size parameters, suggesting that family variation should be accounted for in studies of salmonid developmental biology.     

Water balance trumps ion balance for early marine survival of juvenile pink salmon (Oncorhynchus gorbuscha)

Smolting salmonids typically require weeks to months of physiological preparation in freshwater (FW) before entering seawater (SW). Remarkably, pink salmon (Oncorhynchus gorbuscha) enter SW directly following yolk absorption and gravel emergence at a size of 0.2 g. To survive this exceptional SW migration, pink salmon were hypothesized to develop hypo-osmoregulatory abilities prior to yolk absorption and emergence. To test this, alevins (pre-yolk absorption) and fry (post-yolk absorption) were transferred from FW in darkness to SW under simulated natural photoperiod (SNP). Ionoregulatory status was assessed at 0, 1 and 5 days post-transfer. SW alevins showed no evidence of hypo-osmoregulation, marked by significant water loss and no increase in gill Na?/K?-ATPase (NKA) activity or Na?:K?:2Cl? cotransporter (NKCC) immunoreactive (IR) cell frequency. Conversely, fry maintained water balance, upregulated gill NKA activity by 50 %, increased the NKA α1b/α1a mRNA expression ratio by sixfold and increased NKCC IR cell frequency. We also provide the first evidence of photoperiod-triggered smoltification in pink salmon, as fry exposed to SNP in FW exhibited preparatory changes in gill NKA activity and α1 subunit expression similar to fry exposed to SNP in SW. Interestingly, fry incurred larger increases in whole body Na? than alevins following both SW and FW + SNP exposure (40 and 20 % in fry vs. 0 % in alevins). The ability to incur and tolerate large ion loads may underlie a novel mechanism for maintaining water balance in SW prior to completing hypo-osmoregulatory development. We propose that pink salmon represent a new form of anadromy termed "precocious anadromy".     

The effects of low pH on egg and alevin survival of kokanee and sockeye salmon, Oncorhynchus nerka

1. The effects of low pH water on embryogenesis and vitellogenesis in kokanee and sockeye salmon (Oncorhynchus nerka) were investigated. Eggs were exposed to low pH from fertilization to 45 days post-median hatch or to an episodic exposure at pH 4.0. Adult kokanee were also exposed to low pH just prior to ovulation and spawning. 2. The most sensitive stages of development during chronic or episodic exposure to low pH were early embryonic development and newly-hatched alevins. 3. Incubation of eggs at low pH caused a lower median survival, delayed hatching, higher alevin mortality and reduced the efficiency of yolk conversion to tissue of yolk-sac alevins. Those effects were more pronounced when the eggs were fertilized at low pH. 4. Exposure of sexually mature kokanee salmon to acidified water reduced egg and alevin survival, delayed embryo hatching and decreased the percent hatch. Those effects were more pronounced when their eggs were incubated at low pH.     

Genetic variation in survival of chinook salmon (Oncorhynchus tshawytscha) alevins exposed to an unidentified agent of mortality

Mortality of an unknown etiology occurs after hatching and before emergence among Harrison River chinook salmon (Oncorhynchus tshawytscha) alevins incubated in the Chehalis River Hatchery, British Columbia. Inter- and intra-stock genetic variation for alevin survival and time to death was investigated at Chehalis Hatchery in factorial crosses among chinook salmon from the Harrison and Capilano rivers. Alevin survival by family ranged from 0 to 100%, with a mean value of 35.2%. The mean family survival of pure Harrison alevins (13.0%) was significantly lower than that of Capilano alevins (64.1%). For the Harrison stock, estimates of the heritability of survival were 1.05 +/- 0.62 (sire component) and 0.03 +/- 0.07 (dam component). For the Capilano stock, the corresponding estimates were 0.79 +/- 0.53 and 0.80 +/- 0.54. Family means of time to death ranged from 7.5 to 48 days after exposure to mortality-inducing agents. The mean times to death for pure Harrison (15.3 days) and Capilano (21.8 days) families were not significantly different. Sire and dam component heritability estimates for time to death were high for the Harrison stock (1.39 +/- 0.87 and 0.71 +/- 0.46) but low for the Capilano stock (0.06 +/- 0.11 and 0.17 +/- 0.18). Values of survival and time to death for the reciprocal interstock hybrid alevins generally fell between those of the parental stocks. Neither survival nor time to death differed significantly between the reciprocal hybrids, but both traits were more strongly influenced by sire than by dam. The possibility of asynchronous paternal and maternal allele activation during embryonic development was proposed as an explanation for the strong paternal effects observed in this study.     

Sex ratio control in pink salmon (Oncorhynchus gorbuscha) and chum salmon (O. keta) populations: the possible causes and mechanisms of changes in the sex ratio

Long-term changes in the sex ratio have been studied in pink salmon (Oncorhynchus gorbuscha) and chum salmon (O. keta) populations of Kamchatka and Sakhalin. It has been demonstrated that these changes are an adaptation to population dynamics: an increase in the population size is accompanied by a shift towards a higher proportion of males; a decrease in population size, by a shift towards a higher proportion of females. The correspondence between morphological and molecular characters in populations of the two species has been analyzed in order to determine the mechanism of sex ratio control. In some pink salmon and chum salmon populations, there is a discrepancy between sex identifications based on morphological characters and molecular markers. This discrepancy is assumed to be accounted for by sex inversion mechanisms, which may be population- or region-specific. In two cases, it has been found that the sex ratio discrepancy in populations is related to the numbers of fish in subsequent generations. These findings suggest that sex inversion may be related to population size control.     

Effect of pre-treatment exposures of toluene or naphthalene on the tolerance of pink salmon (Oncorhynchus gorbuscha) and kelp shrimp (Eualis suckleyi)

1. Toluene pre-treatment exposures did not affect survival of kelp shrimp or pink salmon fry in subsequent bioassays.2. Naphthalene pre-treatment exposures to kelp shrimp caused increased sensitivity in subsequent bioassays.3. Naphthalene pre-treatment exposures to pink salmon caused increase in tolerance in subsequent bioassays. Tolerance increase was proportional to concentration and duration of pre-treatment exposures, and decreased with periods of depuration.     

Differential expression of the pro-inflammatory cytokines IL-1beta-1, TNFalpha-1 and IL-8 in vaccinated pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon juveniles

Laboratory-reared pink and chum salmon juveniles (approximately 2g) received an intraperitoneal injection with a commercial, unadjuvanted Aeromonas salmonicida bacterin or sterile saline. Relative to elongation factor-1A, expression levels of genes encoding the proinflammatory cytokines interleukin-1beta-1 (IL-1beta), tumour necrosis factor-alpha-1 (TNFalpha) and interleukin-8 (IL-8) in pools of kidney and liver were examined 6- and 24-h after injection. Expression of IL-1beta was significantly elevated in pink and chum salmon by 6-h, and declined in pink salmon but not in chum salmon by 24-h. Similarly, expression of TNFalpha was significantly elevated in both species at 6h and only in chum salmon after 24-h. Expression of IL-8 was significantly elevated in both species at 6- and 24-h after injection. Expression of the three proinflammatory cytokine genes differed between salmon species both in the timing and magnitude of their expression. The significance of these differences with respect to immune function in these fish requires further research.     

Identification of the sex chromosome pair in chum salmon (Oncorhynchus keta) and pink salmon (Oncorhynchus gorbuscha)

Fluorescence in situ hybridization (FISH) using a probe to the male-specific GH-Y (growth hormone pseudogene) was used to identify the Y chromosome in the karyotypes of chum salmon (Oncorhynchus keta) and pink salmon (Oncorhynchus gorbuscha). The sex chromosome pair is a small acrocentric chromosome pair in chum salmon and the smallest metacentric chromosome pair in pink salmon. Both of these chromosome pairs are morphologically different from the sex chromosome pairs in chinook salmon (Oncorhynchus tshawytscha) and coho salmon (Oncorhynchus kisutch). The 5S rRNA genes are on multiple chromosome pairs including the sex chromosome pair in chum salmon, but at the centromeres of two autosomal metacentric pairs in pink salmon. The sex chromosome pairs and the chromosomal locations of the 5S rDNA appear to be different in all five of the North American Pacific salmon species and rainbow trout. The implications of these results for evolution of sex chromosomes in salmonids are discussed.     

Sex ratio control in pink salmon (<Emphasis Type="Italic">Oncorhynchus gorbuscha</Emphasis> and chum salmon (<Emphasis Type="Italic">O. keta</Emphasis>) populations: The possible causes and mechanisms of changes in the sex ratio

Long-term changes in the sex ratio have been studied in pink salmon (Oncorhynchus gorbuscha and chum salmon (O. keta) populations of Kamchatka and Sakhalin. It has been demonstrated that these changes are an adaptation to population dynamics: an increase in the population size is accompanied by a shift towards a higher proportion of males; a decrease in population size, by a shift towards a higher proportion of females. The correspondence between morphological and molecular characters in populations of the two species has been analyzed in order to determine the mechanism of sex ratio control. In some pink salmon and chum salmon populations, there is a discrepancy between sex identifications based on morphological characters and molecular markers. This discrepancy is assumed to be accounted for by sex inversion mechanisms, which may be population-or region-specific. In two cases, it has been found that the sex ratio discrepancy in populations is related to the numbers of fish in subsequent generations. These findings suggest that sex inversion may be related to population size control.     

Size‐dependent growth of individual Atlantic salmon Salmo salar alevins from hatch to first feeding

Variation in egg size, hatch timing and size at hatch, and their influence on individual growth rates of Atlantic salmon Salmo salar alevins up to first feeding were examined in pure strain and hybrid crosses of fish from Scotland and Canada. At the intra‐female, intra‐cross type and inter‐cross type levels, specific growth rates prior to first feed were strongly size dependent, with smaller and later hatching alevins growing significantly faster. The magnitude of this size‐dependent growth was greatest in the hybrid crosses. This resulted in a 40% reduction in the coefficient of variation (c.v. ) in alevin size from post‐hatch to first feeding at the intra‐female level, and a reduction of both intra‐ and inter‐cross differences in alevin sizes in the same period.     

Functional response of juvenile pink and chum salmon: effects of consumer size and two types of zooplankton prey

Feeding rate experiments were conducted for pink salmon Oncorhynchus gorbuscha fry [mean fork length ( L _F) 39 mm], juveniles (103–104 mm L _F) and juvenile chum salmon Oncorhynchus keta (106–107 mm L _F). Fishes were presented with small copepod ( Tisbi sp.) or larger mysid shrimp ( Mysidopsis bahia ) prey at varying densities ranging from 1 to 235 prey l⁻¹ in feeding rate experiments conducted at water temperatures ranging from 10·5 to 12·0° C under high light levels and low turbidity conditions. Juvenile pink and chum salmon demonstrated a type II functional response to mysid and copepod prey. Mysid prey was readily selected by both species whereas the smaller bodied copepod prey was not. When offered copepods, pink salmon fry fed at a higher maximum consumption rate (2·5 copepods min⁻¹) than larger juvenile pink salmon (0·4 copepods min⁻¹), whereas larger juvenile chum salmon exhibited the highest feeding rate (3·8 copepods min⁻¹). When feeding on mysids, the maximum feeding rate for larger juvenile pink (12·3 mysids min⁻¹) and chum (11·5 mysids min⁻¹) salmon were similar in magnitude, and higher than feeding rates on copepods. Functional response models parameterized for specific sizes of juvenile salmon and zooplankton prey provide an important tool for linking feeding rates to ambient foraging conditions in marine environments, and can enable mechanistic predictions for how feeding and growth should respond to spatial-temporal variability in biological and physical conditions during early marine life stages.     

The abundance and distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on pink (Oncorhynchus gorbuscha) and chum (O. keta) salmon in coastal British Columbia

In total, 23,750 specimens of the salmon louse, Lepeophtheirus salmonis, were collected from 3,907 juvenile pink and 3,941 chum salmon caught within the Broughton Archipelago during a 2-yr survey. The prevalence on pink salmon was significantly higher than on chum salmon in 2004 (62.3% and 58.6%, respectively) and in 2005 (26.4% and 23.1%, respectively). The mean abundance on chum salmon was significantly higher than on pink salmon in 2004 (7.0 +/- 0.3 and 2.8 +/- 0.2, respectively), whereas in 2005 the mean abundance did not differ between species (0.6 +/- 0.1 and 0.5 +/- 0.0, respectively). The mean intensity on chum salmon was significantly higher than on pink salmon in 2004 (12.0 +/- 0.4 and 4.5 +/- 0.2, respectively) and in 2005 (2.5 +/- 0.2 and 1.7 +/- 0.1, respectively). The prevalence, intensity, and abundance of L. salmonis were significantly higher on salmon belonging to both host species in 2004 compared with 2005. In both years, a majority of pink and chum salmon had 2 or fewer lice. In general, a decline in abundance of L. salmonis over the 3 collection periods in each year coincided with an increased percentage of motile developmental stages. The abundance was lowest on fish collected from zones in which the seawater surface salinity was also lowest. Seawater surface temperature was higher and salinity was lower in 2004 compared with 2005. The spatial and temporal trends in the abundance of L. salmonis in relation to host size, infestation rates, and seawater salinity and temperature, evident in both years, must be considered in future studies assessing the role of farmed salmon in the epizootiology of this parasite on juvenile salmon in this area.     

Hatching Time and Alevin Growth Prior to the Onset of Exogenous Feeding in Farmed,Wild and Hybrid Norwegian Atlantic Salmon

The onset of exogenous feeding, when juveniles emerge from the gravel, is a critical event for salmonids where early emergence and large size provide a competitive advantage in the wild. Studying 131 farmed, hybrid and wild Norwegian Atlantic salmon families, originating from four wild populations and two commercial strains, we investigated whether approximately 10 generations of selection for faster growth has also resulted in increased somatic growth prior to the onset of exogenous feeding. In addition, we tested whether relaxed selection in farms has allowed for alterations in hatching time between farmed and wild salmon. Across three cohorts, wild salmon families hatched earlier than farmed salmon families, while hybrid families displayed intermediate hatching times. While the observed differences were small, i.e., 1–15 degree-days (0–3 days, as water temperatures were c. 5–6°C), these data suggest additive genetic variation for hatching time. Alevin length prior to exogenous feeding was positively related to egg size. After removal of egg size effects, no systematic differences in alevin length were observed between the wild and farmed salmon families. While these results indicate additive genetic variation for egg development timing, and wild salmon families consistently hatched earlier than farmed salmon families, these differences were so small they are unlikely to significantly influence early life history competition of farmed and wild salmon in the natural environment. This is especially the case given that the timing of spawning among females can vary by several weeks in some rivers. The general lack of difference in size between farmed and wild alevins, strongly suggest that the documented differences in somatic growth rate between wild and farmed Norwegian Atlantic salmon under hatchery conditions are first detectable after the onset of exogenous feeding.     

Climate warming causes phenological shift in Pink Salmon, Oncorhynchus gorbuscha, behavior at Auke Creek, Alaska

Thirty‐four years (1972–2005) of water temperature data and extensive biological observations at Auke Creek, Alaska indicate a general warming trend that affected the native pink salmon (Oncorhynchus gorbuscha) population. Serial environmental records at nearby Auke Bay, Alaska over 46 years show trends of increasing air and sea surface temperatures. Trends of increased total precipitation and earlier date of ice out on nearby Auke Lake also occurred, but not at significant rates. Average water temperatures during the incubation of pink salmon in Auke Creek increased at a rate of 0.03 °C yr^?1 over the 34‐year period. For the 1972–2005 broods, midpoints of fry migrations from Auke Creek ranged between April 2 and May 7, and there was a trend of earlier migration of pink salmon fry at a rate of ? 0.5 days yr^?1. The migration timing of adult salmon into Auke Creek also showed a trend toward earlier timing. The earlier adult migration combined with warmer incubation temperatures are related to earlier migration of pink salmon fry. If the observed warming trend continues, Auke Creek may become unsuitable habitat for pink salmon. Given the trend for salmon fry to migrate earlier, a larger portion of the population may become mismatched with optimum environmental conditions during their early marine life history. If salmon adults continue to migrate into the creek earlier when water temperatures are commonly high, it will result in increased prespawning mortality.     

A genetic analysis of body size in pink salmon (Oncorhynchus gorbuscha)

Two small-sized and two large-sized male pink salmon (Oncorhynchus gorbuscha) were mated to each of four females, producing eight families sired by small males and eight sired by large males. The juveniles were reared for 500 d after fry emergence. Juvenile weight in the two male size classes was similar until the spring of the year of maturity, when juveniles sired by large males grew faster than those sired by small ones. Heritability estimates of weight based upon the dam component of variance increased during 500 d of rearing from 0.4 to 0.8. Heritability of weight based upon the sire component of variance generally ranged between 0.1 and 0.3. The large variation in male body size in spawning pink salmon populations may have resulted from different male breeding strategies.     

Annual changes in the population size of the salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae) on high-seas Pacific Salmon (Oncorhynchus spp.), and relationship to host abundance

The population size of the salmon louse, Lepeophtheirus salmonis, was monitored annually in the summers of 1991–1997 by examining six species of Pacific salmon (Oncorhynchus spp.) caught by surface long-lines in oceanic offshore waters of the North Pacific Ocean and Bering Sea. The annual copepod population size on all salmonids caught was estimated by combining the calculated number of copepods carrying on each salmonid species. The copepod population fluctuated markedly from year to year, which resulted largely from marked annual changes in abundance of pink salmon (O. gorbuscha). Since pink salmon were most frequently and heavily infected and since their abundance changed every year, the copepod population was high in the years when this salmonid species was abundant, but low when it was rare. On the contrary, chum salmon (O. keta) did not show high prevalence and intensity of infection, but the annual abundance of this host species was consistently high, i.e. chum salmon carried many copepods every year. Copepods on other salmonid species (sockeye salmon O. nerka, coho salmon O. kisutch, chinook salmon O. tshawytscha, and steelhead trout O. mykiss) constantly formed a small percentage of the total copepod population. Both chum and pink salmon are the most important hosts in terms of their substantial contribution to support the copepod population, but the importance as hosts of each species is definitely different between the species. Chum salmon is a stable important host supporting the copepod population at a relatively high level every year, while the number of copepods on pink salmon annually exhibits marked fluctuations, and this salmonid species is regarded as an unstable important host.     

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.     

Temperature seasonality during fry out‐migration influences the survival of hatchery‐reared chum salmon Oncorhynchus keta

Among years, fry‐to‐adult survival of hatchery‐reared chum salmon Oncorhynchus keta was positively correlated with the length (in days) of the fry out‐migration period with temperatures suitable for migration. Furthermore, survival decreased with increasing difference in mean temperature between May and June. Thus, prolonged out‐migration periods increased the probability of survival from fry to adult, lending support to the hypothesis that long migration periods decrease the risk of mortality (bet‐hedging), and increase the probability of migration when environmental conditions in fresh water and the ocean are suitable (match–mismatch).     

The Salmon Smai Family of Short Interspersed Repetitive Elements (Sines): Interspecific and Intraspecific Variation of the Insertion of Sines in the Genomes of Chum and Pink Salmon

The genomes of chum salmon and pink salmon contain a family of short interspersed repetitive elements (SINEs), designated the salmon SmaI family. It is restricted to these two species, a distribution that suggests that this SINE family might have been generated in their common ancestor. When insertions of the SmaI SINEs at 10 orthologous loci of these species were analyzed, however, it was found that there were no shared insertion sites between chum and pink salmon. Furthermore, at six loci where SmaI SINEs have been species-specifically inserted in chum salmon, insertions of SINEs were polymorphic among populations of chum salmon. By contrast, at four loci where SmaI SINEs had been species-specifically inserted in pink salmon, the SINEs were fixed among all populations of pink salmon. The interspecific and intraspecific variation of the SmaI SINEs cannot be explained by the assumption that the SmaI family was amplified in a common ancestor of these two species. To interpret these observations, we propose several possible models, including introgression and the horizontal transfer of SINEs from pink salmon to chum salmon during evolution.     

Condition factor dependency of burst swimming ability between wild and hatchery-reared chum salmon fry (Oncorhynchus keta)

Ichthyological Research - Burst swimming velocity (Uburst) was compared between wild and hatchery-reared chum salmon fry. In the hatchery-reared fry, Uburst was significantly correlated with the...