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Article

Heterogeneity of Biochemical Parameters of Non-Native Pink Salmon Oncorhynchus gorbuscha Spawners at the Beginning of Up-River Movements

by
Ekaterina V. Ganzha
*,
Dmitry S. Pavlov
and
Efim D. Pavlov
*
Institute of Ecology and Evolution A.N. Severtsov of the Russian Academy of Sciences—IEE RAS, 119071 Moscow, Russia
*
Authors to whom correspondence should be addressed.
Water 2024, 16(14), 2000; https://doi.org/10.3390/w16142000
Submission received: 11 June 2024 / Revised: 10 July 2024 / Accepted: 12 July 2024 / Published: 15 July 2024
(This article belongs to the Special Issue Exotic Species in Aquatic Environments)
Versions Notes

Abstract

:
In the last decades, non-native pink salmon Oncorhynchus gorbuscha successfully spread and occupied the rivers of the White Sea basin. We studied twenty-two blood parameters characterizing lipid metabolism, osmoregulation, energy exchange, and steroidogenesis at the crucial time point of pink salmon spawning migration: the passage of the critical salinity barrier in the estuary, preceding the migration upstream of the Umba River. The heterogeneity of biochemical parameters of non-native pink salmon predominantly was demonstrated in sexual dimorphism. We attributed this result to two main processes: maturation features and different timings of fish running from seawater to freshwater. Maturation features were characterized by differences between females and males in concentrations of estradiol-17β, triglycerides, and alanine aminotransferase. Both sexes had increased levels of cortisol due to changes in fish osmoregulation. Females had higher levels of cortisol, total protein, and calcium in comparison with males, which indicated that pink salmon females run to the river later than males.

1. Introduction

Pink salmon Oncorhynchus gorbuscha is a pacific semelparous species, whose range has expanded due to the invasion into the Great Lakes [1,2] and introduction to the White Sea basin [3,4]. Within the latter, pink salmon initially used the Umba River (Murmansk Region, Russia) as a spawning area. Subsequently, pink salmon expanded its range and occupied new watercourses of the White Sea basin most likely due to the ability to adapt to non-natal stream odors [3,5]. Nowadays, non-native pink salmon successfully widely spread to the Barents Sea basin, waters of Norway, Iceland, and Great Britain islands [6,7,8], and even across the ocean to North America [9]. It seems that pink salmon have the potential to spread further in the North water ecosystems, which was consistent with previous reports [9,10].
The introduction of non-native pink salmon could have a significant impact on native species and watershed productivity. According to Ruggerone and Nielsen [11], the abundance of hatchery-produced and wild pink salmon was associated with a reduction in other Pacific salmonids such as chum salmon (Oncorhynchus keta) and sockeye salmon (Oncorhynchus nerka). Hypothetically, a large population of non-native pink salmon may decrease the production and abundance of Atlantic salmon (Salmo salar), brown trout (Salmo trutta), and Arctic charr (Salvelinus alpinus) [9]. Pink salmon appear to exhibit higher plasticity compared to some other salmonids, which suggests that rapid evolutionary processes and high adaptation of pink salmon in the White Sea basin have resulted in phenotypes different from its original population [12].
A key factor in the successful reproduction and spread of non-native pink salmon in a new habitat is the timing of river entrance and spawning. Strong preference for late autumn spawning could potentially enable pink salmon to succeed in the rivers of the Atlantic basin [9], potentially overlapping with the spawning periods of native salmonids such as Atlantic salmon and brown trout, with unpredictable consequences for these species. Conversely, climate change could synchronize spawning times between native and non-native salmonids due to earlier adult migration to rivers [13,14]. Climate warming has negatively affected native fish [15]. However, the spread of non-native pink salmon could accelerate as warmer annual water temperatures no longer inhibit its population expansion in the rivers of the White Sea [12].
Given the potential risks associated with the transformation of spawning timings in pink salmon, it is crucial to consider biochemical divergence in adult pink salmon and its relationship with river entrance and physiological readiness for spawning. Currently, there is only one study focusing on the physiological state of a broad population of non-native pink salmon during spawning migration in the Northwest Region of Russia [4]. Based on the potential risks of spawning timings’ transformation of pink salmon, it is necessary to assume biochemical divergence in adult pink salmon and its relation with the river entrance and physiological preparation to spawning. Until now, there was a single study aimed at the physiological state of the wide population of non-native pink salmon during spawning migration in the Northwest Region of Russia [4]. In this study, we examined a complex of twenty-two biochemical blood parameters that characterize the endocrine and biochemical status of non-native White Sea pink salmon at a critical moment in its life cycle: the passage through the critical salinity barrier prior to upstream migration to spawning grounds in the Umba River and final maturation. In particular, we analyzed the level of thyroid hormones, parameters of lipid and protein metabolism as indicators of the energy exchange, and overall metabolic rate [16,17,18]. Additionally, we measured the content of steroid hormones—cortisol, testosterone, and estradiol, as indicators of stress and maturation state. Assuming that pink salmon experiences electrolyte deficiency after crossing the salinity barrier, we also measured concentrations of K+, Na+, Cl−, Ca2+, P+, and Mg2+, as indicators of fish osmoregulation. We hypothesize that a comprehensive analysis of these biochemical parameters would shed light on our understanding of the life history features of pink salmon in a new environment.
The study aimed to estimate the heterogeneity of the endocrine and biochemical status of the pink salmon population in its distribution during a crucial time point of their life cycle: passing the critical salinity barrier associated with final preparation to single spawning in their ontogeny.

2. Materials and Methods

2.1. Field Study

The study was conducted on 14 July 2021, focusing on the pink salmon in the Umba River during the peak of their spawning migration in the region. The Umba River has a length of 123 km with a total catchment area of 6250 km2 [19]. The water temperature in the river was 16 °C during sampling.
To capture adult pink salmon, we used 24 h recreational fishing licenses (21-y No. 006608 and 21-y No. 006609 from 14.07.2021). Fish were captured two kilometers from the sea (66°40′49″ N 34°18′35″ E) using two fishing rods in the evening (from 18:00 to 23:00). In total, forty-seven fish were caught, comprising 23 females and 24 males.

2.2. Blood Sampling

Individual blood sampling was conducted less than five minutes after fish capture. After the capture, each fish was placed in a 10 L container filled with river water and covered with moist multilayer surgical gauze, as an alternative to fish holding bags [20]. One person handled the fish using wet textile gloves to protect pink salmon from the heat shock. Another person sampled the blood with a single puncture of the caudal vessel using disposable 3 mL syringes. Each sampling procedure lasted 1–2 min for fish. We did not use anesthetics before blood sampling due to express manipulations according to blood sample protocol [20,21] and the possibility of the potential impacts of anesthetics on biochemical results [22,23,24]. Immediately after blood sampling, the fish were euthanized by decapitation, and their sex, fork length, and body weight were assessed for each fish.
Each individual blood sample with a total volume of 2.5–3.0 mL was divided equally into two 2 mL tubes. One hour later, the serum was separated by centrifugation (2000 rpm) for five minutes. Individual serum samples were poured into new tubes, labeled, stored, and transported to the laboratory at −20 °C in a portable fridge freezer, Waeco CFX-40W.

2.3. Biochemical Analysis

In the laboratory, serum samples were thawed at room temperature. Commercial enzyme-linked immunosorbent assay (ELISA) kits from DRG-international (Germany) were used to analyze total triiodothyronine (T3), total thyroxine (T4), cortisol (Crt), testosterone (Ts), and estradiol-17β (E). The level of hormone in each individual sample was measured in duplicate using ELISA equipment (Mindray, China). Ratios of T4/T3 and Ts/E were calculated to assess the rate of conversion of T4 to T3 (deiodination) and Ts to E, respectively.
We determined another seventeen blood parameters using an automatic biochemistry analyzer iMagic-S7 (Shenzhen iCubio BioMedical Technology, Shenzhen, China). Lipid metabolism was evaluated through cholesterol (CHOL), phospholipids (PL), triglycerides (TGs), non-esterified fatty acids (NEFA), low-density lipoproteins (LDL), and high-density lipoproteins (HDL). Protein metabolism was evaluated by total protein (TP), creatinine (CREA), alanine aminotransferase (ALT), urea (UREA), and glucose (GLU). The concentrations of electrolytes K+, Na+, Cl−, Ca2+, P+, and Mg2+ were determined to estimate fish osmoregulation after their movement from seawater to freshwater. We used commercial biochemical kits: BSBE (Beijing, China) for K+, Na+; DiaSys (Holzheim, Germany) for PL, NEFA, LDL, and HDL; and Diakon-Vet (Russia) kits were used for CHOL, TGs, TP, CREA, ALT, UREA, GLU, Cl−, Ca2+, P+, and Mg2+.
Statistical data analysis was conducted using Minitab 18.1. The Shapiro–Wilk test assessed normality distribution of samples. Student’s t-test and Kruskal–Wallis H test were used to register significant differences in morphological (fish length and weight) and biochemical parameters. Correction for multiple comparisons was carried out by Holm’s sequential Bonferroni procedure. We used Spearmen rank correlation to find statistical dependence between different biochemical parameters and fish morphological features (sex, length, and weight).
All procedures with fish adhered to the guidelines, laws, and ethical standards of the Russian Federation. The bioethics commission for the regulation of experimental research of the Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences approved the original study based on the Provisions of the commission dated 13 June 2017 (paragraph 1.3) (https://sev-in.ru/en/komissia-po-bioetike) (accesed on 14 July 2024).

3. Results

3.1. Fish Length and Weight

Pink salmon females had a fork length of 45 ± 0.7 (40–51) cm and a body weight of 1104 ± 58.8 (740–1960) g (values before brackets represent mean value and its error; in brackets represent min and max). Males had a fork length of 47 ± 0.8 (41–53) cm and a body weight of 1227 ± 67.2 (640–1880) g. The length and weight of males and females did not significantly differ (Student t-test: p > 0.055).

3.2. Thyroid and Steroid Hormones

Estimated serum thyroid hormone varied significantly (Table 1). The level of T3 was highly correlated with the concentration of T4 in both males and females (rs = 0.68, p < 0.001).
Females exhibited significantly higher concentrations of E (2.9 times), Crt level (3.4 times) and lower Ts/E ratio (3.0 times) compared to males (Kruskal–Wallis H test: H3; 39 = 15.92; p = 6.6 × 10−5; H3; 39 = 13.14; p = 2.9 × 10−4; H3; 41 = 11.37; p = 7.4 × 10−4, respectively) (Table 1). Concentrations of E correlated positively with Ts levels (rs = 0.59, p = 0.007) in females. The level of Crt correlated positively with concentrations of Ts (rs = 0.59, p = 0.020) and E (rs = 0.74, p = 0.002) in females.

3.3. Parameters of Lipid Metabolism

Females had significantly higher (1.4 times) concentrations of TGs (Kruskal–Wallis H test: H3; 47 = 14.67; p = 1.3 × 10−4) and significantly lower (1.2 times) levels of HDL (Kruskal–Wallis H test: H3; 45 = 14.38; p = 1.5 × 10−4) compared to males (Table 2). The level of TGs correlated positively with concentrations of NEFA (rs = 0.51, p = 0.003) and negatively with HDL (rs = −0.52, p < 0.001) in both sexes. NEFA concentrations were highly correlated with concentrations of TGs (rs = 0.66, p = 0.007) and PL (rs = 0.71, p = 0.003) in females.

3.4. Protein Exchange Parameters

Females had significantly higher (1.2 times) concentrations of TP (Kruskal–Wallis H test: H3; 46 = 15.29; p = 9.2 × 10−5) and significantly lower (1.2 times) levels of ALT (Kruskal–Wallis H test: H3; 47 = 13.48; p = 2.4 × 10−4) compared to males (Table 3). The level of GLU and UREA correlated positively with concentrations of T3 (rs = 0.61, p = 0.005 and rs = 0.55, p = 0.013, respectively) in females.

3.5. Electrolyte Parameters

Females had significantly higher concentrations of K+ (1.3 times) and Ca2+ (1.5 times) (Kruskal–Wallis H test: H3; 37 = 8.87; p = 0.003; H3; 38 = 19.75; p = 8.8 × 10−6, respectively) and lower level of Na+ (Kruskal–Wallis H test: H3; 37 = 7.15; p = 0.008) compared to males (Table 4). In females, the levels of K+ negatively correlated with concentrations of Na+ (rs = − 0.64, p = 0.004) and highly positively correlated with the levels of NEFA (rs = 0.78, p = 0.004). The levels of Ca2+ correlated positively with TP (rs = 0.67, p = 0.002) and PL (rs = 0.62, p = 0.006); concentrations of P+ correlated positively with CHOL levels (rs = 0.64, p = 0.005) in females.

4. Discussion

We characterized a physiological status of adult pink salmon after their entering to the Umba River for spawning migration and revealed sexual dimorphism in hormonal and biochemical parameters.
The variables of the studied thyroid hormones’ concentrations in pink salmon from the Umba River were comparable to those observed in pink salmon in the Keret River at the same time point [4]. In our study, the levels of cholesterol, triglycerides, total protein, and creatinine in pink salmon were similar to the values reported in Atlantic salmon Salmo salar adults maintained in a sea net pen [25]. Also, the values of glucose, triglycerides, cholesterol, and some electrolytes (P+, Ca2+, Cl−) in our study were similar to the observed values in adult cultivated rainbow trout Oncorhynchus mykiss [26]. Based on the similar biochemical values, we suggest that there are no critical differences in blood parameters amongst closely related salmonid species during the same ontogeny period under different external conditions.
We identified numerous endocrine and metabolic blood parameters that characterized sexual dimorphism in non-native pink salmon. These differences demonstrate physiological adaptations of males and females influenced by internal and external factors. Further in the article, we focus on biochemical parameters that distinguished differences between females and males, exploring potential reasons for these disparities. Each parameter could regulate multiple functions, and its concentration in blood varies due to different internal and external factors. During migration, salmon experience significant shifts in their environment including salinity, temperature fluctuations, water chemistry changes, olfactory cues, and variations in flow dynamics. These factors, as well as physiological and developmental shifts associated with starvation, maturation, and senescence, can create a complex, interacting matrix of processes [27]. We suggest that two primary factors contribute to the observed sexual dimorphism of pink salmon during this studied time point: differences in maturation processes and variations in the timing of spawners’ runs to the river.

4.1. Parameters Related to Maturation

The primary evolutionary drive for upstream migration in salmonid fish, such as pink salmon, is successful spawning to reproduce new generations. Final maturation in salmonids is achieved in freshwater and regulated by steroidogenesis and synthesis of steroid sex hormones and their metabolism [28,29]. Steroidogenesis is a complex process of conversion of cholesterol to biologically active steroid hormones involving multiple enzymes [30]. In the current study, we did not find any differences between pink salmon males and females in the cholesterol levels. However, adult females had significantly higher estradiol-17β concentration and lower Ts/E ratio than males due to intensive testosterone conversion at the beginning of the spawning run to the river [4]. The sexual dimorphism was more pronounced in the concentration of estradiol-17β in comparison with the level of testosterone.
Females had a higher level of triglycerides and lower concentration of high-density lipoproteins in comparison with males because triglycerides are insoluble in water, and their transport is possible within protein complexes [31]. Therefore, females and males differ in transport volume intensity and the aggregation process of triglycerides in the blood. Increased concentration of triglycerides in pink salmon females probably reflects the lipid transport and aggregation into oocytes prior to spawning. Salmon eggs contain not only phospholipids but also neutral lipids, mainly triglyceride, which may play an important role in the development of embryos and juvenile fish [32]. In the current study, levels of total protein varied based on the concentrations of circulating vitellogenin, which is a very high-density lipoprotein (d > 1.21 g/mL) and was detected in the blood of numerous fish species during their normal reproductive cycle [33]. Vitellogenin is mostly transported via blood and accumulates in eggs during vitellogenesis [32]. Because of this, serum vitellogenin concentrations and, respectively, serum total protein were higher in the blood of females than males.
In our investigation, females had a lower concentration of alanine aminotransferase than males, which is likely related to different energy investment in the reproduction of females and males [16,34]. Mommsen et al. [35] suggested that ALT and malic enzyme’s function in the Krebs Cycle is to sustain essential biochemical functions in the course of the spawning migration of salmonids: ALT, along with the other ten enzymes, approximately halved over the migration distance of salmon. Perhaps, ALT participates in energy regulation of fish maturation and movement to the spawning grounds.

4.2. Parameters Related to Osmoregulation

We did not observe differences between sexes in thyroid levels, primarily due to their strong individual variations. These results correspond with the earlier study indicating that there was no difference in concentrations of thyroid hormones between pink salmon males and females during spawning migration [4]. It seems that individual variability of thyroid hormones values is related to the different timing of fish runs to the river and high response of the thyroid axis movement passing through the critical salinity barrier. Despite their osmoregulatory and metabolic actions, thyroid hormones may fine-tune these processes in accordance with the actions of stress hormones such as cortisol and adrenaline [36]. Both osmolality and ion levels may be influenced by a range of stressors, including changes in salinity water. Water salinity changes primarily affect the sympathetic nervous system and endocrine system with cortisol concentration rising [37,38]. Our results show that pink salmon were stressed after they passed the critical salinity barrier. The cortisol levels in studied pink salmon correspond with observations of this parameter in stressed salmonid fish, in which cortisol concentrations could increase up to 40 times in comparison with unstressed fish [37]. In our study, cortisol concentration in pink salmon females was significantly higher than in males. The causes of this difference could be due to different times at which males and females enter the river from the sea. We hypothesize that females with higher levels of cortisol entered the Umba River later than males with lower cortisol concentrations, i.e., the males spent more time in freshwater than females. That is, the homeostasis of males was already stabilized and accompanied by a decrease in osmotic stress and cortisol levels. The hypothesis is consistent with information that males of pink salmon occurred in greater numbers than females at the beginning of the spawning run in McClinton Creek of British Columbia [39]. Also, the level of cortisol decreased in fish always when they entered the river [40]. According to Jonsson and Jonsson [41], brown trout Salmo trutta males access the spawning grounds earlier and stay there longer than females. Early run to freshwater males were observed for coho salmon Oncorhynchus kisutch and rainbow trout Oncorhynchus mykiss [42], spawning kokanee (sockeye salmon, Oncorhynchus nerka) [43], and some other salmonids [44]. Other data [45] presented the first run of brown trout females to the river in comparison with males.
Other results of our study confirmed the hypothesis of unsynchronized males and females running to the freshwater. We found lower concentrations of high-density lipoproteins in pink salmon females in contrast with males. These data indicate that differences in osmoregulatory processes linked to HDL remodeling are likely a primary mechanism for maintaining osmotic homeostasis in fish [46,47]. As mentioned before, pink salmon females had higher levels of total protein than males. According to Fletcher et al. [48], the concentration of total protein decreased during the transit of sockeye salmon adults from seawater to freshwater spawning grounds, and the decline in males was more rapid than in females. In the course of spawning migration, the fish degraded almost all their lipids and about half their white muscle mass, replenishing the lost protein with water to maintain their mass and external shape [17,27,40]. More intensive muscle degradation in pink salmon males in comparison with females (low total protein) indirectly supports our hypothesis of their earlier run to the freshwater.
The freshwater environment with lower ion levels (Na+, Cl−, or Ca2+) relative to fish body fluids generally results in passive ion losses to the environment that must be compensated by active uptake to maintain ionic homeostasis [49,50]. The difference in serum concentration of several electrolytes (K+, Na+, and Ca2+) in pink salmon males compared with females could be explained by their prolongated stay in freshwater. Cooke et al. [40] found that plasma Na+ was higher, with non-significant differences of K+ and Cl− in sockeye salmon entering the river. In our study, we caught fish in the river only, but Na+ was higher in males than in females. A similar phenomenon was registered for calcium concentration, which was higher in pink salmon males as well. However, during upstream river movement, the calcium concentration could be decreased in both sexes, as was shown in sockeye salmon spawners [51].

4.3. Correlations of Blood Parameters

The studied blood parameters of adult pink salmon weakly correlated with their length and weight. High statistical correlations were found between blood parameters in females compared to males. It could be related to the high level of hypoosmotic stress response in females due to the short time after their run to the freshwater. During osmotic stress, the compensatory effects of homeostasis could be observed in the metabolic system [33]. Spearmen correlation analyses revealed moderate-to-high relationships between endocrine regulation and metabolic process (T3–GLU, T3–UREA), electrolytes and lipid metabolism (K+–NEFA, Ca2+–PL, P+–CHOL), calcium and total protein in females. A strong positive correlation between T3 with T4 was found in both sexes of pink salmon due to the deiodination process and a high negative correlation of K+ and Na+, which characterized the osmoregulation of fish during hypoosmotic stress.

5. Conclusions

Our field observations and obtained biochemical results showed the heterogeneity of biochemical blood parameters between males and females of non-native pink salmon. These differences were likely based on pink salmon spawners’ sequence patterns of runs to the river Umba from the White Sea. High levels of cortisol, total protein, and calcium in females compared to males indicated that a pink salmon female runs to the river later than males. These patterns of sequence of male and female river runs are supported by the literature data on native pink salmon runs and runs of other salmonid species into the rivers. Also, we suggest that the biochemical blood parameters indicated features of sex differences in female and male maturation. The content of estradiol-17β, triglycerides, and ALT in blood mainly indicates the difference in maturation between males and females at the beginning of up-river movements. Observed heterogeneity of blood parameters of pink salmon could be useful as the first data in the assessment of their physiological divergence in the White Sea basin. The species plasticity could potentially increase their impact on native salmonids.

Author Contributions

E.V.G. and E.D.P. contributed to the study conception and design. Material preparation and data collection in the field were performed by E.D.P. and E.V.G. performed biochemical analysis and interpreted the results. The first draft of the manuscript was written by E.V.G., and E.D.P. and D.S.P. commented on previous versions of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

The sampling collection and biochemical analysis were supported by Russian Science Foundation No. 19-14-00015. Russian Science Foundation No. 24-14-00111 supported data analysis and manuscript preparation.

Data Availability Statement

Data generated or analyzed during this study are available from the corresponding author upon reasonable request. The data can be reused by citing the original paper.

Acknowledgments

We are grateful to F.N. Shkill (IEE RAS) for valuable comments that greatly improved the manuscript and to M.A. Ruchiev (IEE RAS) and K.I. Boiko (IEE RAS) for help with fish catching and materials sampling.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Concentrations of triiodothyronine (T3), thyroxine (T4), cortisol (Crt), testosterone (Ts), and estradiol-17β (E) in the blood serum of Oncorhynchus gorbuscha and values of T4/T3 and Ts/E ratios.
Table 1. Concentrations of triiodothyronine (T3), thyroxine (T4), cortisol (Crt), testosterone (Ts), and estradiol-17β (E) in the blood serum of Oncorhynchus gorbuscha and values of T4/T3 and Ts/E ratios.
ParametersFemalesMales
ValuenValuen
T3, ng/mL3.0 ± 0.62 (0.1–7.7)214.1 ± 0.69 (0.6–12.5)22
T4, ng/mL10.6 ± 2.38 (0.9–41.8)2114.0 ± 2.88 (1.5–54.6)22
T4/T36.5 ± 1.43 (0.7–21.6)213.9 ± 0.56 (1.0–10.4)22
Crt, ng/mL129 ± 33.4 (6–510) *2038 ± 14.7 (0.7–297) *22
Ts, ng/mL22.0 ± 1.15 (11.3–28.1)1919.0 ± 1.08 (10.2–25.8)21
E, ng/mL3.7 ± 0.26 (0.2–4.7) *191.3 ± 0.28 (0.2–5.1) *21
Ts/E9.2 ± 3.09 (3.5–64.0) *1927.4 ± 5.85 (3.8–116.2) *21
Note: * indicates significant differences (Kruskal–Wallis H test) in the values between sexes. n—number of samples; before brackets are the mean value and its error; in the brackets are min and max.
Table 2. Concentrations of cholesterol (CHOL), phospholipids (PL), triglycerides (TGs), non-esterified fatty acids (NEFA), low-density lipoproteins (LDL), and high-density lipoproteins (HDL) in the blood serum of Oncorhynchus gorbuscha.
Table 2. Concentrations of cholesterol (CHOL), phospholipids (PL), triglycerides (TGs), non-esterified fatty acids (NEFA), low-density lipoproteins (LDL), and high-density lipoproteins (HDL) in the blood serum of Oncorhynchus gorbuscha.
ParametersFemalesMales
ValuenValueN
CHOL, mmol/L12.5 ± 0.42 (9.5–16.1)2312.7 ± 0.43 (9.6–16.9)24
PL, mmol/L3.7 ± 0.03 (3.4–3.9)223.6 ± 0.03 (3.3–3.8)23
TGs, mmol/L4.4 ± 0.18 (2.9–6.2) *233.2 ± 0.17 (2.0–5.0) *24
NEFA, mmol/L0.4 ± 0.04 (0.1–0.7)160.4 ± 0.03 (0.2–0.6)19
LDL, mg/dL0.5 ± 0.03 (0.2–0.7)220.5 ± 0.03 (0.4–0.7)23
HDL, mg/dL3.2 ± 0.12 (2.5–4.7) *223.9 ± 0.11 (2.9–5.1) *23
Note: * indicates significant differences (Kruskal–Wallis H test) in the values between the sexes. n—number of samples; before brackets are the mean value and its error; in the brackets are min and max.
Table 3. Concentrations of total protein (TP), creatinine (CREA), glucose (GLU), alanine aminotransferase (ALT), and urea (UREA) in the blood serum of Oncorhynchus gorbuscha.
Table 3. Concentrations of total protein (TP), creatinine (CREA), glucose (GLU), alanine aminotransferase (ALT), and urea (UREA) in the blood serum of Oncorhynchus gorbuscha.
ParametersFemalesMales
ValuenValuen
TP, g/L58.3 ± 1.29 (45.4–68.5) *2349.5 ± 1.38 (37.2–63.2) *23
CREA, umol/L34.6 ± 2.87 (20.2–79.6)2335.1 ± 2.29 (22.5–58.0)23
GLU, mmol/L3.6 ± 0.25 (1.1–5.6)233.7 ± 0.24 (1.8–6.5)22
ALT, U/L71.5 ± 1.65 (54.4–88.5) *2382.1 ± 2.00 (56.1–92.1) *24
UREA, mmol/L16.4 ± 0.27 (13.6–18.6)2317.2 ± 0.28 (14.5–19.5)24
Note: * indicates significant differences (Kruskal–Wallis H test) in the values between the sexes. n—number of samples; before brackets are the mean value and its error; in the brackets are min and max.
Table 4. Concentrations of electrolytes in the blood serum of Oncorhynchus gorbuscha.
Table 4. Concentrations of electrolytes in the blood serum of Oncorhynchus gorbuscha.
ParametersFemalesMales
ValuenValuen
K+, mmol/L5.6 ± 0.36 (2.8–8.8) *184.2 ± 0.25 (2.6–7.1) *19
Na+, mmol/L161 ± 1.2 (152–171) *19167 ± 1.7 (147–176) *18
Cl−, mmol/L108 ± 0.9 (102–115)19110 ± 0.8 (102–118)20
Ca2+, mmol/L6.1 ± 0.23 (3.8–7.3) *184.1 ± 0.10 (3.5–5.6) *20
P+, mmol/L8.0 ± 0.09 (7.5–8.8)187.9 ± 0.13 (6.4–8.6)20
Mg2+, mmol/L2.1 ± 0.06 (1.6–2.5)192.1 ± 0.07 (1.6–2.8)19
Note: * indicates significant differences (Kruskal–Wallis H test) in the values between the sexes. n—number of samples; before brackets are the mean value and its error; in the brackets are min and max.
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Ganzha, E.V.; Pavlov, D.S.; Pavlov, E.D. Heterogeneity of Biochemical Parameters of Non-Native Pink Salmon Oncorhynchus gorbuscha Spawners at the Beginning of Up-River Movements. Water 2024, 16, 2000. https://doi.org/10.3390/w16142000

AMA Style

Ganzha EV, Pavlov DS, Pavlov ED. Heterogeneity of Biochemical Parameters of Non-Native Pink Salmon Oncorhynchus gorbuscha Spawners at the Beginning of Up-River Movements. Water. 2024; 16(14):2000. https://doi.org/10.3390/w16142000

Chicago/Turabian Style

Ganzha, Ekaterina V., Dmitry S. Pavlov, and Efim D. Pavlov. 2024. "Heterogeneity of Biochemical Parameters of Non-Native Pink Salmon Oncorhynchus gorbuscha Spawners at the Beginning of Up-River Movements" Water 16, no. 14: 2000. https://doi.org/10.3390/w16142000

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