Brian R. Beckman

Previtellogenic Oocyte Growth in Salmon: Relationships among Body Growth, Plasma Insulin-Like Growth Factor-1, Estradiol-17beta, Follicle-Stimulating Hormone and Expression of Ovarian Genes for Insulin-Like Growth Factors, Steroidogenic-Acute Regulatory Protein and Receptors for Gonadotropins, Growth Hormone, and Somatolactin

Abstract Body growth during critical periods is known to be an important factor in determining the age of maturity and fecundity in fish. However, the endocrine mechanisms controlling oogenesis in fish and the effects of growth on this process are poorly understood. In this study interactions between the growth and reproductive systems were examined by monitoring changes in various components of the FSH-ovary axis, plasma insulin-like growth factor 1 (Igf1), and ovarian gene expression in relation to body and previtellogenic oocyte growth in coho salmon. Samples were collected from females during two hypothesized critical periods when growth influences maturation in this species. Body growth during the fall-spring months was strongly related to the degree of oocyte development, with larger fish possessing more advanced oocytes than smaller, slower growing fish. The accumulation of cortical alveoli in the oocytes was associated with increases in plasma and pituitary FSH, plasma estradiol-17beta, and ovarian steroidogenic acute regulatory protein (star) gene expression, whereas ovarian transcripts for growth hormone receptor and somatolactin receptor decreased. As oocytes accumulated lipid droplets, a general increase occurred in plasma Igf1 and components of the FSH-ovary axis, including plasma FSH, estradiol-17beta, and ovarian mRNAs for gonadotropin receptors, star, igf1, and igf2. A consistent positive relationship between plasma Igf1, estradiol-17beta, and pituitary FSH during growth in the spring suggests that these factors are important links in the mechanism by which body growth influences the rate of oocyte development.

Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes

Many physiological processes are modulated by the endocrine system, including growth. Insulin-like growth factor 1 is one of the primary hormones involved in growth regulation in vertebrates, including fishes. Current work on IGF1 in fishes is driven both by a desire to better understand mechanisms of growth as well as to develop a reliable index of growth rate. A review of studies relating IGF1 to growth broadly reveals positive and significant relations between IGF1 and growth; however, relations found in individual studies range from no correlation to highly significant correlations. Potential sources for this variation include both biological and methodological issues and range from differences in how growth is defined (changes in length or weight), the duration of growth assessed (weeks to months) and how growth is calculated (total change, rate, percent change); yet, these methodological concerns cannot account for all the variation found. A further review of the literature reveals a number of physiological conditions and environmental factors that might influence IGF1 level and the subsequent relation of that IGF1 level to growth rate. The term concordance is introduced to categorize factors that influence IGF1 and growth in a similar fashion, such that positive and significant relations between IGF1 and growth are maintained even though the factor stimulates changes in IGF1 level. Conversely, the term discordance is introduced to categorize factors that stimulate changes in the relations between IGF1 and growth, such that IGF1 is not an efficacious index of growth for both pre and post-stimulus fish combined. IGF1 and growth relations generally remain concordant after changes in nutrition (consumption rate or diet). Differences in IGF1 level of juvenile, maturing male and maturing female fish are common and IGF1-growth relations appear discordant between these groups. Acute changes in temperature and salinity induce discordant relations between IGF1 and growth but acclimation to persistent differences in environmental condition generally result in concordant relations. Overall, by discriminating between fish of differing physiological status and discerning and categorizing differences among environments one may effectively use IGF1 as a growth index for fishes.

The role of growth in endocrine regulation of salmon smoltification

Keywords: growth, salmon, smoltification, insulin, insulin-like growth factor I (IGF-I), growthhormone, thyroxine, photoperiod, temperature, nutritioncreases hepatic IGF-I mRNA (Cao et al. 1989;Sakamoto and Hirano 1993; Duan et al. 1994) andelevates blood IGF-I levels (Moriyama et al.1994). The majority of IGF-I in salmonid blood isprobably bound to specific binding proteins(IGFBPs), some of which are influenced by GH,insulin and nutrition (Kelley et al. 1992; Siharathand Bern 1993). The IGFBPs in blood and in tis-sues surrounding target cells undoubtedly play asignificant role in modifying the action of IGF-Iin fish, as they do in mammals, although this islargely unexplored in the context of salmon smol-tification. IGF-I inhibits GH release by negativefeedback, as shown

Endocrine Biomarkers of Growth and Applications to Aquaculture: A Minireview of Growth Hormone, Insulin-Like Growth Factor (IGF)-I, and IGF-Binding Proteins as Potential Growth Indicators in Fish

Abstract Growth in fish and other vertebrates is under endocrine control, particularly through the growth hormone (GH)–insulin-like growth factor (IGF) axis. For this reason, it has been of interest to aquaculture researchers and the industry to establish endocrine biomarkers that can both reflect and predict growth rates in fish subject to various biotic and abiotic manipulations. Ultimately, by understanding the hormones that control growth and utilizing them as biomarkers, we hope to achieve optimal growth conditions in the aquaculture environment with less need for lengthy and costly grow-out trials. While the most appropriate endocrine biomarkers for growth can be both species and situation specific, IGF-I may be the most promising candidate for measuring instantaneous growth in fish. This is based on the direct contributions of IGF-I in regulating cell proliferation and ultimately somatic growth, along with its previously established correlations with the specific growth rate in fish under various c...

Assessment of High Rates of Precocious Male Maturation in a Spring Chinook Salmon Supplementation Hatchery Program

Abstract The Yakima River Spring Chinook Salmon Supplementation Project in Washington State is one of the most ambitious efforts to enhance a natural salmon population currently under way in the United States. Over the past 5 years we have conducted research to characterize the developmental physiology of natural and hatchery-reared wild progeny spring Chinook salmon Oncorhynchus tshawytscha in the Yakima River basin. Fish were sampled at the main hatchery in Cle Elum, at remote acclimation sites, and, during smolt migration, at downstream dams. Throughout these studies, we characterized the maturational state of all fish using combinations of visual and histological analyses of testes, computation of gonadosomatic indices, and measurement of plasma 11-ketotestosterone (11-KT). We established that a plasma 11-KT threshold of 0.8 ng/mL can be used to designate male fish as either immature or precociously maturing approximately 8 months prior to final maturation (1–2 months prior to release as “smolts”). Ou...

Physiological Status of Naturally Reared Juvenile Spring Chinook Salmon in the Yakima River: Seasonal Dynamics and Changes Associated with Smolting

Abstract Two year-classes of juvenile spring chinook salmon Oncorhynchus tshawytscha from the Yakima River, Washington, were sampled from July (3–4 months postemergence) through May (yearling smolt out-migration). Physiological characters measured included liver glycogen, body lipid, gill Na+-K+ ATPase, plasma thyroxine (T4), and plasma insulin-like growth factor-I (IGF-I). Distinct physiological changes were found that corresponded to season. Summer and fall were characterized by relatively high body lipid and condition factor. Winter was characterized by decreases in body lipid, condition factor, and plasma hormones. An increase in condition factor and body lipid was found in February and March. Finally, April and May were characterized by dramatic changes characteristic of smolting, including increased gill Na+-K+ ATPase activity, plasma T4, and IGF-I and decreased condition factor, body lipid, and liver glycogen. These results create a physiological template for juvenile spring chinook salmon in the d...

Growth, smoltification, and smolt-to-adult return of spring chinook salmon from hatcheries on the Deschutes River, Oregon

Abstract The relationship between smoltification and smolt-to-adult return (SAR) of spring chinook salmon Oncorhynchus tshawytscha from the Deschutes River, Oregon, was examined for four release groups in each of three successive years. Fish were reared, marked with coded wire tags, and released from Round Butte Hatchery, Pelton Ladder rearing facility, and Warm Springs National Fish Hatchery. Smolt releases occurred in nearly the same place at similar times, allowing a direct comparison of SAR to several characters representing smolt quality. Return rates varied significantly among facilities, varying over an order of magnitude each year. The highest average SAR was from Pelton Ladder, the lowest was from Warm Springs. Each of the characters used as metrics of smoltification—fish size, spring growth rate (February–April), condition factor, plasma hormone concentration (thyroxine, cortisol, and insulin-like growth factor-I [IGF-I]), stress challenge, gill Na+, K+-ATPase activity, and liver glycogen concen...

Relation of Fish Size and Growth Rate to Migration of Spring Chinook Salmon Smolts

Abstract We examined the relation of size and growth rate to downstream migration in yearling spring chinook salmon Oncorhynchus tshawytscha. A group of juvenile chinook salmon was graded by size into small and large categories; half the fish in each category were reared at an elevated temperature beginning in mid-February, resulting in four distinct treatment groups: large–warm, large–cool, small–warm, and small–cool. Fish from warmwater treatment groups displayed significantly higher growth rates through the spring than coolwater groups. Fish were released into a natural creek on two dates (25 March, release 1 and 12 April, release 2), and downstream movement was monitored. For each release, fish that migrated past a weir within the first 5 d postrelease had significantly higher spring growth rates than fish that did not migrate within that period. A similar comparison of release length to migration demonstrated significant differences only in release 2. Also for release 2, fish from the large–warm and ...

Big dams and salmon evolution: changes in thermal regimes and their potential evolutionary consequences

Dams designed for hydropower and other purposes alter the environments of many economically important fishes, including Chinook salmon (Oncorhynchus tshawytscha). We estimated that dams on the Rogue River, the Willamette River, the Cowlitz River, and Fall Creek decreased water temperatures during summer and increased water temperatures during fall and winter. These thermal changes undoubtedly impact the behavior, physiology, and life histories of Chinook salmon. For example, relatively high temperatures during the fall and winter should speed growth and development, leading to early emergence of fry. Evolutionary theory provides tools to predict selective pressures and genetic responses caused by this environmental warming. Here, we illustrate this point by conducting a sensitivity analysis of the fitness consequences of thermal changes caused by dams, mediated by the thermal sensitivity of embryonic development. Based on our model, we predict Chinook salmon likely suffered a decrease in mean fitness after the construction of a dam in the Rogue River. Nevertheless, these demographic impacts might have resulted in strong selection for compensatory strategies, such as delayed spawning by adults or slowed development by embryos. Because the thermal effects of dams vary throughout the year, we predict dams impacted late spawners more than early spawners. Similar analyses could shed light on the evolutionary consequences of other environmental perturbations and their interactions.

Growth Modulation Alters the Incidence of Early Male Maturation and Physiological Development of Hatchery-Reared Spring Chinook Salmon: A Comparison with Wild Fish

Abstract Previous studies conducted at the Cle Elum Spring Chinook Salmon Supplementation Hatchery in Washington State demonstrated that 37–49% of the male Chinook salmon Oncorhynchus tshawytscha released from this facility in its first years of operation precociously matured at age 2 rather than the more typical age 4. We examined the effects of altering seasonal growth rate on the incidence of age-2 male maturation in an experimental subset of that population and compared their physiological development (size, growth rate, condition factor, whole-body lipid, gill Na+,K+-ATPase activity, and plasma insulin-like growth factor-I [IGF-I]) with that of both hatchery (production) and wild fish. Altering summer and autumn rations resulted in four growth trajectories with the following size and precocious male maturation rates: The high summer—high autumn growth trajectory produced fish averaging 25 g and 69% precocious maturation; the high summer—low autumn trajectory yielded fish that averaged 18 g and exhibi...