Fitness and behavioral correlates of pre-stress and stress-induced plasma cortisol titers in pink salmon (Oncorhynchus gorbuscha) upon arrival at spawning grounds

Semelparous Pacific salmon (Onchorynchus spp.) serve as an excellent model for examining the relationships between life history, behavior and individual variation in glucocorticoid (GC) stress hormone levels because reproductive behaviors are highly variable between individuals and failure to reproduce results in zero fitness. Pink salmon (O. gorbuscha) were intercepted upon arrival at the spawning grounds across three time periods. Pre-stress and stress-induced plasma cortisol concentrations were assessed in relation to behavior, longevity and reproductive success. Results revealed differences between sexes and with arrival time. The study period marked a year of high reproductive success and only nine females (12% of sample) failed to spawn. Female pre-spawn mortalities were characterized by significantly elevated stress-induced cortisol concentrations and decreased longevity as well as pre-stress cortisol above the normal range in pink salmon from the study area. Interestingly, reproductive behaviors were only associated with pre-stress cortisol levels. For females, aggression and mate interaction time were reduced in individuals with elevated pre-stress cortisol concentrations. In males, a similar negative relationship between pre-stress cortisol concentration and mate interaction time was detected. The observed behavioral correlations are likely a factor of social status where dominant individuals, known to have higher reproductive success, are characterized by lower cortisol levels relative to subordinate conspecifics. Findings show both elevated pre-stress and stress-induced cortisol concentrations at arrival to the spawning grounds to be associated with reduced survival.     

Changes in plasma thyroid hormone levels in pink salmon, Oncorhynchus gorbuscha, during their spawning migration in the Fraser River (Canada)

Plasma thyroid hormone levels were measured in pink salmon, Oncorhynchus gorbuscha , during their spawning migration in the Fraser River, British Columbia. The plasma levels of both l-thyroxine (T₄) and triiodo-l-thyronine (T₃) were significantly higher in males than in females. In both sexes the hormone levels were maintained, or increased somewhat, during the early stages of migration, but fell thereafter. In females the plasma T₄ and T₃ levels of salmon collected on the spawning grounds were at or below detectable levels of the assays. The changes in thyroid hormone levels are correlated with changes in plasma insulin, gonadotropin, gonadal steroid hormones, cortisol and vitellogenin levels measured in the same specimens.     

Behavior of juvenile pink salmon (Oncorhynchus gorbuscha Walbaum) toward novel prey: influence of ontogeny and experience

Synopsis The behavior of individual, juvenile pink salmon toward novel prey (Artemia salina) under laboratory conditions is described. Two aspects of predatory behavior, namely latency time to initial prey-capture attempt and prey-capture success, are quantified in relation to chronological age and feeding experience. Initially, mean latency time declined slightly with increasing age up to Day 19 (post-emergence from gravel), but increased sharply to an asymptote with further aging. Mean percentage capture success gradually increased from 7.88% on Day 1 to 92.9% on Day 45. Prior feeding experience on the prey resulted in a decline (to a stable level) in mean latency time in experienced fish compared to control fish. Mean percentage capture success was not significantly altered by prior feeding experience on the prey.     

Changes in structure of tissues and in plasma cortisol during the spawning migration of pink salmon, Oncorhynchus gorbucha (Walbaum)

Changes in the structure of the gonad, skin, interrenal, liver, kidney, stomach, gill and pituitary gland, as well as blood cortisol and haematocrit values were investigated in adult pink salmon during their migration through the Fraser and Thompson Rivers to the spawning grounds. At the commencement of their freshwater migration the gonads of both males and females were in an advanced state of development, the pituitary contained a large complement of well-granulated gonadotrops, and hypertrophy was evident in the interrenal tissue and in the epidermis of the skin. At this time, no change from the normal sexually immature salmon was evident in the structure of the gill, liver or stomach. Sclerosis of the glomeruli was noted in the kidney. The plasma cortisol level was consistent with concentrations in unstressed salmon.
Migration of the fish through a turbulent section of the Fraser River evoked a marked increase in both blood cortisol concentration and in interrenal nuclear diameters.
On arrival at the spawning grounds, 10–15 days after entry into fresh water, a general but not marked deterioration of the tissues was evident. The results are discussed in relation to the spawning migration of other species of Pacific salmon.     

A genetic analysis of early development in pink (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) at three different temperatures

A factorial mating design was employed in which five males were mated to each of five females in each of two stocks for both pink and chum salmon. The resulting embryos and alevins were incubated at constant water temperatures of 4, 8, and 16 degrees C for pink salmon and 3, 8, and 15 degrees C for chum salmon. Variation among families in alevin and fry survival rates, hatching, button-up time, length, and weight was the least at 8 degrees C. Heritability of traits directly correlated with fitness, such as survival rates and button-up time, was low at all temperatures (h2 less than or equal to 0.25). Maternal effects could account for a substantial portion of the variation in alevin and fry size characters. Nonadditive genetic variance accounted for more of the variation in fry size characters than in those of alevins. Negative genetic correlations were observed between embryo survival and subsequent alevin size and between hatching time and subsequent alevin and fry size. Genotype-temperature interactions could underlie a substantial amount of phenotypic variation in the developmental characters examined for both species.     

Active feeding of downstream migrating juvenile pink salmon (Oncorhynchus gorbuscha) revealed in a large Barents Sea river using diet and stable isotope analysis

The recent, rapid spreading of non-native pink salmon Oncorhynchus gorbuscha in the North Atlantic area has raised concerns about their possible negative impacts on native salmonid species. Potential interactions include competition for food resources during the short freshwater phase of juvenile O. gorbuscha, but little is known about their feeding behavior in the newly occupied North Atlantic rivers. Using stable isotope and stomach content analyses, patterns of freshwater feeding of non-native O. gorbuscha fry were studied in a large Fennoscandian river, the Teno, that discharges to the Barents Sea. Changes in stable isotope values (δ¹³C, δ¹⁵N, δ³⁴S) and stomach contents from the period of emergence (April to mid-May) to estuarine entry (late May/June) were examined and provided both temporally integrated and short-term indicators of freshwater feeding dependency. In addition, the occurrence of juvenile O. gorbuscha and changes in their length and weight during their emergence/migration period were investigated. Juvenile O. gorbuscha were at the spawning grounds from April through to mid-May with abundance peaking in mid-May. Fish moved to the estuary by late May and their abundance decreased toward June, and their body size increased concurrently. Stomach analyses indicated no feeding activity in April–early May in the spawning areas, but the stomach fullness indices increased markedly in fish sampled in the estuary in May and June. The most important prey items in stomachs were Chironomidae and Ephemeroptera larvae. Significant changes in all analysed stable isotopes were detected among sample periods, with a peak in mid-May and June showing significantly lower values than other sample periods. A change from the higher values reflective of parental marine feeding to the lower values reflective of freshwater feeding indicated active in-river feeding by juveniles during the study period. The documented active freshwater feeding of non-native juvenile O. gorbuscha suggests potential resource competition with native fluvial fishes, particularly salmonids.     

Gene expression of neuronal soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex components in the olfactory organ and brain during seaward and homeward migration by pink salmon (Oncorhynchus gorbuscha)

The expression of synaptic vesicle exocytosis-regulator SNARE complex component genes (snap25, stx1 and vamp2) was examined in the olfactory nervous system during seaward and homeward migration by pink salmon (Oncorhynchus gorbuscha). The expression levels of snares in the olfactory organ were higher in seaward fry than in feeding and homeward adults, reflecting the development of the olfactory nervous system. The expression of snap25a, b and stx1a was upregulated or stable in the adult olfactory bulb and telencephalon. This upregulated expression suggested alterations in olfactory neuronal plasticity that may be related to the discrimination of natal rivers. The expression of stx1b was downregulated in the adult olfactory bulb, but remained stable in the adult telencephalon. The expression of vamp2 was initially strong in seaward fry, but was downregulated in adults in both the olfactory bulb and telencephalon. Pink salmon has the lowest diversity of maturation age, the largest population, and the most evolutional position in Pacific salmon (genus Oncorhynchus). The expression of snares in the olfactory center of pink salmon reflected the timing of sexual maturation and homeward migration. The present results and our previous studies indicate that snares show distinct expression patterns between two salmon species that depend on physiological and ecological features of migration.     

Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia)

This study examines factors affecting androgen and cortisol levels in wild, male golden lion tamarins (Leontopithecus rosalia). Golden lion tamarins are a cooperatively breeding species in which groups often contain two potentially breeding males. Brothers frequently emigrate together and develop a clear dominance hierarchy, but interactions between them are primarily affiliative. Duos in which the males are not related are less stable. In addition, reproductive skew theory predicts that dominant males will be less likely to share reproduction with related subordinates. As such, we predicted that both androgens and cortisol would be higher in subordinate males unrelated to the dominant male. We also predicted that androgens in breeding males would be higher during the mating season than the birth/infant care season, as per Wingfield's "challenge hypothesis" (1990). Fecal samples were collected from 24 males in 14 social groups and assayed by enzyme immunoassay. Androgen levels were higher in breeding males during the mating season, thus supporting the challenge hypothesis. However, while subordinate males unrelated to the dominant male had significantly lower androgens than any other group, cortisol levels were not correspondingly higher. These results suggest that unrelated subordinate males show measurable reproductive suppression and may use strategies such as infantilization to avert aggression from dominant males.     

Reproductive investment patterns,sperm characteristics,and seminal plasma physiology in alternative reproductive tactics of Chinook salmon (Oncorhynchus tshawytscha)

Although alternative reproductive tactics (ARTs) are common across a range of taxa, little is known about whether the different tactics have adapted to sperm competition risk. Chinook salmon, Oncorhynchus tshawytscha, have two ARTs: large males that participate in dominance‐based hierarchies for access to spawning females, known as hooknoses, and small males that attempt to sneak fertilizations during spawning events from peripheral positions, known as jacks. Jacks continually face sperm competition risk because they always spawn in the presence of another male, whereas hooknoses face relatively low sperm competition risk because other males are not always present during spawning events. Based on the sneak‐guard model of sperm competition this asymmetry in sperm competition risk predicts that jacks ought to invest significantly more into sperm‐related traits important for sperm competition success relative to hooknoses. In the present study we report on reproductive investment patterns, sperm characteristics, and seminal plasma physiology of males that exhibit ARTs in Chinook salmon. We found that jacks invest significantly more of their somatic tissue into gonads compared with hooknoses. Sperm velocity also varied significantly between the ARTs, with jacks having significantly faster sperm than hooknoses. No significant differences in seminal plasma physiology metrics related to sperm quality were detected between the ARTs. We interpret these sperm investment patterns in light of the sneak‐guard model of sperm competition that is based on differences in sperm competition risk and alternative investment possibilities among ARTs. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Intraspecific variation in sand-diving and predator avoidance behavior of green razorfish,Xyrichtys splendens (Pisces,Labridae): effect on courtship and mating success

Synopsis Green razorfish are Caribbean wrasses that live in harems on shallow sand or seagrass beds, which offer little cover for predator avoidance (PA). Field observations showed that non-conspecific fishes that intruded were either attacked, ignored, or actively avoided. Food competitors and small piscivores were attacked by male razorfish. Razorfish PA behaviors varied among three habitats with different substratum compositions, suggesting that these fish possess phenotypic plasticity for PA behavior. In a rocky-rubble habitat, razorfish dove into the coarse sand for PA, but most sand dives observed there were to soften a small site for future PA. In a sandbed habitat, they hid among coral branches and dove into the sand when attacked; few maintenance dives were observed as soft sand was widespread. In a seagrass habitat, they hid among blades of grass for PA, and dove into the sand less frequently than at the other sites. Some female razorfish that were transferred among habitats adopted PA behaviors similar to those of females in the new site, while others did not, suggesting that behavioral plasticity is not universal in this species. Razorfish spawned lower in the water column in the presence of natural predators and a predator model, than when these were absent. When the predator model was introduced into a male's territory during spawning periods, there was a reduction in his courtship rate, but not in the number of spawns he achieved. Predation pressure may reduce males' long-term fitness by causing decreased courtship rates which can facilitate sex change in harem females.     

Swimming patterns and behaviour of upriver-migrating adult pink (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by EMG telemetry in the Fraser River,British Columbia,Canada

Little is known about the behaviour patterns and swimming speed strategies of anadromous upriver migrating fish. We used electromyogram telemetry to estimate instantaneous swimming speeds for individual sockeye (Oncorhynchus nerka) and pink salmon (O. gorbuscha) during their spawning migrations through reaches which spanned a gradient in river hydraulic features in the Fraser River, British Columbia. Our main objectives were to describe patterns of individual-specific swim speeds and behaviours, identify swimming speed strategies and contrast these between sexes, species and reaches. Although mean swimming speeds did not differ between pink salmon (2.21 BL s^–1) and sockeye salmon (1.60 BL s^–1), sockeye salmon were over twice as variable (mean CV; 54.78) in swimming speeds as pink salmon (mean CV; 22.54). Using laboratory-derived criteria, we classified swimming speeds as sustained (<2.5 BL s^–1), prolonged (2.5–3.2 BL s^–1), or burst (>3.2 BL s^–1). We found no differences between sexes or species in the proportion of total time swimming in these categories – sustained (0.76), prolonged (0.18), burst (0.06); numbers are based on species and sexes combined. Reaches with relatively complex hydraulics and fast surface currents had migrants with relatively high levels of swimming speed variation (e.g., high swimming speed CV, reduced proportions of sustained speeds, elevated proportions of burst speeds, and high rates of bursts) and high frequency of river crossings. We speculate that complex current patterns generated by river constrictions created confusing migration cues, which impeded a salmon's ability to locate appropriate pathways.     

Cellular responses of the skin and changes in plasma cortisol levels of trout (Oncorhynchus mykiss) exposed to acidified water

The skin structure and the plasma cortisol levels of trout, Oncorhynchus mykiss, were examined during 7 days of exposure to water of pH 5. By day-4 and-7, the thickness of the epidermis was significantly (P<0.05) less in acid exposed fish than in controls, and degenerative cells were common in the upper epidermal layers. Many epidermal cells exhibited signs of necrosis, and by day-7 many apoptotic cells were also present. Secretory vesicles of high electron density were abundant in the filament cells of the 3–4 outermost layers of epidermis, and intercellular spaces had increased. Mitotic figures occureed throughout the epidermis, with the exception of the outermost cell layer. Mucous cells became elongated after day-1, and later, newly differentiating mucous cells could be seen close to the skin surface, and many mucocytes contained mucosomes of high electron density. Rodlet cells were occasionally seen. Chloride cells appeared similar to those of control fish. Many leucocytes, mainly macrophages and lymphocytes, had penetrated the epidermis via the highly undulating basal lamina, and at day-7, numerous apoptotic lymphocytes were found. In the dermis, melanosomes became dispersed in the cytoplasmic extensions of melanocytes which were present in the epidermis of all acid-exposed fish. Iridocytes were rate after day-4, while fibroblasts were abundant and secreted large amounts of collagen. After 1 day of exposure to acidified water, a significant (P<0.05) elevation of the plasma cortisol level had occurred, but this subsequently declined, and had returned to control values by day-7. The changes in skin structure, however, remained throughout the whole exposure period.     

A pilot study of the social correlates of levels of urinary cortisol,prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis)

Urine samples were collected from individuals in a wild population of Sumatran long-tailed macaques (Macaca fascicularis), and the levels of cortisol, immunoreactive prolactin, and (for males) testosterone were determined. The amount of foraging during the 2 hr preceding urine collection were found to affect the levels of urinary cortisol, but not those of the other hormones. Immigration into a new group and having one's infant kidnapped led to increased levels of cortisol. Levels of cortisol and testosterone were correlated both within and between individuals, whereas prolactin varied independently. The effects of age, reproductive status, and social rank on the mean values of individuals were also examined. Lactating females had higher prolactin levels than non-lactating ones; reproductive state interacted with the age effect on prolactin and possibly cortisol. No effects of social status were found in spite of a small, but consistent effect of rank on birth rate in this population. Among males, age and rank are strongly linked. The low ranking old males had increased levels of cortisol, even though the younger high-ranking males were involved in the fiercest conflicts.     

The effect of somatostatins (SRIF-14, 25 and 28), galanin and anti-SRIF on plasma growth hormone levels in Coho salmon (Oncorhynchus kisutch, Walbaum)

Porcine galanin, somatostatins (SRIF-25 and SRIF-28) and invariant SRIF-14, known to have inhibitory-stimulatory actions on growth hormone (GH) secretion in higher vertebrates, were tested for their ability to affect plasma GH levels in coho salmon. Peptides were administered by intraperitoneal injection of 10 or 100 ng g⁻¹ body weight. All three SRIFs decreased plasma GH concentrations, their activity following the order SRIF-14 > SRIF-28 > SRIF-25. Galanin and an anti-SRIF produced pronounced, although transient increases in plasma GH.