Physiological Ecology of Aquatic Animals under Extreme Environments

A special issue of Biology (ISSN 2079-7737). This special issue belongs to the section "Ecology".

Deadline for manuscript submissions: closed (31 March 2023) | Viewed by 18633

Special Issue Editors


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Guest Editor
College of Life Sciences, Beijing Normal University, Beijing 100875, China
Interests: stress; antioxidant defense system; fresh water turtle; bioenergetics; adaptive evolution; phenotypic plasticity; life history strategy; rotifer; aquaculture

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Guest Editor
College of Life Sciences, Shanxi University, Taiyuan 030006, China
Interests: ecological immunology; evolutionary immunology; stress and immunity; host–microbe cross-talk; thermal ecology

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Guest Editor
Laboratory of Evolutionary Physiology and Behavior, College of Life Sciences, Chongqing Normal University, Chongqing 401331, China
Interests: fish physiological ecology; behavioral ecology; conservation ecology; thermal ecology; phenotypic plasticity and individual variation

Special Issue Information

Dear Colleagues,

Animal physiological ecology studies how the interaction of animals with their environments shapes physiological characteristics that are relevant to ecology, as well as how the animal’s physiological functions adapt to their surroundings in light of evolution. The adaptive mechanism of animals living in extreme environments especially attracts attention from scientists. On one hand, exploring the physiological function maintenance mechanism of animals naturally distributed in extreme environments (e.g., polar, plateau, and intertidal zones) can help us to understand the adaptive limits of life. On the other hand, exploring the physiological and ecological responses of animals to stressful environmental changes caused by anthropogenic activities (e.g., climate change, pollution, and farming) is helpful to evaluate and predict the ecological risks of environmental events. Although 70% of the Earth’s surface is covered by water, there are far fewer physiological ecology studies on aquatic animals compared with those on terrestrial animals. This Special Issue welcomes reviews and research articles on "physiological ecology of aquatic animals under extreme environment". Please send us an abstract before submission in order for us to ensure that your work falls within the scope of this Special Issue. We look forward to your valuable contribution!

Prof. Dr. Cuijuan Niu
Dr. Zuobing Zhang
Prof. Dr. Jigang Xia
Guest Editors

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Keywords

  • aquatic ecosystem
  • extreme environment
  • aquatic animals
  • physiological ecology
  • adaptive evolution
  • stress response
  • bioenergetics

Published Papers (10 papers)

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Research

16 pages, 2625 KiB  
Article
Induction of Hibernation and Changes in Physiological and Metabolic Indices in Pelodiscus sinensis
by Runlan Lin, Jiahao Wu, Ziyi You, Dongjie Xu, Caiyan Li, Wei Wang and Guoying Qian
Biology 2023, 12(5), 720; https://doi.org/10.3390/biology12050720 - 15 May 2023
Viewed by 1521
Abstract
Pelodiscus sinensis (P. sinensis) is a commonly cultivated turtle species with a habit of hibernation. To study the changes in histone expression and methylation of P. sinensis during hibernation induction, a model was established by artificial induction. Physiological and metabolic indices [...] Read more.
Pelodiscus sinensis (P. sinensis) is a commonly cultivated turtle species with a habit of hibernation. To study the changes in histone expression and methylation of P. sinensis during hibernation induction, a model was established by artificial induction. Physiological and metabolic indices were measured, and the expression and localization of histone (H1, H2A, H2B, H3, and H4) and methylation-related genes (ASH2L, KMT2A, KMT2E, KDM1A, KDM1B, and KDM5A) were measured by quantitative PCR, immunohistochemistry, and Western blot analysis. The results indicated that the metabolism, antioxidation index, and relative expression of histone methyltransferase were significantly decreased (p < 0.05), whereas the activity and expression of histone demethyltransferase were significantly increased (p < 0.05). Although our results showed significant changes in physiological and gene expression after hibernation induction, we could not confirm that P. sinensis entered deep hibernation. Therefore, for the state after cooling-induced hibernation, cold torpor might be a more accurate description. The results indicate that the P. sinensis can enter cold torpor through artificial induction, and the expression of histones may promote gene transcription. Unlike histones expressed under normal conditions, histone methylation may activate gene transcription during hibernation induction. Western blot analysis revealed that the ASH2L and KDM5A proteins were differentially expressed in the testis at different months (p < 0.05), which may perform a role in regulating gene transcription. The immunohistochemical localization of ASH2L and KDM5A in spermatogonia and spermatozoa suggests that ASH2L and KDM5A may perform a role in mitosis and meiosis. In conclusion, this study is the first to report changes in histone-related genes in reptiles, which provides insight for further studies on the physiological metabolism and histone methylation regulation of P. sinensis during the hibernation induction and hibernation period. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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13 pages, 2423 KiB  
Article
Water Hardness Improves the Antioxidant Response of Zinc-Exposed Goldfish (Carassius auratus)
by Cheol Young Choi, Min Ju Kim, Jin Ah Song and Kang Hee Kho
Biology 2023, 12(2), 289; https://doi.org/10.3390/biology12020289 - 10 Feb 2023
Cited by 1 | Viewed by 1102
Abstract
Zinc (Zn), a heavy metal, is an essential element in fish; however, exposure to high concentrations causes oxidative stress. Water hardness reduces oxidative stress reactions caused by heavy metals. To confirm the effect of water hardness on oxidative stress caused by Zn, goldfish [...] Read more.
Zinc (Zn), a heavy metal, is an essential element in fish; however, exposure to high concentrations causes oxidative stress. Water hardness reduces oxidative stress reactions caused by heavy metals. To confirm the effect of water hardness on oxidative stress caused by Zn, goldfish were exposed to various Zn concentrations (1.0, 2.0, and 5.0 mg/L) and water hardness (soft (S), hard (H), and very hard (V)). The activity of superoxide dismutase (SOD) and catalase (CAT) in plasma increased with 1.0, 2.0, and 5.0 mg/L of Zn, and decreased with H and V water hardness. The levels of H2O2 and lipid peroxide (LPO) increased with Zn above 1.0 mg/L and decreased with H and V of water hardness. Caspase-9 mRNA expression in the liver increased after 7 and 14 days of Zn exposure and decreased with H and V water hardness. It was confirmed that DNA damage was less dependent on H and V water hardness. Based on the results of this study, at least 1.0 mg/L Zn causes oxidative stress in goldfish, and a high level of apoptosis occurs when exposed for more than 7 days. It appears that the oxidative stress generated by Zn can be alleviated by water hardness of at least 270 mg/L CaCO3. This study provides information on the relationship between the antioxidant response caused by heavy metals and water hardness in fish. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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15 pages, 4613 KiB  
Article
Defense System of the Manila Clam Ruditapes philippinarum under High-Temperature and Hydrogen Sulfide Conditions
by Yi Liu, Xinmeng Wang, Yanqiu Du, Yi Zhong, Wenguang Wu, Jun Yang and Jihong Zhang
Biology 2023, 12(2), 278; https://doi.org/10.3390/biology12020278 - 09 Feb 2023
Cited by 2 | Viewed by 1281
Abstract
Hydrogen sulfide (H2S) acts as an environmental toxin. Despite its toxicity, little is known about the defense strategies of marine bivalves against it. Thus, the tolerance, behavioral characteristics, and physiological response strategies against H2S treatment in the sentinel organism [...] Read more.
Hydrogen sulfide (H2S) acts as an environmental toxin. Despite its toxicity, little is known about the defense strategies of marine bivalves against it. Thus, the tolerance, behavioral characteristics, and physiological response strategies against H2S treatment in the sentinel organism Manila clam Ruditapes philippinarum were examined. We monitored the survival and behavioral status of Manila clams exposed to different combinations of temperature and H2S. The physiological response strategies were examined by measuring the enzymatic activity of cytochrome C oxidase (CCO), fumarate reductase (FRD), superoxide dismutase (SOD), and catalase enzymes (CAT). Moreover, adverse effects of H2S on the tissue and cell structure of Manila clams were also examined under a transmission electron microscope. Manila clams responded to H2S stress through behavioral and chemical defenses. With exposure to H2S alone, Manila clams primarily enhanced aerobic respiratory metabolic pathways in the beginning stages by opening the shell and increasing the CCO activity to obtain more oxygen; with increasing exposure time, when aerobic respiration was inhibited, the shell was closed, and FRD, CAT, and SOD were activated. At this point, Manila clams responded to H2S stress through the anaerobic metabolism and antioxidant defense systems. However, high temperatures (≥28 °C) altered the defense strategy of Manila clams. With co-exposure to high temperatures and high H2S concentrations (≥20 μmol/L), the Manila clams immediately closed their shells and changed from aerobic respiration to anaerobic metabolism while immediately activating antioxidant defense systems. Nevertheless, this defense strategy was short lived. In addition to this, apparent damage to tissue and cell structures, including mitochondrial ridge dissolution and many vacuoles, was observed in Manila clams exposed to high temperatures and high H2S concentrations. Thus, prolonged exposure to high temperature and H2S damages the tissue structure of Manila clams, affecting their behavioral capacity and future survival. In summary, profiling Manila clams’ physiological response strategies to H2S exposure provided ecological behavioral support for our current understanding of H2S detrimental toxicity on marine bivalves. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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14 pages, 2210 KiB  
Article
Diverse Response Pattern to Anoxia in Three Freshwater Turtle Species
by Min Li, Cuijuan Niu and Yixuan Chen
Biology 2023, 12(1), 50; https://doi.org/10.3390/biology12010050 - 27 Dec 2022
Cited by 1 | Viewed by 1323
Abstract
With increasing water eutrophication and global warming, anoxia and hypoxia are becoming more and more common in water environments. Most vertebrates have a limited tolerance to anoxia of only a few minutes, but some species, such as turtles, can survive for months being [...] Read more.
With increasing water eutrophication and global warming, anoxia and hypoxia are becoming more and more common in water environments. Most vertebrates have a limited tolerance to anoxia of only a few minutes, but some species, such as turtles, can survive for months being exposed to anoxia. Antioxidant defense systems may have a potential role in resisting anoxia stress in freshwater turtles. The three-keeled pond turtle Chinemys reevesii, the snapping turtle Chelydra serpentina and the soft-shelled turtle Pelodiscus sinensis are three popular aquaculture species and share similar habitats in China. While C. reevesii and C. serpentina are hard-shelled turtles with poor skin permeability, P. sinensis is soft-shelled turtle whose skin permeability is good. We examined the antioxidant defense responses in different tissues of the three turtle species under acute anoxia stress for 10 h and subsequently recovered for 24 h in order to reveal the response patterns of the antioxidant defense system of the three turtle species that differed in morphological structure and life history strategy. We found that the antioxidant response patterns to acute anoxia stress were tissue- and species-specific. The soft-shelled turtle was more sensitive to anoxia than the hard-shelled turtles. Under anoxia stress, the three species kept the activities of most antioxidant enzymes stable. C. reevesii and P. sinensis were highly dependent on vitamin C in antioxidant defense, while high activities of structural antioxidant enzymes were found in the tissues of C. serpentina. The above diverse patterns may be related with adaptive evolution of morphological structure and physiological functions of the three turtle species. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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17 pages, 3936 KiB  
Article
Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming
by Ting Li, Qiuwen Chen, Qi Zhang, Tao Feng, Jianyun Zhang, Yuqing Lin, Peisi Yang, Shufeng He and Hui Zhang
Biology 2022, 11(12), 1829; https://doi.org/10.3390/biology11121829 - 15 Dec 2022
Cited by 2 | Viewed by 1578
Abstract
Field investigation indicated that the reduction in fish spawning was associated with the alteration in water temperatures, even a 2–3 °C monthly difference due to reservoir operations. However, the physiological mechanism that influences the development of fish ovary (DFO) remains unclear. Thus, experiments [...] Read more.
Field investigation indicated that the reduction in fish spawning was associated with the alteration in water temperatures, even a 2–3 °C monthly difference due to reservoir operations. However, the physiological mechanism that influences the development of fish ovary (DFO) remains unclear. Thus, experiments of Coreius guichenoti were conducted at three different temperatures, optimal temperature (~20 °C, N) for fish spawning, lower (~17 °C, L), and higher (~23 °C, H), to reveal the effects of altered water temperature on the DFO. Comparisons were made between the L and N (LvsN) conditions and H and N (HvsN) conditions. Transcriptomic analysis differentially expressed transcripts (DETs) related to heat stress were observed only in LvsN conditions, indicating that the DFO showed a stronger response to changes in LvsN than in HvsN conditions. Upregulation of DETs of vitellogenin receptors in N temperature showed that normal temperature was conducive to vitellogenin entry into the oocytes. Other temperature-sensitive DETs, including microtubule, kinesin, dynein, and actin, were closely associated with cell division and material transport. LvsN significantly impacted cell division and nutrient accumulation in the yolk, whereas HvsN only influenced cell division. Our results highlight the impact of altered water temperature on the DFO, thereby providing insights for future reservoir operations regarding river damming and climate change and establishing fish conservation measures. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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14 pages, 2221 KiB  
Article
Gut Microbial Composition and Liver Metabolite Changes Induced by Ammonia Stress in Juveniles of an Invasive Freshwater Turtle
by Han Li, Qinyuan Meng, Wanling Wang, Dongmei Mo, Wei Dang and Hongliang Lu
Biology 2022, 11(9), 1315; https://doi.org/10.3390/biology11091315 - 05 Sep 2022
Viewed by 1761
Abstract
As the most common pollutant in aquaculture systems, the toxic effects of ammonia have been extensively explored in cultured fish, molluscs, and crustaceans, but have rarely been considered in turtle species. In this study, juveniles of the invasive turtle, Trachemys scripta elegans, [...] Read more.
As the most common pollutant in aquaculture systems, the toxic effects of ammonia have been extensively explored in cultured fish, molluscs, and crustaceans, but have rarely been considered in turtle species. In this study, juveniles of the invasive turtle, Trachemys scripta elegans, were exposed to different ammonia levels (0, 0.3, 3.0, and 20.0 mg/L) for 30 days to evaluate the physiological, gut microbiomic, and liver metabolomic responses to ammonia in this turtle species. Except for a relatively low growth rate of turtles exposed to the highest concentration, ammonia exposure had no significant impact on the locomotor ability and gut microbial diversity of turtles. However, the composition of the microbial community could be altered, with some pathogenic bacteria being increased in ammonia-exposed turtles, which might indicate the change in their health status. Furthermore, hepatic metabolite profiles via liquid chromatography–mass spectrometry revealed extensive metabolic perturbations, despite being primarily involved in amino acid biosynthesis and metabolism. Overall, our results show that ammonia exposure causes gut dysbacteriosis and disturbs various metabolic pathways in aquatic turtle species. Considering discrepant defense mechanisms, the toxic impacts of ammonia at environmentally relevant concentrations on physiological performance might be less pronounced in turtles compared with fish and other invertebrates. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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15 pages, 2477 KiB  
Article
Effects of Extreme Light Cycle and Density on Melatonin, Appetite, and Energy Metabolism of the Soft-Shelled Turtle (Pelodiscus sinensis)
by Zhonghua Tang, Shifan Liu and Cuijuan Niu
Biology 2022, 11(7), 965; https://doi.org/10.3390/biology11070965 - 26 Jun 2022
Cited by 1 | Viewed by 2079
Abstract
Constant darkness and constant light exposure often disturb the circadian rhythm in the behavior and energy metabolism of vertebrates. Melatonin is known as the hormonal mediator of photoperiodic information to the central nervous system and plays a key role in food intake and [...] Read more.
Constant darkness and constant light exposure often disturb the circadian rhythm in the behavior and energy metabolism of vertebrates. Melatonin is known as the hormonal mediator of photoperiodic information to the central nervous system and plays a key role in food intake and energy balance regulation in vertebrates. The popularly cultured soft-shelled turtle Pelodiscus sinensis has been reported to grow better under constant darkness; however, the underlying physiological mechanism by which darkness benefits turtle growth is not clear yet. We hypothesized that increased melatonin levels induced by darkness would increase appetite and energy metabolism and thus promote growth in P. sinensis. In addition, in order to elucidate the interaction of photoperiod and density, juvenile turtles were treated under three photoperiods (light/dark cycle: 24L:0D, 12L:12D, 0L:24D, light density 900 lux) and two stocking densities (high density: 38.10 ind./m2, low density: 6.35 ind./m2) for 4 weeks, and then the blood and brain tissues of turtles were collected during the day (11:00–13:00) and at night (23:00–1:00) after 2 days of fasting. We examined changes in plasma melatonin levels, food intake (FI), and appetite-related hormones (plasma ghrelin and leptin), as well as growth and energy metabolism parameters such as specific growth rate (SGR), standard metabolic rate (SMR), plasma growth hormone (GH), and thyroid hormone/enzyme activity (plasma triiodothyronine T3, thyroxine T4, and T45′-deiodinase activity). Moreover, we also assessed the responses of mRNA expression levels of food intake-related genes (kisspeptin 1 (Kiss1); cocaine amphetamine-regulated transcript (CART); neuropeptide Y (NPY)) in the brain. The results showed that under high density, SGR was the lowest in 24L:0D and the highest in 0L:24D. FI was the highest in 0L:24D regardless of density. Plasma melatonin was the highest in 0L:24D under high density at night. SMR increased with decreasing light time regardless of density. Most expressions of the measured appetite-related genes (Kiss1, CART, and NPY) were not affected by photoperiod, nor were the related hormone levels, such as plasma leptin, ghrelin, and GH. However, thyroid hormones were clearly affected by photoperiod. T3 level in 0L:24D under high density during the day was the highest among all treatment groups. T4 in 24L:0D under high density during the day and T45′-deiodinase activity in 24L:0D under low density at night were significantly reduced compared with the control. Furthermore, the energy metabolism-related hormone levels were higher under higher density, especially during the day. Together, melatonin secretion is not only modulated by light but also likely to be regulated by unknown endogenous factors and density. Altered plasma melatonin induced by constant darkness and density seems to be involved in the modulation of energy metabolism rather than appetite in the soft-shelled turtle. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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12 pages, 9694 KiB  
Article
CDK5/NFAT5-Regulated Transporters Involved in Osmoregulation in Fejervarya cancrivora
by Jiao Li, Xinru Wang, Tian Lan, Yingnan Lu, Meiling Hong, Li Ding and Lijun Wang
Biology 2022, 11(6), 858; https://doi.org/10.3390/biology11060858 - 03 Jun 2022
Cited by 1 | Viewed by 2090
Abstract
Crab-eating frogs (Fejervarya cancrivora) can live in brackish water with a salinity of up to 18‰, although most amphibians are not able to tolerate such high saline environments. To investigate its potential osmoregulation, we conducted experiments in F. cancrivora and F. [...] Read more.
Crab-eating frogs (Fejervarya cancrivora) can live in brackish water with a salinity of up to 18‰, although most amphibians are not able to tolerate such high saline environments. To investigate its potential osmoregulation, we conducted experiments in F. cancrivora and F. multistriata. The results showed that F. cancrivora made use of ions (such as Na+ and Cl) to increase intracellular concentrations via the Na+/K+-ATPase (NKA) enzyme. The mRNA expression of aldose reductase (AR) was significantly higher in F. cancrivora (p < 0.05), indicating that more organic osmolytes were produced and transported to maintain cellular homeosis. The mRNA expressions of Aquaporin 1 (AQP1) and AQP3 in kidney were significantly higher in F. cancrivora, while AQP expression in skin was higher in F. multistriata (p < 0.05). The mRNA level in activating the transcription of the nuclear factor of activated T cells-5 (NFAT5) which is one of the target genes of regulating the cellular response to hypertonicity, was higher in F. cancrivora. The protein expression of CDK5, the upstream protein of the NFAT5 pathway, was 2 times higher in F. cancrivora. Therefore, we can conclude that CDK5/NFAT5-regulated transporters might be involved in osmoregulation in F. cancrivora. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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19 pages, 3208 KiB  
Article
Does a Moderately Warming Climate Compensate for the Negative Effects of UV-B Radiation on Amphibians at High Altitudes? A Test of Rana kukunoris Living on the Qinghai–Tibetan Plateau
by Xiaolong Tang, Lu Xi, Zhiyi Niu, Lun Jia, Yucheng Bai, Huihui Wang, Miaojun Ma and Qiang Chen
Biology 2022, 11(6), 838; https://doi.org/10.3390/biology11060838 - 29 May 2022
Cited by 1 | Viewed by 2085
Abstract
Both the warming climate and ultraviolet-B radiation (UVBR) are considered to be notable environmental factors affecting amphibian population decline, with particular effects on tadpole development. However, the phenotypes of tadpoles living at high altitudes may be improved by moderately warming temperatures, reducing or [...] Read more.
Both the warming climate and ultraviolet-B radiation (UVBR) are considered to be notable environmental factors affecting amphibian population decline, with particular effects on tadpole development. However, the phenotypes of tadpoles living at high altitudes may be improved by moderately warming temperatures, reducing or eliminating the negative effects of oxidative damage caused by cool temperatures or strong UVBR at high altitudes. To verify this hypothesis, Rana kukunoris tadpoles, which live at high altitudes, were used to test the effect of the interaction of temperature and UVBR on their development and antioxidant systems in a fully factorial design. The tadpoles were exposed to UVBR and UVBR-free environments at 14 (cool temperature) and 22 °C (warm temperature), respectively. UVBR and a warm temperature had opposite influences on several traits of the tadpoles, including their survival, developmental rate, individual size, preferred body temperature, thermal tolerance temperature, oxidative damage, and enzymatic and nonenzymatic antioxidant systems. The moderate temperature could compensate for or override the negative effects of UVBR by increasing the tadpoles’ preferred body temperature and critical tolerance temperature, thus enhancing the locomotion ability and thermal sensitivity of their antioxidant systems. Furthermore, the dark skin coloration and aggregation behavior of R. kukunoris tadpoles may also be effective strategies for allowing them to resist UVBR and helping them to better adapt to a warming environment with stronger UVBR. Thus, it is possible that a moderate degree of warming may increase the capacity of living organisms to adapt to environmental changes and thus have positive effects on the development of tadpoles living at high altitudes. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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14 pages, 1115 KiB  
Article
Hibernation with Rhythmicity in the Retina, Brain, and Plasma but Not in the Liver of Hibernating Giant Spiny Frogs (Quasipaa spinosa)
by Zhigang Xie, Ibrahim M. Ahmad, Lirong Zuo, Hui Wang and Dongming Li
Biology 2022, 11(5), 722; https://doi.org/10.3390/biology11050722 - 09 May 2022
Viewed by 2021
Abstract
Hibernation in ectotherms is well known, however, it is unclear how the circadian clock regulates endocrine and antioxidative defense systems of aquatic hibernators. Using the giant spiny frog (Quasipaa spinosa), we studied mRNA expression levels of (1) circadian core clock ( [...] Read more.
Hibernation in ectotherms is well known, however, it is unclear how the circadian clock regulates endocrine and antioxidative defense systems of aquatic hibernators. Using the giant spiny frog (Quasipaa spinosa), we studied mRNA expression levels of (1) circadian core clock (Bmal1, Clock, Cry1 and Per2), clock-controlled (Ror-α, Mel-1c and AANAT), and antioxidant enzyme (AOE) (SOD1, SOD2, CAT and GPx) genes in retina, brain, and liver; and (2) plasma melatonin (MT) and corticosterone (CORT) levels, over a 24-hour period at six intervals pre-hibernation and during hibernation. Our results showed that brain Bmal1, Cry1, Per2 and Mel-1c were rhythmic pre-hibernation and Clock and Ror-α during hibernation. However, the retina Bmal1, Clock and Mel-1c, and plasma MT became rhythmic during hibernation. All brain AOEs (SOD1, SOD2, CAT and GPx) were rhythmic pre-hibernation and became non-rhythmic but upregulated, except SOD1, during hibernation. However, plasma CORT and liver clocks and AOEs were non-rhythmic in both periods. The mRNA expression levels of AOEs closely resembled those of Ror-α but not plasma MT oscillations. In the hibernating aquatic frogs, these modulations of melatonin, as well as clock and clock-controlled genes and AOEs might be fundamental for them to remain relatively inactive, increase tolerance, and escape hypoxia, and to prepare for arousal. Full article
(This article belongs to the Special Issue Physiological Ecology of Aquatic Animals under Extreme Environments)
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