Pub Date : 2024-10-01Epub Date: 2024-03-26DOI: 10.1007/s00360-024-01545-5
Michael A Sackville, J Andrew Gillis, Colin J Brauner
Gill function in gas exchange and ion regulation has played key roles in the evolution of fishes. In this review, we summarize data from the fields of palaeontology, developmental biology and comparative physiology for when and how the gills first acquired these functions. Data from across disciplines strongly supports a stem vertebrate origin for gas exchange structures and function at the gills with the emergence of larger, more active fishes. However, the recent discovery of putative ionocytes in extant cephalochordates and hemichordates suggests that ion regulation at gills might have originated much earlier than gas exchange, perhaps in the ciliated pharyngeal arches in the last common ancestor of deuterostomes. We hypothesize that the ancestral form of ion regulation served a filter-feeding function in the ciliated pharyngeal arches, and was later coopted in vertebrates to regulate extracellular ion and acid-base balance. We propose that future research should explore ionocyte homology and function across extant deuterostomes to test this hypothesis and others in order to determine the ancestral origins of ion regulation in fish gills.
{"title":"The origins of gas exchange and ion regulation in fish gills: evidence from structure and function.","authors":"Michael A Sackville, J Andrew Gillis, Colin J Brauner","doi":"10.1007/s00360-024-01545-5","DOIUrl":"10.1007/s00360-024-01545-5","url":null,"abstract":"<p><p>Gill function in gas exchange and ion regulation has played key roles in the evolution of fishes. In this review, we summarize data from the fields of palaeontology, developmental biology and comparative physiology for when and how the gills first acquired these functions. Data from across disciplines strongly supports a stem vertebrate origin for gas exchange structures and function at the gills with the emergence of larger, more active fishes. However, the recent discovery of putative ionocytes in extant cephalochordates and hemichordates suggests that ion regulation at gills might have originated much earlier than gas exchange, perhaps in the ciliated pharyngeal arches in the last common ancestor of deuterostomes. We hypothesize that the ancestral form of ion regulation served a filter-feeding function in the ciliated pharyngeal arches, and was later coopted in vertebrates to regulate extracellular ion and acid-base balance. We propose that future research should explore ionocyte homology and function across extant deuterostomes to test this hypothesis and others in order to determine the ancestral origins of ion regulation in fish gills.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"557-568"},"PeriodicalIF":1.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140295375","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-01Epub Date: 2024-03-30DOI: 10.1007/s00360-024-01548-2
Michael G Jonz
Seminal studies from the early 20th century defined the structural changes associated with development and regeneration of the gills in goldfish at the gross morphological and cellular levels using standard techniques of light and electron microscopy. More recently, investigations using cell lineage tracing, molecular biology, immunohistochemistry and single-cell RNA-sequencing have pushed the field forward and have begun to reveal the cellular and molecular processes that orchestrate cell proliferation and regeneration in the gills. The gill is a multifunctional organ that mediates an array of important physiological functions, including respiration, ion regulation and excretion of waste products. It is comprised of unique cell types, such as pavement cells, ionocytes, chemoreceptors and undifferentiated stem or progenitor cells that regulate growth and replenish cell populations. The gills develop from the embryonic endoderm and are rich in cell types derived from the neural crest. The gills have the capacity to remodel themselves in response to environmental change, such as in the case of ionocytes, chemoreceptors and the interlamellar cell mass, and can completely regenerate gill filaments and lamellae. Both processes of remodeling and regeneration invariably involve cell proliferation. Although gill regeneration has been reported in only a limited number of fish species, the process appears to have many similarities to regeneration of other organs in fish and amphibians. The present article reviews the studies that have described gill development and growth, and that demonstrate a suite of genes, transcription factors and other proteins involved in cell proliferation and regeneration in the gills.
{"title":"Cell proliferation and regeneration in the gill.","authors":"Michael G Jonz","doi":"10.1007/s00360-024-01548-2","DOIUrl":"10.1007/s00360-024-01548-2","url":null,"abstract":"<p><p>Seminal studies from the early 20th century defined the structural changes associated with development and regeneration of the gills in goldfish at the gross morphological and cellular levels using standard techniques of light and electron microscopy. More recently, investigations using cell lineage tracing, molecular biology, immunohistochemistry and single-cell RNA-sequencing have pushed the field forward and have begun to reveal the cellular and molecular processes that orchestrate cell proliferation and regeneration in the gills. The gill is a multifunctional organ that mediates an array of important physiological functions, including respiration, ion regulation and excretion of waste products. It is comprised of unique cell types, such as pavement cells, ionocytes, chemoreceptors and undifferentiated stem or progenitor cells that regulate growth and replenish cell populations. The gills develop from the embryonic endoderm and are rich in cell types derived from the neural crest. The gills have the capacity to remodel themselves in response to environmental change, such as in the case of ionocytes, chemoreceptors and the interlamellar cell mass, and can completely regenerate gill filaments and lamellae. Both processes of remodeling and regeneration invariably involve cell proliferation. Although gill regeneration has been reported in only a limited number of fish species, the process appears to have many similarities to regeneration of other organs in fish and amphibians. The present article reviews the studies that have described gill development and growth, and that demonstrate a suite of genes, transcription factors and other proteins involved in cell proliferation and regeneration in the gills.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"583-593"},"PeriodicalIF":1.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140330322","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-01Epub Date: 2024-06-25DOI: 10.1007/s00360-024-01565-1
Raymond W M Kwong
In fish, the gill plays a vital role in regulating the absorption of trace metals and is also highly susceptible to metal toxicity. Trace metals such as iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn) are involved in various catalytic activities and molecular binding within the gill, thereby supporting a range of physiological processes in this organ. While beneficial at normal levels, these metals can become toxic when present in excess. Conversely, nonessential metals like cadmium (Cd) and lead (Pb) can gain entry into gill cells through similar metal transport pathways, potentially interfering with various cellular processes. The transepithelial transport of these metals across the gill epithelium is governed by a variety of metal transport and metal binding proteins. These include the Cu transporter 1 (CTR1), divalent metal transporter 1 (DMT1), and members of the Zrt-/Irt-like protein (ZIP) and zinc transport (ZnT) families. Additionally, some of these metals can compete with major ions (e.g., calcium, sodium) for absorption sites in the gill. This complex crosstalk suggests an interdependent mechanism that balances metal uptake to meet physiological needs while preventing excessive accumulation. In this article, I review the roles of trace metals in proteins/enzymes that support the different functions in the gill of teleost fish. I also discuss current understanding of the pathways involved in regulating the branchial uptake of metals and their influence on ionic regulation, and the potential detoxification mechanisms in the gill. Finally, I summarize knowledge gaps and potential areas for further investigation.
{"title":"Trace metals in the teleost fish gill: biological roles, uptake regulation, and detoxification mechanisms.","authors":"Raymond W M Kwong","doi":"10.1007/s00360-024-01565-1","DOIUrl":"10.1007/s00360-024-01565-1","url":null,"abstract":"<p><p>In fish, the gill plays a vital role in regulating the absorption of trace metals and is also highly susceptible to metal toxicity. Trace metals such as iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn) are involved in various catalytic activities and molecular binding within the gill, thereby supporting a range of physiological processes in this organ. While beneficial at normal levels, these metals can become toxic when present in excess. Conversely, nonessential metals like cadmium (Cd) and lead (Pb) can gain entry into gill cells through similar metal transport pathways, potentially interfering with various cellular processes. The transepithelial transport of these metals across the gill epithelium is governed by a variety of metal transport and metal binding proteins. These include the Cu transporter 1 (CTR1), divalent metal transporter 1 (DMT1), and members of the Zrt-/Irt-like protein (ZIP) and zinc transport (ZnT) families. Additionally, some of these metals can compete with major ions (e.g., calcium, sodium) for absorption sites in the gill. This complex crosstalk suggests an interdependent mechanism that balances metal uptake to meet physiological needs while preventing excessive accumulation. In this article, I review the roles of trace metals in proteins/enzymes that support the different functions in the gill of teleost fish. I also discuss current understanding of the pathways involved in regulating the branchial uptake of metals and their influence on ionic regulation, and the potential detoxification mechanisms in the gill. Finally, I summarize knowledge gaps and potential areas for further investigation.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"749-763"},"PeriodicalIF":1.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141447667","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-01Epub Date: 2024-07-31DOI: 10.1007/s00360-024-01575-z
Deep Soor, Liam R Tigert, Elissa Khodikian, Arsheen Bozai, Gwangseok R Yoon, Cosima S Porteus
Coastal marine environments are characterized by daily, seasonal and long-term changes in both O2 and CO2, driven by local biotic and abiotic factors. The neuroepithelial cells (NECs) of fish are thought to be the putative chemoreceptors for sensing oxygen and CO2, and, thus, NECs play a key role in detecting these environmental changes. However, the role of NECs as chemosensors in marine fish remains largely understudied. In this study, the NECs of marine threespine sticklebacks (Gasterosteus aculeatus) were characterized using immunohistochemistry. We then determined if there were changes in NEC size and density, and in gill morphology in response to either mild (10 kPa) or moderate (6.8 kPa) hypoxia and two levels of elevated CO2 (1,500 and 3,000 µatm). We found that the NECs of stickleback contained synaptic vesicles and were innervated, and were 50-300% larger and 2 to 4 times more abundant than in other similar sized freshwater fishes. NEC size and density were largely unaffected by exposure to hypoxia, but there was a 50% decrease in interlamellar cell mass (ILCM) in response to mild and moderate hypoxia. NECs increased in size, but not abundance in response to elevated CO2. Moreover, fish exposed to moderate or elevated CO2 had 53-78% larger ILCMs compared to control fish. Our results demonstrated that adult marine sticklebacks have NECs that can respond to environmentally relevant pCO2 and likely hypoxia, which highlights the importance of NECs in marine fishes under the heterogeneity of environmental conditions in coastal areas.
{"title":"Changes in gill neuroepithelial cells and morphology of threespine stickleback (Gasterosteus aculeatus) to hypoxia and simulated ocean acidification.","authors":"Deep Soor, Liam R Tigert, Elissa Khodikian, Arsheen Bozai, Gwangseok R Yoon, Cosima S Porteus","doi":"10.1007/s00360-024-01575-z","DOIUrl":"10.1007/s00360-024-01575-z","url":null,"abstract":"<p><p>Coastal marine environments are characterized by daily, seasonal and long-term changes in both O<sub>2</sub> and CO<sub>2</sub>, driven by local biotic and abiotic factors. The neuroepithelial cells (NECs) of fish are thought to be the putative chemoreceptors for sensing oxygen and CO<sub>2</sub>, and, thus, NECs play a key role in detecting these environmental changes. However, the role of NECs as chemosensors in marine fish remains largely understudied. In this study, the NECs of marine threespine sticklebacks (Gasterosteus aculeatus) were characterized using immunohistochemistry. We then determined if there were changes in NEC size and density, and in gill morphology in response to either mild (10 kPa) or moderate (6.8 kPa) hypoxia and two levels of elevated CO<sub>2</sub> (1,500 and 3,000 µatm). We found that the NECs of stickleback contained synaptic vesicles and were innervated, and were 50-300% larger and 2 to 4 times more abundant than in other similar sized freshwater fishes. NEC size and density were largely unaffected by exposure to hypoxia, but there was a 50% decrease in interlamellar cell mass (ILCM) in response to mild and moderate hypoxia. NECs increased in size, but not abundance in response to elevated CO<sub>2</sub>. Moreover, fish exposed to moderate or elevated CO<sub>2</sub> had 53-78% larger ILCMs compared to control fish. Our results demonstrated that adult marine sticklebacks have NECs that can respond to environmentally relevant pCO<sub>2</sub> and likely hypoxia, which highlights the importance of NECs in marine fishes under the heterogeneity of environmental conditions in coastal areas.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"765-777"},"PeriodicalIF":1.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141861799","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-01Epub Date: 2024-07-03DOI: 10.1007/s00360-024-01574-0
Liliane Soares Presa, Carlos Eduardo Copatti, Daniel Sá Britto Pinto, José Maria Monserrat, Luciano Garcia
The present study investigated the best photoperiod for culturing pacu (Piaractus mesopotamicus) in recirculation aquaculture systems (RAS) based on its growth performance and hematological and oxidative stress responses. Juveniles (∼ 5 g) were subjected to five treatments (in triplicate): 24 L (light):0D (dark), 15 L: 09D, 12 L:12D, 9 L:15D, and 0 L:24D for 45 days. A total of 225 pacu individuals were randomly distributed among 15 tanks of 210 L (n = 15 per tank). Zootechnical, hematological (glucose, lactate, hematocrit, and hemoglobin), and antioxidant and oxidative stress parameters (glutathione S-transferase (GST), total antioxidant capacity against peroxyl radicals (ACAP), and lipid peroxidation (LPO) were analyzed. The zootechnical parameters (e.g., weight gain, Fulton's condition factor, and specific growth rate) were better and worse with 9 L:15D and 24 L:0D photoperiods, respectively. The hepatosomatic index was higher and lower in the 0 L:24D and 9 L:15D photoperiods. Blood lactate levels and antioxidant and oxidative stress responses were increased in the longest photoperiods (15 L:9D and 24 L:0D). In contrast, the treatments that showed lower oxidative damage (liver, gills, brain, and muscle) were 9 L:15D and 12 L:12D. In conclusion, manipulating artificial light is one way to improve fish growth and health, where the best photoperiod for pacu farming in RAS is 9 L:15D.
{"title":"Can photoperiod improve growth performance and antioxidant responses of pacu (Piaractus mesopotamicus) reared in recirculation aquaculture systems?","authors":"Liliane Soares Presa, Carlos Eduardo Copatti, Daniel Sá Britto Pinto, José Maria Monserrat, Luciano Garcia","doi":"10.1007/s00360-024-01574-0","DOIUrl":"10.1007/s00360-024-01574-0","url":null,"abstract":"<p><p>The present study investigated the best photoperiod for culturing pacu (Piaractus mesopotamicus) in recirculation aquaculture systems (RAS) based on its growth performance and hematological and oxidative stress responses. Juveniles (∼ 5 g) were subjected to five treatments (in triplicate): 24 L (light):0D (dark), 15 L: 09D, 12 L:12D, 9 L:15D, and 0 L:24D for 45 days. A total of 225 pacu individuals were randomly distributed among 15 tanks of 210 L (n = 15 per tank). Zootechnical, hematological (glucose, lactate, hematocrit, and hemoglobin), and antioxidant and oxidative stress parameters (glutathione S-transferase (GST), total antioxidant capacity against peroxyl radicals (ACAP), and lipid peroxidation (LPO) were analyzed. The zootechnical parameters (e.g., weight gain, Fulton's condition factor, and specific growth rate) were better and worse with 9 L:15D and 24 L:0D photoperiods, respectively. The hepatosomatic index was higher and lower in the 0 L:24D and 9 L:15D photoperiods. Blood lactate levels and antioxidant and oxidative stress responses were increased in the longest photoperiods (15 L:9D and 24 L:0D). In contrast, the treatments that showed lower oxidative damage (liver, gills, brain, and muscle) were 9 L:15D and 12 L:12D. In conclusion, manipulating artificial light is one way to improve fish growth and health, where the best photoperiod for pacu farming in RAS is 9 L:15D.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"443-455"},"PeriodicalIF":1.7,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141494413","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-01Epub Date: 2024-06-16DOI: 10.1007/s00360-024-01570-4
Mahdi Golshan, Sayyed Mohammad Hadi Alavi, Azadeh Hatef, Negar Kazori, Magdalena Socha, Sylvain Milla, Mirosława Sokołowska-Mikołajczyk, Suraj Unniappan, Ian A E Butts, Otomar Linhart
There is a link between metabolism and reproduction as metabolic hormones affect hypothalamus-pituitary-testis (HPT) hormonal functions and vice versa. The aim of the present study was to investigate the effects of negative energy balance on the reproductive system in male goldfish exposed to testosterone (T) and 17β-estradiol (E2). Following 7 days of food deprivation (FD), ANOVA models showed significant FD × sex steroid interactions on sperm quality and circulating sex steroid levels. When FD effects were investigated, 11-ketotestosterone (11-KT) level and sperm motility and velocity decreased in food-deprived goldfish in the control group. In E2-exposed goldfish, FD decreased sperm production in addition to sperm motility and velocity that coincided with an elevation of circulating E2 level. However, FD did not significantly impact sex steroids and sperm quality in T-exposed goldfish. ANOVA models showed non-significant FD × sex steroid interactions for HSI, GSI, circulating luteinizing hormone (Lh) level, and metabolic (preproghrelin, goat and nucb2) and reproductive (kiss1, gpr54 and gnrh3) mRNAs. Furthermore, results showed that FD decreased HSI, and increased Lh levels and testicular preproghrelin and goat mRNAs, while sex steroids increased mid-brain nucb2, kiss1 and gpr54 mRNAs. Together, our results suggest that FD-induced inhibition of androgenesis resulted in diminished sperm quality associated with activation of the testicular ghrelinergic system, and negative feedback of 11-KT increased Lh level. The FD-induced testicular metabolic and hormonal system was impacted in goldfish exposed to sex steroids. However, the negative effects of FD on sperm quality were accelerated in E2-exposed goldfish due to estrogenic activity. This study provides novel information to better understand metabolic-associated reproductive disorders in fish.
{"title":"Impact of absolute food deprivation on the reproductive system in male goldfish exposed to sex steroids.","authors":"Mahdi Golshan, Sayyed Mohammad Hadi Alavi, Azadeh Hatef, Negar Kazori, Magdalena Socha, Sylvain Milla, Mirosława Sokołowska-Mikołajczyk, Suraj Unniappan, Ian A E Butts, Otomar Linhart","doi":"10.1007/s00360-024-01570-4","DOIUrl":"10.1007/s00360-024-01570-4","url":null,"abstract":"<p><p>There is a link between metabolism and reproduction as metabolic hormones affect hypothalamus-pituitary-testis (HPT) hormonal functions and vice versa. The aim of the present study was to investigate the effects of negative energy balance on the reproductive system in male goldfish exposed to testosterone (T) and 17β-estradiol (E<sub>2</sub>). Following 7 days of food deprivation (FD), ANOVA models showed significant FD × sex steroid interactions on sperm quality and circulating sex steroid levels. When FD effects were investigated, 11-ketotestosterone (11-KT) level and sperm motility and velocity decreased in food-deprived goldfish in the control group. In E<sub>2</sub>-exposed goldfish, FD decreased sperm production in addition to sperm motility and velocity that coincided with an elevation of circulating E<sub>2</sub> level. However, FD did not significantly impact sex steroids and sperm quality in T-exposed goldfish. ANOVA models showed non-significant FD × sex steroid interactions for HSI, GSI, circulating luteinizing hormone (Lh) level, and metabolic (preproghrelin, goat and nucb2) and reproductive (kiss1, gpr54 and gnrh3) mRNAs. Furthermore, results showed that FD decreased HSI, and increased Lh levels and testicular preproghrelin and goat mRNAs, while sex steroids increased mid-brain nucb2, kiss1 and gpr54 mRNAs. Together, our results suggest that FD-induced inhibition of androgenesis resulted in diminished sperm quality associated with activation of the testicular ghrelinergic system, and negative feedback of 11-KT increased Lh level. The FD-induced testicular metabolic and hormonal system was impacted in goldfish exposed to sex steroids. However, the negative effects of FD on sperm quality were accelerated in E<sub>2</sub>-exposed goldfish due to estrogenic activity. This study provides novel information to better understand metabolic-associated reproductive disorders in fish.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"411-426"},"PeriodicalIF":1.7,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141332580","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-01Epub Date: 2024-07-08DOI: 10.1007/s00360-024-01573-1
Gerhard Heldmaier, Luzie Braulke, Johanna Flick, Thomas Ruf
Ultradian rhythms of metabolism, body temperature and activity are attenuated or disappear completely during torpor in Djungarian hamsters, for all three ultradian periodicities (URsmall, URmedium and URlarge). URsmall and URmedium disappear during entrance into torpor, whereas URlarge disappear later or continue with a low amplitude. This suggests a tight functional link between torpor and the expression of ultradian rhythms, i.e. torpor is achieved by suppression of metabolic rate as well as silencing of ultradian rhythms. Spontaneous torpor is often initiated after an ultradian burst of activity and metabolic rate, beginning with a period of motionless rest and accompanied by a decrease of metabolic rate and body temperature. To extend previous findings on the potential role of the adrenergic system on torpor induction we analysed the influence of the ß3-adrenergic agonist Mirabegron on torpor in Djungarian hamsters, as compared to the influence of the ß-adrenergic antagonist Propranolol. Hamsters were implanted with 10 day release pellets of Mirabegron (0.06 mg day-1) or Propranolol (0.3 mg day-1). Mirabegron transiently supressed and accelerated ultradian rhythms but had no effect on torpor behaviour. Propranolol did not affect torpor behaviour nor the expression of ultradian rhythms with the dosage applied during this study.
{"title":"Silencing of ultradian rhythms and metabolic depression during spontaneous daily torpor in Djungarian hamsters.","authors":"Gerhard Heldmaier, Luzie Braulke, Johanna Flick, Thomas Ruf","doi":"10.1007/s00360-024-01573-1","DOIUrl":"10.1007/s00360-024-01573-1","url":null,"abstract":"<p><p>Ultradian rhythms of metabolism, body temperature and activity are attenuated or disappear completely during torpor in Djungarian hamsters, for all three ultradian periodicities (URsmall, URmedium and URlarge). URsmall and URmedium disappear during entrance into torpor, whereas URlarge disappear later or continue with a low amplitude. This suggests a tight functional link between torpor and the expression of ultradian rhythms, i.e. torpor is achieved by suppression of metabolic rate as well as silencing of ultradian rhythms. Spontaneous torpor is often initiated after an ultradian burst of activity and metabolic rate, beginning with a period of motionless rest and accompanied by a decrease of metabolic rate and body temperature. To extend previous findings on the potential role of the adrenergic system on torpor induction we analysed the influence of the ß3-adrenergic agonist Mirabegron on torpor in Djungarian hamsters, as compared to the influence of the ß-adrenergic antagonist Propranolol. Hamsters were implanted with 10 day release pellets of Mirabegron (0.06 mg day<sup>-1</sup>) or Propranolol (0.3 mg day<sup>-1</sup>). Mirabegron transiently supressed and accelerated ultradian rhythms but had no effect on torpor behaviour. Propranolol did not affect torpor behaviour nor the expression of ultradian rhythms with the dosage applied during this study.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"519-535"},"PeriodicalIF":1.7,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11316710/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141556029","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-01Epub Date: 2024-07-02DOI: 10.1007/s00360-024-01564-2
Elena N Surkova, Ludmila E Savinetskaya, Ivan S Khropov, Andrey V Tchabovsky
Individuals colonizing new areas at expanding ranges encounter numerous and unpredictable stressors. Exposure to unfamiliar environments suggests that colonists would differ in stress levels from residents living in familiar conditions. Few empirical studies tested this hypothesis and produced mixed results, and the role of stress regulation in colonization remains unclear. Studies relating stress levels to colonization mainly use a geographical analysis comparing established colonist populations with source populations. We used faecal glucocorticoid metabolites (FGMs) to assess both spatial and temporal dynamics of stress levels in an expanding population of midday gerbils (Meriones meridianus). We demonstrated that adult males and females had higher FGM levels in newly emerged colonies, compared with the source population, but differed in the pattern of FGM dynamics post-foundation. In males, FGM levels sharply decreased in the second year after colony establishment. In females, FGM levels did not change with time and remained high despite the decreasing environmental unpredictability, exhibiting among-individual variation. Increased stress levels of colonist males damping with time post-colonization suggest they are flexible in responding to immediate changes in environmental uncertainty. On the contrary, high and stable over generations stress levels uncoupled from the changes in the environmental uncertainty in female colonists imply that they carry a relatively constant phenotype associated with the reactive coping strategy favouring colonization. We link sex differences in consistency and plasticity in stress regulation during colonization to the sex-specific life-history strategies.
{"title":"Flexible males, reactive females: faecal glucocorticoid metabolites indicate increased stress in the colonist population, damping with time in males but not in females.","authors":"Elena N Surkova, Ludmila E Savinetskaya, Ivan S Khropov, Andrey V Tchabovsky","doi":"10.1007/s00360-024-01564-2","DOIUrl":"10.1007/s00360-024-01564-2","url":null,"abstract":"<p><p>Individuals colonizing new areas at expanding ranges encounter numerous and unpredictable stressors. Exposure to unfamiliar environments suggests that colonists would differ in stress levels from residents living in familiar conditions. Few empirical studies tested this hypothesis and produced mixed results, and the role of stress regulation in colonization remains unclear. Studies relating stress levels to colonization mainly use a geographical analysis comparing established colonist populations with source populations. We used faecal glucocorticoid metabolites (FGMs) to assess both spatial and temporal dynamics of stress levels in an expanding population of midday gerbils (Meriones meridianus). We demonstrated that adult males and females had higher FGM levels in newly emerged colonies, compared with the source population, but differed in the pattern of FGM dynamics post-foundation. In males, FGM levels sharply decreased in the second year after colony establishment. In females, FGM levels did not change with time and remained high despite the decreasing environmental unpredictability, exhibiting among-individual variation. Increased stress levels of colonist males damping with time post-colonization suggest they are flexible in responding to immediate changes in environmental uncertainty. On the contrary, high and stable over generations stress levels uncoupled from the changes in the environmental uncertainty in female colonists imply that they carry a relatively constant phenotype associated with the reactive coping strategy favouring colonization. We link sex differences in consistency and plasticity in stress regulation during colonization to the sex-specific life-history strategies.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"545-554"},"PeriodicalIF":1.7,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141494415","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-01Epub Date: 2024-05-15DOI: 10.1007/s00360-024-01559-z
Kate J Dutton-Regester, Alice Roser, Haley Meer, Andrew Hill, Michael Pyne, Aiman Al-Najjar, Tim Whaites, Jane C Fenelon, Katherine L Buchanan, Tamara Keeley, Marilyn B Renfree, Stephen D Johnston
It is possible that the reproductive strategy of the short-beaked echidna is related to seasonal changes in fat deposition and energy availability, regulated by seasonal changes in endocrine function. We predicted that circulating leptin levels would be directly proportional to adiposity during most of the year, but that a change in this relationship would occur during the pre-breeding season to allow increased fat deposition. To test this hypothesis, we made use of a captive colony of echidnas to describe and quantify changes in fat distribution and the adipostatic hormone leptin. First we assessed seasonal changes in circulating leptin levels, body mass and adiposity for three male and three female adult echidnas maintained on a standard diet. Second, we explored the relationship between circulating leptin levels and increased caloric intake for an additional five adult female echidnas that were provided with supplemented nutrition. Third we visualised fat distribution in male and female adult echidnas using magnetic resonance imaging (MRI) before and after the breeding season, to determine where fat is deposited in this species. For echidnas maintained on the standard diet, there were no seasonal changes in body mass, body fat or plasma leptin levels. However, female echidnas provided with supplemented nutrition had significantly elevated plasma leptin levels during the breeding season, compared to the pre-and post- breeding periods. MRI showed substantial subcutaneous fat depots extending dorso-laterally from the base of the skull to the base of the tail, in both sexes. Pre-breeding season, both sexes had considerable fat deposition in the pelvic/rump region, whilst the female echidna accumulated most fat in the abdominal region. This study shows that male and female echidnas accumulate body fat in the pelvic/rump and the abdominal regions, respectively and that circulating leptin may promote fattening in female echidnas during the breeding season by means of leptin resistance. However, further research is required to evaluate the precise relationship between seasonal changes in leptin and adiposity.
{"title":"Body fat and circulating leptin levels in the captive short-beaked echidna (Tachyglossus aculeatus).","authors":"Kate J Dutton-Regester, Alice Roser, Haley Meer, Andrew Hill, Michael Pyne, Aiman Al-Najjar, Tim Whaites, Jane C Fenelon, Katherine L Buchanan, Tamara Keeley, Marilyn B Renfree, Stephen D Johnston","doi":"10.1007/s00360-024-01559-z","DOIUrl":"10.1007/s00360-024-01559-z","url":null,"abstract":"<p><p>It is possible that the reproductive strategy of the short-beaked echidna is related to seasonal changes in fat deposition and energy availability, regulated by seasonal changes in endocrine function. We predicted that circulating leptin levels would be directly proportional to adiposity during most of the year, but that a change in this relationship would occur during the pre-breeding season to allow increased fat deposition. To test this hypothesis, we made use of a captive colony of echidnas to describe and quantify changes in fat distribution and the adipostatic hormone leptin. First we assessed seasonal changes in circulating leptin levels, body mass and adiposity for three male and three female adult echidnas maintained on a standard diet. Second, we explored the relationship between circulating leptin levels and increased caloric intake for an additional five adult female echidnas that were provided with supplemented nutrition. Third we visualised fat distribution in male and female adult echidnas using magnetic resonance imaging (MRI) before and after the breeding season, to determine where fat is deposited in this species. For echidnas maintained on the standard diet, there were no seasonal changes in body mass, body fat or plasma leptin levels. However, female echidnas provided with supplemented nutrition had significantly elevated plasma leptin levels during the breeding season, compared to the pre-and post- breeding periods. MRI showed substantial subcutaneous fat depots extending dorso-laterally from the base of the skull to the base of the tail, in both sexes. Pre-breeding season, both sexes had considerable fat deposition in the pelvic/rump region, whilst the female echidna accumulated most fat in the abdominal region. This study shows that male and female echidnas accumulate body fat in the pelvic/rump and the abdominal regions, respectively and that circulating leptin may promote fattening in female echidnas during the breeding season by means of leptin resistance. However, further research is required to evaluate the precise relationship between seasonal changes in leptin and adiposity.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"457-471"},"PeriodicalIF":1.7,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11316712/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140923421","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-01Epub Date: 2024-07-05DOI: 10.1007/s00360-024-01569-x
Gerhard Heldmaier, Luzie Braulke, Johanna Flick, Thomas Ruf
Djungarian hamsters (Phodopus sungorus) living at constant 15 °C Ta in short photoperiod (8:16 h L:D) showed pronounced ultradian rhythms (URs) of metabolic rate (MR), body temperature (Tb) and locomotor activity. The ultradian patterns differed between individuals and varied over time. The period length of URs for MR, Tb and activity was similar although not identical. Wavelet analysis showed that three different URs are existing in parallel, URs of small amplitude and short duration (URsmall), URs of medium amplitude and medium duration (URmedium) and URs of large amplitude (URlarge), superimposed on each other. URlarge were accompanied by an increase in locomotor activity, whereas URsmall and URmedium were of metabolic origin with lacking or delayed responses of activity. An energetic challenge to cold which raised total energy requirements by about 50% did not accelerate the period length of URs, but extended the amplitude of URsmall and URmedium. URlarge corresponds with the URs of activity, feeding and drinking, sleep and arousal as described in previous studies, which are related to midbrain dopaminergic signalling and hypothalamic ultradian signalling. The cause and control of URmedium and URsmall is unknown. Their periods are similar to periods of central and peripheral endocrine ultradian signalling, suggesting a link with URs of metabolism.
生活在恒定 15 °C、短光周期(8:16 h L:D)条件下的滇仓鼠(Phodopus sungorus)表现出明显的新陈代谢率(MR)、体温(Tb)和运动活动的超昼夜节律(UR)。不同个体的超昼夜节律模式不同,且随时间而变化。新陈代谢率(MR)、体温(Tb)和活动(UR)的周期长度虽然不尽相同,但却相似。小波分析表明,有三种不同的UR并行存在,即小振幅和短持续时间的UR(UR小)、中等振幅和中等持续时间的UR(UR中)和大振幅的UR(UR大),它们相互叠加。大振幅UR伴随着运动活动的增加,而小振幅UR和中振幅UR则源于新陈代谢,缺乏或延迟活动反应。寒冷带来的能量挑战使总能量需求增加了约50%,但这并没有加快URs的周期长度,反而延长了URsmall和URmedium的振幅。UR大与之前研究中描述的活动、进食和饮水、睡眠和唤醒的UR相对应,这与中脑多巴胺能信号和下丘脑超昼夜节律信号有关。UR中和UR小的原因和控制尚不清楚。它们的周期与中枢和外周内分泌的昼夜节律信号周期相似,这表明它们与新陈代谢的昼夜节律信号有关。
{"title":"Multiple ultradian rhythms of metabolism, body temperature and activity in Djungarian hamsters.","authors":"Gerhard Heldmaier, Luzie Braulke, Johanna Flick, Thomas Ruf","doi":"10.1007/s00360-024-01569-x","DOIUrl":"10.1007/s00360-024-01569-x","url":null,"abstract":"<p><p>Djungarian hamsters (Phodopus sungorus) living at constant 15 °C T<sub>a</sub> in short photoperiod (8:16 h L:D) showed pronounced ultradian rhythms (URs) of metabolic rate (MR), body temperature (T<sub>b</sub>) and locomotor activity. The ultradian patterns differed between individuals and varied over time. The period length of URs for MR, T<sub>b</sub> and activity was similar although not identical. Wavelet analysis showed that three different URs are existing in parallel, URs of small amplitude and short duration (URsmall), URs of medium amplitude and medium duration (URmedium) and URs of large amplitude (URlarge), superimposed on each other. URlarge were accompanied by an increase in locomotor activity, whereas URsmall and URmedium were of metabolic origin with lacking or delayed responses of activity. An energetic challenge to cold which raised total energy requirements by about 50% did not accelerate the period length of URs, but extended the amplitude of URsmall and URmedium. URlarge corresponds with the URs of activity, feeding and drinking, sleep and arousal as described in previous studies, which are related to midbrain dopaminergic signalling and hypothalamic ultradian signalling. The cause and control of URmedium and URsmall is unknown. Their periods are similar to periods of central and peripheral endocrine ultradian signalling, suggesting a link with URs of metabolism.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"501-518"},"PeriodicalIF":1.7,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11316713/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141536046","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}