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Article

Adverse Impacts of Toxic Metal Pollutants on Sex Steroid Hormones of Siganus rivulatus (Teleostei: Siganidae) from the Red Sea

by
Zaki M. Al-Hasawi
Biological Sciences Department, Faculty of Science, King Abdulaziz University, P.O. Box 80203, Jeddah 21589, Saudi Arabia
Fishes 2022, 7(6), 367; https://doi.org/10.3390/fishes7060367
Submission received: 26 October 2022 / Revised: 29 November 2022 / Accepted: 29 November 2022 / Published: 30 November 2022
(This article belongs to the Special Issue Aquatic Pollutants: Risks, Consequences, Possible Solutions and Novel Testing Approaches)
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Abstract

:
Toxic metal pollutants in aquatic environments negatively affect the natural characteristics of water and living organisms. Herein, 254 and 232 specimens (8–14/month) of the fish Siganus rivulatus (Teleostei: Siganidae) were caught alive during four successive seasons in the Red Sea, Egypt, from a chronically polluted bay and from an unpolluted bay, respectively. In each bay, the monthly water temperature was recorded, and the seasonal concentrations of Cd and Pb were determined in the water and in the intestine, liver, and gonads of both fish sexes. In the polluted bay, Cd and Pb were found in significantly high concentrations in the water and in the fish’s intestine, liver, and gonads, and the concentrations only significantly increased in the fish gonads during the spring (spawning season). In each bay, seasonal levels of sex steroid hormones (testosterone T, 17β-estradiol E2, and progesterone P4) in both fish sexes were determined, and they only peaked in both sexes during the spring. In male fish, the serum levels of these hormones throughout the year were in the order T > E2 > P4, while in the females, they were in the order E2 > T > P4. Compared to those in the fish from the unpolluted bay, the levels of these hormones in the fish from the polluted bay were greatly altered. Our results strongly suggest that the serum levels of sex steroid hormones are sensitive biomarkers for detecting heavy metal pollutants in aquatic environments and their effect on fish reproduction.

1. Introduction

Some heavy metals (e.g., Cu, Fe, Ni, and Zn) play extremely vital roles in the metabolic activities of organisms and are therefore termed as “biologically essential”. Other metals (e.g., Hg, Cd, Pb, and As) are not necessary for biological systems and are therefore termed as “non-biologically essential” and are extremely toxic, even in minute traces [1]. Heavy metal pollutants in aquatic environments adversely affect the natural characteristics of water, sediments, and living organisms. In these environments, heavy metals have high affinity for adsorption on particulate organic matter, or tend to be bound to suspended particles, and only minute portions of them are found as free ions in water (hydrated). These portions are bioavailable or mobile portions, i.e., they can be transferred from water to living organisms [2]. Generally, heavy metal contamination in aquatic environments negatively affects fish health and leads to metal accumulation in several organs of the fish, particularly the gills, intestine, liver, muscle, kidneys, and gonads [3]. Accumulation of such metals, especially the toxic ones, in the tissues of these organs leads to tissue damage, biochemical abnormalities, functional disorders, and various severe diseases [3,4,5,6].
Reproduction in fish is complex and controlled by the brain (hypothalamus)–pituitary–gonad axis and some external environmental factors [7,8]. The most important environmental factor is the water temperature, which trigger the brain and consequently this axis into action. The hypothalamus produces the gonadotropin-releasing hormone, which stimulates the pituitary gland to release gonadotropin hormones, which act on the ovaries and testes to trigger the stages of gametogenesis and the production of sex steroid hormones [8,9,10]. In teleost fish, these hormones are essential in the regulation of reproductive processes, such as spermatogenesis and spermiation in males and oocyte growth, maturation, and ovulation in females [10,11].
Heavy metal pollution can adversely affect fish reproduction by altering or impairing any pathway in the reproductive system [12]. Blood biochemical and hormonal parameters are considered as convenient biomarkers for detecting the effect of heavy metals on fish reproduction [13,14]. In modern studies, these parameters are extensively used, as a qualified technique, to assess the effect of pollutants on fish [15], since they are sensitive to water pollution, and their normal levels significantly altered in fish inhabiting heavy metal-polluted environments, leading to serious health problems [16,17].
Siganus rivulatus (Teleostei: Siganidae) is an economically important fish in the Red Sea. Several local studies on the reproductive biology of this fish [18,19,20] concluded that its individuals (both sexes) become sexually mature at lengths up to 15 cm (total length), and they reproduce once a year in a spawning season extending from March to May [18,19,20]. This fish was found to be resident in a chronically polluted bay and in a clear unpolluted bay in the Red Sea, Egypt. Pollution in the first bay is mostly due to extensive tourism and the untreated sewage of motorized diving boats (~600 boats) that use the bay as an anchoring area [21,22,23]. The unpolluted bay is uninhabited and away from any anthropogenic activities. In this study, individuals of S. rivulatus were caught from wild populations in both bays to describe the seasonal variations in its serum levels of sex steroid hormones and to elucidate the impact of some toxic heavy metals such as Cd and Pb on these levels.

2. Materials and Methods

2.1. Ethics

The present study was carried out in accordance with the guidelines of the Declaration of Helsinki and permitted by the current Egyptian regulations of Institutional Animal Care and Use Committee (local IACUC–Cairo University, Cairo, Egypt: approval code, CU/F/12411: 5/6/2021) and by the Egyptian universities’ guidelines for the care of experimental animals.

2.2. Sample Collection and Preparation

During four successive seasons (from September 2020 to August 2021), 254 specimens (8–14/month) of the fish Siganus rivulatus (Teleostei: Siganidae), almost equal in size (19.8 ± 1.9 cm in total length), were caught alive by a casting net from a chronically and severely polluted bay known as “Sharm El-Maya Bay” (27°51.234′ N, 34°17.605′ E) in the Red Sea, at Sharm El-Sheikh, South Sinai, Egypt (Figure 1). Contamination of this bay is due to extensive and active tourism, the huge number of motorized diving boats (~600 boats) that use the bay as an anchoring area and evacuate their untreated sewage directly into its water, the accumulation of a thick layer of solid wastes on it bottom, and other anthropogenic activities [21,22,23]. Similarly, and during the same period, 232 specimens of this fish species (8–13/month), almost equal in size (20.3 ± 1.40 cm in total length), were caught alive from another uninhabited small bay (45 km west of Sharm El-Sheikh). This bay is clear, natural, and away from any anthropogenic activities.
During the study period, the water temperature (°C) in each bay was recorded at a depth of 10 m, on the middle day of every month, and at mid-day, by the temperature sensor of a Hydrolab (DS5X Water Quality Multiprobes: Hach Environmental; Loveland, CO, USA).
To determine metal contaminants in the bay water, 15 water samples, each of 100 mL, were taken seasonally from different locations in each bay. Each sample was filtered and quickly preserved with 2 mL of conc. HNO3 until metal analysis as recommended by Zimmermann et al. [24].
To reduce fish stress, each fish was quickly anesthetized after trapping by using benzocaine (ethyl 4-aminobenzoate 80 mg/L). A blood sample of 6 mL was drawn from its caudal vein via a sterile disposable syringe. Then, the sample was placed in a 6 mL blood collection tube (BD Vacutainer®: Becton, Dickinson and Company, San Francisco, CA, USA), centrifuged at 3000 rpm for 10 min, and the extracted serum was maintained frozen at −25 °C in a clean polypropylene tube until hormone analyses.
After dissection, the sex of each fish and the maturity stage of their gonads were recorded as recommended by Amin [25,26]. However, three samples, each of 3 g, were taken separately from the intestine, liver, and gonads and maintained frozen at −20 °C until metal analysis.

2.3. Sample Analyses

From each extracted blood serum sample, three replicates were used to determine the serum levels of sex steroid hormones by enzyme-linked immuno sorbent assays (ELISA). In this technique three kits from MyBioSource, Inc. (San Diego, CA, USA) were used: the Fish Testosterone (T) ELISA Kit (MBS933475), Fish Estradiol (E2) ELISA Kit (MBS283228), and Fish Progesterone (PROG) ELISA Kit (MBS706075); the manufacturers protocols were typically followed.
Each seawater sample was filtered through a 0.4-μm membrane filter. Then, HNO3 65% EMPLURA® (Merck KGaA, Darmstadt, Germany) was used to acidify the sample to a pH lower than 2 as recommended by Zimmermann et al. [24]. This sample was analyzed directly for detection of Cd and Pb in a Shimadzu Inductively Coupled Plasma Mass Spectrometer (ICPMS-2030, Shimadzu Scientific Instruments Inc. Kyoto, Japan). The metal concentration in the seawater is expressed as mg·L−1.
From the frozen intestine, liver, and gonad (testes or ovaries) samples of each fish, three replicates were taken for metal analysis as suggested by Zimmermann et al. [24] and Nachev [27]. After thawing, 300 mg (wet weight) of homogenized fish tissue was placed into a 150 mL perfluoroalkoxy (PFA) vessel. Then, 2 mL of HNO3 65% EMPLURA® and 2.5 mL of H2O2 35% EMPLURA® were added to the vessel, and for sample digestion, the vessel was heated for 90 min at about 175 °C in a laboratory microwave system (BP110: Microwave Research and Applications, Inc., Carol Stream, IL, USA). Molecular grade H2O was used to dilute the obtained solution to 5 mL, and then it was analyzed for metal contamination in the previously mentioned ICPMS. The metal concentrations in all of the tissue samples were calculated as “mg kg−1 wet weight”. To check the precision of the ICP-MS analyses, two standard certified reference materials were used: SRM–NIST 1640-Trace Elements in Natural Water (National Institute of Standards and Technology, Gaithersburg, MD, USA) and Dogfish liver-DOLT–5 (National Research Council, Ottawa, ON, Canada).

2.4. Data Analysis

Duncan’s multiple range test [28] was used to check the differences in monthly water temperature, in metal concentrations found in the selected fish tissues, and in serum levels of sex steroid hormones; possibilities lower than 0.05 were regarded as statistically significant (p < 0.05). Spearman’s rank correlation coefficient (rs) was calculated to determine possible correlations between metal concentrations in the selected fish tissues, and between these concentrations and the serum levels of sex steroid hormones.

3. Results

3.1. Water Temperature in the Two Bays

Monthly water temperatures (°C) were mostly similar in the two bays (Table 1), but the water temperatures of each season significantly differed from those of the other seasons (p < 0.05).

3.2. Heavy Metal Pollution in the Two Bays

Cd and Pb concentrations recovered from the standard reference materials and the accuracy and detection limits recorded by ICP-MS analyses are shown in Table 2.
Mean seasonal concentrations of Cd and Pb in the water of each bay and in the intestine, liver, and gonads of both sexes of S. rivulatus inhabiting each bay are shown in Table 3. Cadmium was undetectable in the water of the uninhabited bay, while Pb was found in very low concentrations. In contrast, these toxic metals were found in high concentrations in the water of Sharm El-Maya Bay. Mean seasonal concentrations of these metals in the water of each bay were mostly similar in all seasons, without any significant variation.
In the uninhabited bay, Cd was undetectable in the intestine, liver, and gonads of both sexes of S. rivulatus, while Pb was found in the intestine and liver in very low concentrations, but it was undetectable in their gonads. Accordingly, this bay was considered as clean and as an “unpolluted” bay”. In contrast, in the Sharm El-Maya Bay, the mean seasonal concentrations of Cd and Pb in the intestine, liver, and gonads of both sexes of S. rivulatus were significantly high (p < 0.05), the Pb concentrations were consistently higher than those of Cd (p < 0.05), and both Cd and Pb concentrations were higher in males than in females (p < 0.05). Accordingly, Sharm El-Maya Bay was considered as a “polluted bay”, as this is how it is known. Mean seasonal concentrations of Cd and Pb in the intestine, liver, and gonads of each sex of S. rivulatus from this bay were mostly similar during all of the seasons, except during the spring (spawning season), when the mean concentrations of these metals abruptly and significantly increased in the male testes (p < 0.05) or in the female ovaries (p < 0.05), and meanwhile, the concentrations significantly decreased in the intestine and liver of both sexes (p < 0.05). However, in both sexes, there were moderate positive correlations between mean Cd and Pb concentrations in both the liver and gonads and their concentrations in the intestine during the spring (Table 4), and there were strong negative correlations between the mean concentrations of these metals in the liver and their concentrations in the testes or ovaries (Table 4). This means that as the metal concentrations in the intestine decreased, their concentrations in the liver and gonads decreased, and as metal concentrations in the gonads increased, their concentrations in the liver significantly decreased during the spawning season.

3.3. Serum Levels of Sex Steroid Hormones in Both Sexes of S. rivulatus in the Two Bays

Male fish collected from both bays during the autumn and winter months contained unripe testes (small in size) (Figure 2A), while those collected during the spring months contained ripe testes (large, swollen, fully packed with spermatozoa) (Figure 2B), and those collected during the summer months contained spent testes (shriveled, greatly reduced in size) (Figure 2C). Similarly, female fish collected during the autumn and winter months contained unripe ovaries (small in size) (Figure 2D), while those collected during the spring months contained ripe ovaries (large, swollen, fully packed with mature or yolked-eggs) (Figure 2E), and those collected during the summer months contained spent ovaries (shriveled, greatly reduced in size) (Figure 2F).
The monthly levels of serum sex steroid hormones in male fish from both bays were measured (Table S1). In male fish living in the unpolluted bay, the monthly serum levels of T were significantly higher than those of E2 and P4 (p < 0.05), while E2 levels were slightly higher than those of P4 throughout the year (Figure 3A). However, all of the levels of these hormones were low in the autumn and winter, but significantly increased in the spring (p < 0.05), when the T levels peaked in May and those of E2 and P4 peaked in April, and then all of the levels gradually decreased to reach their lowest values in early winter (December). Monthly or seasonal levels of serum sex steroid hormones in male fish living in the unpolluted bay were regarded herein as the means of baseline levels because they were measured in uncontaminated fish living in a clear, unpolluted environment. In male fish living in the polluted bay, monthly serum levels of T were significantly lower than those living in the unpolluted bay (p < 0.05) (Figure 3A), while those of E2 were slightly lower (Figure 3B), but those of P4 were irregularly changed or disturbed (hormonal imbalance) (Figure 3C).
The monthly levels of serum sex steroid hormones in female fish from both bays were measured (Table S2). In female fish living in the unpolluted bay, the serum levels of E2 were significantly higher than those of T and P4 (p < 0.05), while P4 levels were slightly higher than those of T throughout the year. However, all of the levels of these hormones were low in the autumn and winter, but significantly increased in the spring (p < 0.05), when all of these levels peaked in April and then all of the gradually decreased to reach their lowest values in early winter (December). Monthly or seasonal levels of serum sex steroid hormones in female fish living in the unpolluted bay were regarded herein as the means of baseline levels because they were measured in uncontaminated fish living in a clear, unpolluted environment. In female fish living in the polluted bay, monthly levels of serum T were slightly lower than those in females living in the unpolluted bay (Figure 3D), while those of E2 were significantly much lower (p < 0.05) (Figure 3E), and those of P4 were irregularly changed or disturbed (hormonal imbalance) (Figure 3F).
In both sexes of S. rivulatus living in the polluted bay, there were moderate negative correlations between the mean Cd and Pb concentrations in the intestine and liver and the mean serum levels of sex steroid hormones (Table 4), and there were strong negative correlations between the mean concentrations of these metals in the gonads and serum levels of these hormones (Table 4). This means that as Cd and Pb concentrations in the fish’s intestine and liver increased, serum levels of sex steroid hormones decreased, and as the concentrations of these metals in the fish’s testes or ovaries increased, serum levels of the sex steroid hormones significantly decreased.

4. Discussion

Cd and Pb concentrations recovered from the certified reference materials (96.5–98.5%), and the detection limits of these metals (0.003–0.005 mg/L or/kg) recorded by ICP-MS analyses were significantly accurate and revealed the high reliability of these analyses.
The toxic metal Cd was undetectable in the water of the uninhabited bay, while Pb was found in very low concentrations. In contrast, the concentrations of these metals in the water of the Sharm El-Maya Bay were significantly high. Based on the World Health Organization (WHO) guidelines [29], the maximum permissible concentrations of these metals in seawater are 0.003 and 0.05 mg L−1, respectively. Accordingly, the metal concentrations in the water of the uninhabited bay were less than the permissible ones, while those in the water of the Sharm El-Maya Bay were much higher.
In the uninhabited bay, Cd was undetectable in the intestine, liver, and gonads (testes/ovaries) of S. rivulatus. In addition, Pb was undetectable in the gonads, but was found in very low concentrations in the intestine and liver. Controversially, in the Sharm El-Maya Bay, these metals were found in high concentrations in the corresponding organs of S. rivulatus. According to the WHO [29], the permissible concentrations of Cd and Pb in fish tissues are 0.05 and 0.2 mg/kg wet wt, respectively. So, the metal concentrations in the selected tissues of S. rivulatus from the uninhabited bay were less than the permissible ones, while those of S. rivulatus from the Sharm El-Maya Bay were much higher. These results strongly suggest that the uninhabited bay is presently clean and “unpolluted”; whereas the Sharm El-Maya Bay is chronically and severely “polluted”, as is known [21,22,23].
In this study, Cd and Pb concentrations in both sexes of S. rivulatus decreased in the order: liver > intestine > gonads. High metabolically active organs tend to accumulate higher levels of heavy metals than those accumulated by low metabolically active ones [30,31,32]. So, the liver tends to accumulate higher levels of Cd and Pb than the intestine, while the gonads tend to accumulate relatively low metal levels. Elevated levels of metals in the liver may be due to its critical role in the production of metallothioneins (metal-binding proteins) [33,34,35], which play an essential role in heavy metal detoxification in the liver [36]. Mean seasonal concentrations of Cd and Pb in the intestine, liver, and gonads of both sex of S. rivulatus living in the polluted bay were mostly similar in all seasons, except during the spring (spawning season), when a significant increase in the levels of these metals in the fish gonads was observed, and this may be due to the increasing metabolic activity in the gonads during this season. However, the negative correlations between Cd and Pb concentrations in the fish gonads and their concentrations in the liver during the spring may be due to the transfer of metallothioneins from the liver to the gonads. Generally, accumulation of toxic metals in fish tissues results in tissue damage, biochemical abnormalities, functional disorders, and various severe diseases [3,4,5,6].
Previous studies have concluded that seawater temperature plays a critical role in controlling the timing and duration of the spawning season of most siganid fish [25,26,37,38,39,40]. George [41] declared that S. rivulatus spawning is triggered when seawater the temperature reaches 27 °C. In the current study, the gonadal morphology of this fish strongly confirms the suggestions of Amin, et al. [24] and Abdelhak, et al. [20] that S. rivulatus spawned during the spring months and under a temperature range within 25–28 °C, as declared by George [41]. During the warmer seasons, summer (29.2–31.4 °C) or autumn (28.2–30.6 °C), no ripe gonads were observed in the examined fish samples, and all of the gonads were in a spent condition. A high seawater temperature seemed to be a limiting factor in the gonadal development of the siganid fish [39]. Popper and Gundermann [42] did not observe any ripe gonads in siganid populations from the Mediterranean Sea during August (29 °C). In addition, Amin [25] observed that all individuals of S. rivulatus were in a spent condition during July when the water temperature in the Red Sea reached 30 °C. In contrast, ripe gonads of S. rivulatus and S. luridus were observed in the Gulf of Aqaba until August and September, respectively, when the mean water temperature was close to 27 °C [39]. Generally, our results strongly suggest that S. rivulatus is a spring spawner species and requires a particular range of water temperatures (25–28 °C) for successful spawning.
Sex steroid hormones, mainly testosterone (T), 17β-estradiol (E2), and progesterone (P4), are responsible for the normal reproductive functions in male and female fish. In male teleosts, T is the major androgenic sex hormone, synthesized by Leydig cells in the testes to regulate spermatogenesis and sexual differentiation and is responsible for the development of secondary sexual characteristics and reproductive behavior [43,44,45]. In female teleosts, T is produced by theca folliculi of the ovarian follicles to modulate the circulation of sexual hormones in the brain [46] and may contribute to oocyte growth and development by triggering germinal vesicle breakdown during final oocyte maturation [47]. In female teleosts, E2 is the major estrogenic sex hormone, synthesized by the cells of ovarian follicles to control physiological events during the reproductive cycles, the growth of oocytes, the vitellogenesis, and the development and maintenance of female sexual characteristics [48,49,50,51]. In male teleosts, E2 is synthesized in the testes to initiate spermatogonial self-renewal [52,53,54,55,56]. P4 is the major progestogenic sex hormone produced in the ovaries and testes. It is a vital steroidogenic mediator for oocyte growth and maturation in female fish and also for spermatogenesis and sperm maturation in male fish [9,57,58]. Abnormal levels of sex steroid hormones adversely affect fish health, for instance by disturbing the normal reproductive events, impairing gametogenesis and fish reproduction, suppressing the reproductive output, disrupting the endocrine and immune systems, or by causing serious reproductive disorders [58,59,60,61,62,63].
Serum levels of sex steroid hormones in both sexes of S. rivulatus living in the unpolluted bay were regarded herein as the means of baseline levels, because they were measured in fish living in a clear, unpolluted environment. In male fish living in this bay, the serum levels of these hormones were in the order T > E2 > P4 throughout the year, and they only peaked during the spring (spawning season), but in males living in the polluted bay, the T levels were significantly much lower and the E2 levels were slightly lower than those in males inhabiting the unpolluted bay, while those of P4 were irregularly changed or disturbed (hormonal imbalance). In female fish living in the unpolluted bay, the serum levels of these hormones were in the order E2 > T > P4 throughout the year and only peaked during the spring (spawning season). In females living in the polluted bay, the E2 levels were significantly much lower and the T levels were slightly lower than those in females inhabiting the unpolluted bay, while those of P4 were irregularly changed or disturbed (hormonal imbalance). So, the present results strongly suggest that serum levels of sex steroid hormones in both sexes of S. rivulatus living in the polluted bay were negatively affected by heavy metal pollution in this bay, particularly during the spring, when the mean Cd and Pb concentrations in the fish gonads were distinctly high and led to a significant decrease in the levels of serum sex steroid hormones (E2, T and P4), levels considerably lower than those in fish living in the unpolluted bay. However, there were strong negative correlations between mean Cd and Pb concentrations in the gonads and the serum levels of these hormones. This means that as metal concentrations in the fish testes or ovaries increased, serum levels of sex steroid hormones significantly decreased. Such a decrease in the levels of these hormones in fish, due to heavy metal pollution, has been reported in several studies [12,14,64,65]. Thus, accumulation of heavy metals in the gonads of S. rivulatus retards their production of sex steroid hormones. As toxic metals, Cd and Pb can affect the endocrine system in teleost fishes, and they are known as “metalloestrogens“or endocrine-disrupting chemicals [66,67]. These chemicals may suppress the production and transfer of natural hormones and steroids [68].
Generally, the effect of heavy metal pollution on fish health can be checked through several biomarkers. Changes in the normal serum levels of sex steroid hormones are considered as convenient or sensitive biomarkers for detecting heavy metal pollution in aquatic environments and its adverse effects on fish reproduction [13,14].

5. Conclusions

Some heavy metals (e.g., Cu, Fe, Ni, and Zn) play extremely important vital roles in the metabolic activities of organisms and are termed as “biologically essential”. Other metals (e.g., Hg, Cd, Pb, and As) are not necessary for biological systems and are termed as “non-biologically essential”, and they are extremely toxic, even in minute traces. Contamination with heavy metals in aquatic environments, particularly with toxic metals, adversely affects the natural characteristics of water and living organisms. This contamination leads to metal accumulation in several organs of the fish. Excessive accumulation of such metals, especially the toxic ones, in the tissue of these organs leads to tissue damage, biochemical abnormalities, functional disorders, and various severe diseases. Our results revealed that accumulation of toxic metals (Cd and Pb) in S. rivulatus gonads (testes and ovaries) during the spawning season alters the normal levels of sex steroid hormones (testosterone T, 17β-estradiol E2, progesterone P4). These hormones are responsible for the normal reproductive functions in males and female fish. Abnormal levels of these hormones adversely affect fish health, for instance by disturbing the normal reproductive events, impairing gametogenesis and fish reproduction, suppressing the reproductive output, disrupting the endocrine and immune systems, or by causing serious reproductive disorders. Generally, our results completely agree with most modern studies that blood hormonal parameters, such as the levels of sex steroid hormones, are convenient and sensitive biomarkers for detecting heavy metal pollution in aquatic environments and its adverse effects on fish reproduction.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/fishes7060367/s1, Table S1: Monthly or seasonal levels of serum sex steroid hormones in male fishes from both bays. Table S2: Monthly or seasonal levels of serum sex steroid hormones in female fishes from both bays.

Funding

This research received no external funding.

Institutional Review Board Statement

The present study was carried out in accordance with the guidelines of the Declaration of Helsinki and was permitted by the current Egyptian regulations of Institutional Animal Care and Use Committee (local IACUC–Cairo University, Cairo, Egypt: approval code, CU/F/12411: 5/6/2021) and by the Egyptian universities’ guidelines for the care of experimental animals.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The author is very grateful to the Rabigh-Faculty of Science and Arts, King Abdulaziz University, Saudi Arabia, for continued encouragement and support. The author would like to extend their appreciation to the staff of the Red Sea Diving Center, Sharm El-Sheikh, South Sinai, Egypt, for their help during the collection of the material.

Conflicts of Interest

The author declares that they have no conflict of interest.

References

  1. Wakawa, R.J.; Uzairu, A.; Kagbu, J.A.; Balarabe, M.L. Impact assessment of effluent discharge on physicochemical parameters and some heavy metal concentrations in surface water of river Challawa Kano. Afr. J. Pure Appl. Chem. 2008, 2, 100–106. [Google Scholar]
  2. Merian, E.; Anke, M.; Ihnat, M.; Stoeppler, M. Elements and Their Compounds in the Environment: Occurrence, Analysis and Biological Relevance, 2nd ed.; Wiley: Weinheim, Germany, 2004; pp. 1–1733. [Google Scholar]
  3. Fazio, F.; Piccione, G.; Tribulato, K.; Ferrantelli, V.; Giangrosso, G.; Arfuso, F.; Faggio, C. Bioaccumulation of heavy metals in blood and tissue of striped mullet in two Italian lakes. J. Aquat. Anim. Health 2014, 26, 278–284. [Google Scholar] [CrossRef] [PubMed]
  4. Robert, R.C. Metal Toxicity–An Introduction. In Metal Chelation in Medicine, 1st ed.; Robert, R.C., Roberta, J.W., Robert, C., Eds.; Royal Society of Chemistry: London, UK, 2016; pp. 1–23. [Google Scholar]
  5. Javed, M.; Usmani, N. An overview of the adverse effects of heavy metal contamination on fish health. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci. 2019, 89, 389–403. [Google Scholar] [CrossRef]
  6. Tahity, T.; Islam, M.R.U.; Bhuiyan, N.Z.; Choudhury, T.R.; Yu, J.; Noman, M.A.; Hosen, M.M.; Quraishi, S.B.; Paray, B.A.; Arai, T.; et al. Heavy metals accumulation in tissues of wild and farmed barramundi from the northern Bay of Bengal coast, and its estimated human health risks. Toxics 2022, 10, 410. [Google Scholar] [CrossRef]
  7. Rottmann, R.W.; Shireman, J.V.; Chapman, F.A. Hormonal control of reproduction in fish for induced spawning. SRAC Publ. 1991, 424, 1–4. [Google Scholar]
  8. Rainis, S.; Ballestrazzi, R. The control of reproduction in finfish species through GnRH treatments, Ital. J. Anim. Sci. 2005, 4, 345–353. [Google Scholar]
  9. Nagahama, Y. Endocrine regulation of gametogenesis in fish. Int. J. Dev. Biol. 1994, 38, 217–229. [Google Scholar]
  10. Sang, H.M.; Ky, P.X.; Lam, H.S.; Thu, P.M. Steroid hormones in reproduction and roles of gnrh-a in gonadal maturation of marine fish: A Review. Annu. Res. Rev. Biol. 2019, 34, 1–12. [Google Scholar] [CrossRef] [Green Version]
  11. Nagahama, Y.; Yoshikuni, M.; Yamashita, M.; Tokumoto, T.; Katsu, Y. Regulation of oocyte growth and maturation in fish. In Current Topics in Developmental Biology; Pedersen, R.A., Schatten, G.P., Eds.; Academic Press: New York, NY, USA, 1995; pp. 103–145. [Google Scholar]
  12. Ebrahimi, M.; Taherianfard, M. The effects of heavy metals exposure on reproductive systems of cyprinid fish from Kor River. Iran. J. Fish. Sci. 2011, 10, 13–24. [Google Scholar]
  13. Hedayati, A.; Zare, P.; Abarghouei, S. Effect of environmental mercury on some hormonal parameters of the main mariculture fish of Persian Gulf. Glob. Vet. 2012, 8, 43–50. [Google Scholar]
  14. Nath, N.B. Effect of heavy metal (loid)s on the level of gonadal hormone during the sexual maturity and breeding period of catfish, Clarias batrachus (L.). JETIR 2019, 6, 124–130. [Google Scholar]
  15. Fazio, F. Fish hematology analysis as an important tool of aquaculture: A review. Aquaculture 2019, 500, 237–242. [Google Scholar] [CrossRef]
  16. Murray, R.K.D.K.; Rranne, P.A.M.; Rodwell, V.W. Harper’s Biochemistry Publisher, 22nd ed.; McGraw-Hill Companies, Inc.: Norwalk, CT, USA; Los Altos, CA, USA, 1990; pp. 1–720. [Google Scholar]
  17. Abalaka, S.E. Evaluation of the haematology and biochemistry of Clarias gariepinus as biomakers of environmental pollution in Tiga dam Nigeria. Braz. Arch. Biol. Technol. 2013, 56, 371–376. [Google Scholar] [CrossRef] [Green Version]
  18. Hashem, M.T. Biological studies on Siganus rivulatus (Forsk.) in the Red Sea. J. Mar. Sci. 1983, 3, 118–128. [Google Scholar]
  19. El-Drawany, M. On the biology of Siganus rivulatus inhabits Bitter Lakes in Egypt. J. Aquac. Res. Dev. 2015, 6, 342. [Google Scholar]
  20. Abdelhak, E.M.; Madkour, F.F.; El Ganainy, A.A.; Abu El-Regal, M.A.; Ahmed, M.I. Reproductive biology of Siganus rivulatus (Forsskal, 1775) in the Red Sea, Suez Canal and the Mediterranean Sea, Egypt. EJABF 2020, 24, 117–134. [Google Scholar] [CrossRef]
  21. Egyptian Environmental Affairs Agency (EEAA). Marine Pollution in the Gulf of Aqaba and Gulf of Suez and Its Effects on South Sinai. A Comprehensive Review. 2003. Available online: http://st-katherine.net/en/downloads/Marine%20Pollution.pdf (accessed on 26 May 2022).
  22. Aly Salem, D.M.S.; Khaled, A.; El Nemr, A.; El-Sikaily, A. Comprehensive risk assessment of heavy metals in surface sediments along the Egyptian Red Sea coast. Egypt. J. Aquat. Res. 2014, 40, 349–362. [Google Scholar] [CrossRef] [Green Version]
  23. Nour, H.E.; Helal, S.A.; Abdel Wahab, M. Contamination and health risk assessment of heavy metals in beach sediments of Red Sea and Gulf of Aqaba, Egypt. Mar. Pollut. Bull. 2022, 177, 113517. [Google Scholar] [CrossRef]
  24. Zimmermann, S.; Menzel, C.; Berner, Z.; Eckhardt, J.D.; Stüben, D.; Alt, F.; Messerschmidt, J.; Taraschewski, H.; Sures, B. Trace analysis of platinum in biological samples: A comparison between high resolution inductively coupled plasma mass spectrometry (HR-ICP-MS) following microwave digestion and adsorptive cathodic stripping voltammetry (ACSV) after high pressure ashing. Anal. Chim. Acta 2001, 439 (Suppl. 2), 203–209. [Google Scholar] [CrossRef]
  25. Amin, E.M. Seasonal developmental changes in the ovaries of Siganus rivulatus from The Red Sea. Bull. Inst. Ocean. Fish. 1985, 11, 131–147. [Google Scholar]
  26. Amin, E.M. Reproductive cycle of male Siganus rivulatus Forsk. With indication to gonadosomatic and hepatosomatic indices. Bull. Inst. Ocean. Fish. (ARE) 1985, 11, 149–164. [Google Scholar]
  27. Nachev, M. Bioindication Capacity of Fish Parasites for the Assessment of Water Quality in the Danube River. Ph.D. Thesis, Universität Duisburg-Essen, Sofia, Bulgaria, 2010. [Google Scholar]
  28. Duncan, D.B. Multiple range and Multiple F-test. Biometrics 1955, 11, 1–42. [Google Scholar] [CrossRef]
  29. World Health Organization WHO. WHO Guidelines for Drinking Water Quality, 4th ed.; WHO Publications: Geneva, Switzerland, 2011; pp. 307–340. ISBN 978-92-4-154815-1.
  30. Dural, M.; LugalGöksu, M.Z.; Özak, A.A.; Derici, B. Bioaccumulation of some heavy metals in different tissues of Dicentrarchus Labrax L., 1758, Sparus Aurata L., 1758 and Mugil Cephalus L., 1758 from the ÇamlIk lagoon of the eastern cost of Mediterranean (Turkey). Environ. Monit. Assess. 2006, 118, 65–74. [Google Scholar] [CrossRef]
  31. Kenšova, R.; Čelehovska, O.; Doubravova, J.; Svobodova, Z. Concentration of metals in tissues of fish from the Vestonice Reservoir. Acta Vet. Brno 2010, 79, 335–345. [Google Scholar] [CrossRef] [Green Version]
  32. Kelle, H.I.; Ngbede, E.O.; Oguezi, V.U.; Ibekwe, F.C. Determination of heavy metals in fish (Clarias gariepinus) organs from Asaba Major Markets, Delta State, Nigeria. Am. Chem. Sci. J. 2015, 5, 135–147. [Google Scholar]
  33. Carpene, E.; Vašák, M. Hepatic metallothioneins from goldfish (Carassius auratus). Comp. Biochem. Physiol. 1989, 92B, 463–468. [Google Scholar] [CrossRef]
  34. Al-Yousuf, M.H.; El-Shahawi, M.S.; Al-Ghais, S.M. Trace elements in liver, skin and muscle of Lethrinus lentjan fish species in relation to body length and sex. Sci. Total Environ. 2000, 256, 87–94. [Google Scholar] [CrossRef] [PubMed]
  35. Yousafzai, A.M.; Khan, A.R.; Shakoori, A.R. Trace metal accumulation in the liver of an endangered South Asian fresh water fish dwelling in sub-lethal pollution. Pak. J. Zool. 2009, 41, 35–41. [Google Scholar]
  36. Kojima, Y.; Kagi, J.H.R. Metallothionein. Trends Biochem. Sci. 1978, 3, 90–93. [Google Scholar] [CrossRef]
  37. Lam, T.J.; Soh, C.L. Effect of photoperiod on gonadal maturation in the rabbitfish, Siganus canaliculatus Park 1797. Aquaculture 1975, 5, 407–410. [Google Scholar] [CrossRef]
  38. Popper, D.; May, R.C.; Lichatowich, T. An experiment in rearing larval Siganus vermiculatus (Valenciennes) and some observations on its spawning cycle. Aquaculture 1976, 7, 281–290. [Google Scholar] [CrossRef]
  39. Bariche, M.; Harmelin-Vivien, M.; Quignard, J.-P. Reproductive cycles and spawning periods of two Lessepsiansiganid fishes on the Lebanese coast. J. Fish Biol. 2003, 62, 129–142. [Google Scholar] [CrossRef]
  40. Takemura, A.; Rahman, M.S.; Nakamura, S.; Park, Y.J.; Takano, K. Lunar cycles and reproductive activity in reef fishes with particular attention to rabbitfishes. Fish Fish. 2004, 5, 317–328. [Google Scholar] [CrossRef]
  41. George, C.J. Notes on the breeding and movements of the rabbitfishes, Siganus rivulatus (ForsskDl) and S. luridus Rüppell, in the coastal waters of the Lebanon. Ann. Mus. Civ. Stor. 1972, 9, 32–44. [Google Scholar]
  42. Popper, D.; Gundermann, N. Some ecological and behavioural aspects of siganid populations in the Red Sea and Mediterranean coasts of Israel in relation to their suitability for aquaculture. Aquaculture 1975, 6, 127–141. [Google Scholar] [CrossRef]
  43. Borg, B. Androgens in teleost fish. Comp. Biochem. Physiol. 1994, 109C, 219–245. [Google Scholar]
  44. Nagahama, Y.; Kobayashi, T.; Chang, X.T.; Nagahama, Y. Gonadal sex differentiation in teleost fish. J. Exp. Zool. 1998, 281, 362–373. [Google Scholar]
  45. Harbott, L.K.; Burmeister, S.S.; White, R.B.; Vagell, M.; Fernald, R.D. Androgen receptors in a cichlid fish, Astatotilapia burtoni: Structure, localization, and expression levels. J. Comp. Neurol. 2007, 504, 57–73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Liu, C.; Yue, S.; Solarz, J.; Lee, J.; Li, L. Improving the sexual activity and reproduction of female zebrafish with high testosterone levels. Sci. Rep. 2021, 11, 3822. [Google Scholar] [CrossRef]
  47. So, Y.P.; Idler, D.R.; Truscott, B.; Walsh, J.M. Progestogens androgens and their glucuronides in the terminal stages of oocyte maturation in landlocked Atlantic salmon. J. Steroid Biochem. 1985, 23, 583–591. [Google Scholar] [CrossRef]
  48. Campbell, C.M.; Idler, D.R. Hormonal control of vitellogenesis in hypophysectomized winter flounder (Pseudopleuronectes americanus Walbaum). J. Endocrinol. 1976, 28, 143–150. [Google Scholar] [CrossRef] [PubMed]
  49. Smith, C.J.; Haley, S.R. Steroid profiles of the female tilapia, Oreochromis mossambicus, and correlation with oocyte growth and mouthbrooding behavior. J. Endocrinol. 1988, 69, 88–98. [Google Scholar] [CrossRef] [PubMed]
  50. Cornish, D.A. Seasonal steroid hormone profiles in plasma and gonads of the tilapia, Oreochromis mossambicus. Water SA 1998, 24, 257–263. [Google Scholar]
  51. Taghizadeh, V.; Imanpoor, M.R.; Mehdinejad, N. Study the seasonal steroid hormones of common carp in Caspian Sea, Iran. Springerplus 2013, 2, 193. [Google Scholar] [CrossRef] [Green Version]
  52. Miura, T.; Miura, C.; Ohta, T.; Nader, M.R.; Todo, T.; Yamauchi, K. Estradiol-17 β stimulates the renewal of spermatogonial stem cells in males. Biochem. Biophys. Res. Commun. 1999, 264, 230–234. [Google Scholar] [CrossRef]
  53. Miura, T.; Miura, C. Japanese eel: A model for analysis of spermatogenesis. Zool. Sci. 2001, 18, 1055–1063. [Google Scholar] [CrossRef]
  54. Schulz, R.W.; Miura, T. Spermatogenesis and its endocrine regulation. Fish Physiol. Biochem. 2002, 26, 43–56. [Google Scholar] [CrossRef]
  55. Song, M.; Gutzeit, H.O. Effect of 17-alpha-ethynylestradiol on germ cell proliferation in organ and primary culture of medaka (Oryziaslatipes) testis. Dev. Growth Differ. 2003, 45, 327–337. [Google Scholar] [CrossRef] [Green Version]
  56. Schulz, R.W.; de França, L.R.; Lareyre, J.-J.; Le Gac, F.; ChiariniGarcia, H.; Nóbrega, R.H.; Miura, T. Spermatogenesis in fish. Gen. Comp. Endocrinol. 2010, 165, 390–411. [Google Scholar] [CrossRef]
  57. Kime, D.E. A strategy for assessing the effects of xenobiotics on fish reproduction. Sci. Total Environ. 1999, 225, 3–11. [Google Scholar] [CrossRef]
  58. Zeilinger, J.; Steger-hartmann, T.; Maser, E.; Goller, S.; Vonk, R.; Lange, R. Effects of synthetic gestagens on fish reproduction. Environ. Toxicol. Chem. 2009, 28, 2663–2670. [Google Scholar] [CrossRef] [PubMed]
  59. Harris, J.; Bird, D.J. Modulation of the fish immune system by hormones. Vet. Immunol. Immunopathol. 2000, 77, 163–176. [Google Scholar] [CrossRef] [PubMed]
  60. Ellis, T.M.; Moser, M.T.; Le, P.T.; Flanigan, R.C.; Kwon, E.D. Alterations in peripheral B cells and B cell progenitors following androgen ablation in mice. Int. Immunol. 2001, 13, 553–558. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  61. Bugel, S.M.; White, L.A.; Cooper, K.R. Decreased vitellogenin inducibility and 17β-estradiol levels correlated with reduced egg production in killifish (Fundulus heteroclitus) from Newark Bay, NJ. Aquat. Toxicol. 2011, 105, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Zhong, C.; Xiong, K.; Wang, X. Effects of progesterone on the reproductive physiology in zebrafish. bioRxiv 2017. [Google Scholar] [CrossRef] [Green Version]
  63. Maciuszek, M.; Pijanowski, L.; Pekala-Safinska, A.; Agnieszka, P.-S.; LidyVerburg-van Kemenade, B.M.; Magdalena, C. 17β-Estradiol affects the innate immune response in common carp. Fish. Physiol. Biochem. 2020, 46, 1775–1794. [Google Scholar] [CrossRef]
  64. Webb, M.A.H.; Feist, G.W.; Fitzpatrick, M.S.; Foster, E.P.; Schreck, C.B.; Plumlee, M.; Wong, C.; Gundersen, D.T. Mercury Concentrations in Gonad, Liver and Muscle of White Sturgeon Acipenser transmontanus in the Lower Columbia River. Arch. Environ. Contam. Toxicol. 2006, 50, 443–451. [Google Scholar] [CrossRef]
  65. Abdel-Kader, H.H.; Mourad, M.H. Bioaccumulation of heavy metals and physiological/histological changes in gonads of catfish (Clarias gariepinus) inhabiting Lake Maryout, Alexandria, Egypt. Egypt. J. Aquat. Biol. Fish. 2019, 23, 363–377. [Google Scholar] [CrossRef] [Green Version]
  66. Waisberg, M.; Joseph, P.; Hale, B.; Beyersmann, D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 2003, 192, 95–117. [Google Scholar] [CrossRef]
  67. Dyer, C.A. Endocrine-Disrupting chemicals: From basic research to clinical practice. In Endocrine-Disrupting Chemicals, 1st ed.; Gore, A.C., Ed.; Humana Press, Inc.: Totowa, NJ, USA, 2007; Volume 5, pp. 111–133. [Google Scholar]
  68. Arcand-Hoy, L.D.; Benson, W.H. Fish reproduction: An ecologically relevant indicator of endocrine disruption. Environ. Toxicol. Chem. 1988, 17, 49–57. [Google Scholar] [CrossRef]
Fishes 07 00367 g001 550
Figure 1. A map showing the locations of Sharm El-Sheikh, South Sinai, Egypt, and the uninhabited bay (45 km west of Sharm El-Sheikh).
Figure 1. A map showing the locations of Sharm El-Sheikh, South Sinai, Egypt, and the uninhabited bay (45 km west of Sharm El-Sheikh).
Fishes 07 00367 g001
Fishes 07 00367 g002 550
Figure 2. (A–F): Testes and ovaries of S. rivulatus. (A)—immature testes during the autumn and winter, (B)—ripe testes during the spring, (C)—spent testes during the summer, (D)—immature ovaries during the autumn and winter, (E)—ripe ovaries during the spring, and (F)—spent ovaries during the summer.
Figure 2. (A–F): Testes and ovaries of S. rivulatus. (A)—immature testes during the autumn and winter, (B)—ripe testes during the spring, (C)—spent testes during the summer, (D)—immature ovaries during the autumn and winter, (E)—ripe ovaries during the spring, and (F)—spent ovaries during the summer.
Fishes 07 00367 g002
Fishes 07 00367 g003 550
Figure 3. (A–F): Monthly levels of serum sex steroid hormones in both sexes of S. rivulatus living in each bay.
Figure 3. (A–F): Monthly levels of serum sex steroid hormones in both sexes of S. rivulatus living in each bay.
Fishes 07 00367 g003
Table
Table 1. Monthly water temperature (°C) in the uninhabited bay and in the Sharm El-Maya Bay.
Table 1. Monthly water temperature (°C) in the uninhabited bay and in the Sharm El-Maya Bay.
SeasonMonthMean Water Temperature (°C)
Uninhabited Bay
(Unpolluted)		Sharm El-Maya Bay (Polluted)
Autumn September 202030.831.1
October30.730.9
November28.028.3
WinterDecember24.424.9
January 202123.323.6
February25.125.4
SpringMarch 25.725.7
April26.527.1
May28.128.3
SummerJune29.229.4
July30.531.0
August31.431.9
Table
Table 2. Heavy metal concentrations recovered from the standard reference materials and the accuracy and detection limits recorded by ICP-MS analyses.
Table 2. Heavy metal concentrations recovered from the standard reference materials and the accuracy and detection limits recorded by ICP-MS analyses.
Standard Reference MaterialMetalCertified Value Recovered ValueAccuracy (%)Detection Limit
SRM–NIST 1640-Trace Elements in Natural Water (mg/L)(mg/L) (mg/L)
Cd3.961 ± 0.072 3.883 ± 0.01398.030.004
Pb12.005 ± 0.040 11.584 ± 0.015 96.500.005
Dogfish liver DOLT-5 (mg/kg)(mg/kg) (mg/kg)
Cd14.5 ± 0.400 14.282 ± 0.014 98.500.005
Pb0.162 ± 0.032 0.157 ± 0.00397.060.003
Table
Table 3. Mean seasonal concentrations of Cd and Pb in the water of each bay and in the intestine, liver, and gonads of both sexes of S. rivulatus inhabiting each bay.
Table 3. Mean seasonal concentrations of Cd and Pb in the water of each bay and in the intestine, liver, and gonads of both sexes of S. rivulatus inhabiting each bay.
SeasonUninhabited Bay (Unpolluted)Sharm El-Maya Bay (Polluted)
Mean Metal Concentration
For Water (mg·L−1), for Tissue (mg kg –1 wet wt.)		Mean Metal Concentration
For Water (mg·L−1), for Tissue (mg kg –1 wet wt.)
CdPbCdPb
WaterAutumn Undetected0.05 ± 0.010.32 ± 0.063.43 ± 0.17
Winter Undetected0.04 ± 0.010.31 ± 0.043.23 ± 0.26
Spring Undetected0.04 ± 0.010.34 ± 0.083.35 ± 0.16
Summer Undetected0.05 ± 0.010.33 ± 0.093.51 ± 0.24
Male S. rivulatusIntestineAutumnUndetected0.04 ± 0.020.23 ± 0.022.53 ± 0.18
WinterUndetected0.03 ± 0.010.22 ± 0.032.51 ± 0.11
SpringUndetected0.04 ± 0.020.17 ± 0.052.05 ± 0.13
SummerUndetected0.05 ± 0.020.24 ± 0.042.55 ± 0.17
LiverAutumnUndetected0.07 ± 0.020.49 ± 0.056.30 ± 0.28
WinterUndetected0.07 ± 0.020.48 ± 0.036.11 ± 0.41
SpringUndetected0.07 ± 0.010.30 ± 0.044.20 ± 0.19
SummerUndetected0.08 ± 0.030.45 ± 0.076.40 ± 0.32
TestsAutumnUndetectedUndetected0.14 ± 0.031.27 ± 0.18
WinterUndetectedUndetected0.13 ± 0.021.24 ± 0.12
SpringUndetectedUndetected0.28 ± 0.042.28 ± 0.10
SummerUndetectedUndetected0.16 ± 0.051.26 ± 0.16
Female S. rivulatusIntestineAutumnUndetected0.04 ± 0.010.21 ± 0.032.46 ± 0.17
WinterUndetected0.04 ± 0.010.20 ± 0.012.43 ± 0.14
SpringUndetected0.04 ± 0.010.14 ± 0.021.97 ± 0.11
SummerUndetected0.05 ± 0.020.21 ± 0.042.45 ± 0.19
LiverAutumnUndetected0.08 ± 0.010.38 ± 0.075.11 ± 0.14
WinterUndetected0.07 ± 0.020.36 ± 0.055.10 ± 0.23
SpringUndetected0.08 ± 0.010.21 ± 0.033.60 ± 0.34
SummerUndetected0.09 ± 0.020.37 ± 0.085.12 ± 0.19
OvaryAutumnUndetectedUndetected0.12 ± 0.031.15 ± 0.13
WinterUndetectedUndetected0.11 ± 0.021.14 ± 0.11
SpringUndetectedUndetected0.22 ± 0.071.98 ± 0.21
SummerUndetectedUndetected0.13 ± 0.071.13 ± 0.10
Table
Table 4. Spearman’s rank correlation (rs) matrix between mean metals concentrations in the intestine, liver, and gonads of S. rivulatus, and between these concentrations and serum levels of sex steroid hormones.
Table 4. Spearman’s rank correlation (rs) matrix between mean metals concentrations in the intestine, liver, and gonads of S. rivulatus, and between these concentrations and serum levels of sex steroid hormones.
Metal ConcentrationMale S. rivulatus
Cd
Liver		Pb
Liver		Cd
Testes/Ovaries		Pb Testes/OvariesSerum Levels of Sex Steroid Hormones
TE2P4
rsprsprsprsprsprsprsp
Cd intestine0.5740.0050.1890.2920.5980.0050.1590.294−0.5980.004−0.6180.004−0.6410.004
Pb intestine0.3520.4120.5980.0030.4390.1720.6280.004−0.5250.005−0.6120.005−0.5720.005
Cd liver 0.2890.384−0.8110.0010.4260.370−0.6020.003−0.6010.002−0.5630.003
Pb liver 0.2790.219−0.9070.001−0.5490.003−0.6270.003−0.5290.005
Cd testes 0.2690.311−0.9470.001−0.9190.001−0.8370.001
Pb testes −0.8380.003−0.8230.003−0.8930.002
Female S. rivulatus
Cd intestine0.5090.0050.2080.4370.6510.0040.1990.393−0.5500.005−0.5010.005−0.5840.004
Pb intestine0.2970.3170.5390.0040.3790.2590.5130.004−0.5130.005−0.5540.004−0.5910.005
Cd liver 0.4920.251−0.8790.0010.3390.283−0.5690.004−0.5890.005−0.5470.004
Pb liver 0.3200.426−0.9320.001−0.6420.003−0.5680.004−0.6090.004
Cd testes 0.4670.407−0.8670.001−0.9450.001−0.8580.001
Pb testes −0.9010.002−0.8480.002−0.8090.001
Values in bold letters show significant correlations (p < 0.05).
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Al-Hasawi, Z.M. Adverse Impacts of Toxic Metal Pollutants on Sex Steroid Hormones of Siganus rivulatus (Teleostei: Siganidae) from the Red Sea. Fishes 2022, 7, 367. https://doi.org/10.3390/fishes7060367

AMA Style

Al-Hasawi ZM. Adverse Impacts of Toxic Metal Pollutants on Sex Steroid Hormones of Siganus rivulatus (Teleostei: Siganidae) from the Red Sea. Fishes. 2022; 7(6):367. https://doi.org/10.3390/fishes7060367

Chicago/Turabian Style

Al-Hasawi, Zaki M. 2022. "Adverse Impacts of Toxic Metal Pollutants on Sex Steroid Hormones of Siganus rivulatus (Teleostei: Siganidae) from the Red Sea" Fishes 7, no. 6: 367. https://doi.org/10.3390/fishes7060367

APA Style

Al-Hasawi, Z. M. (2022). Adverse Impacts of Toxic Metal Pollutants on Sex Steroid Hormones of Siganus rivulatus (Teleostei: Siganidae) from the Red Sea. Fishes, 7(6), 367. https://doi.org/10.3390/fishes7060367

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