Pub Date : 2025-02-01Epub Date: 2025-01-16DOI: 10.1007/s00360-024-01601-0
Alyssa M Weinrauch, Tamzin A Blewett, W Gary Anderson
Elasmobranchs are commonly carnivores and are important in energy transfer across marine ecosystems. Despite this, relatively few studies have examined the physiological underpinnings of nutrient acquisition in these animals. Here, we investigated the mechanisms of uptake at the spiral valve intestine for two representative amino acids (L-alanine, L-leucine) and one representative fatty acid (oleic acid), each common to the diet of a carnivore, the Pacific spiny dogfish (Squalus suckleyi). Transport was saturable for all three nutrients, depending upon transport calculation metric (i.e., mucosal disappearance, serosal appearance, or tissue accumulation). Over 0-10 mM range of amino acids the concentration at which ½ maximal transport occurred (Km; a measure of transporter affinity) was 11.9 and 11.2 mM for tissue accumulation of alanine and leucine, respectively. Oleic acid transport was measured at lower concentrations (0-200 µM) and tissue accumulation did not reach saturation. Putative amino acid transport systems were delineated upon confirmation of sodium dependence and competitive inhibition with threonine, glycine, and lysine. The interplay of nutrient combinations on the modulation of nutrient acquisition rates, which better mimics the complex composition of both a meal and the internal osmolytes, was next investigated. Here, the application of serosal oleic acid led to diminished mucosal disappearance of leucine. Feeding did not significantly alter transport rates, perhaps indicative of maximal transport of these energy sources whenever the substrate is available given their importance both as metabolic fuels and precursors to the osmolyte urea.
{"title":"Characterisation of intestinal amino acid and oleic acid absorption and their interaction in the Pacific spiny dogfish (Squalus suckleyi).","authors":"Alyssa M Weinrauch, Tamzin A Blewett, W Gary Anderson","doi":"10.1007/s00360-024-01601-0","DOIUrl":"10.1007/s00360-024-01601-0","url":null,"abstract":"<p><p>Elasmobranchs are commonly carnivores and are important in energy transfer across marine ecosystems. Despite this, relatively few studies have examined the physiological underpinnings of nutrient acquisition in these animals. Here, we investigated the mechanisms of uptake at the spiral valve intestine for two representative amino acids (<sub>L</sub>-alanine, <sub>L</sub>-leucine) and one representative fatty acid (oleic acid), each common to the diet of a carnivore, the Pacific spiny dogfish (Squalus suckleyi). Transport was saturable for all three nutrients, depending upon transport calculation metric (i.e., mucosal disappearance, serosal appearance, or tissue accumulation). Over 0-10 mM range of amino acids the concentration at which ½ maximal transport occurred (K<sub>m</sub>; a measure of transporter affinity) was 11.9 and 11.2 mM for tissue accumulation of alanine and leucine, respectively. Oleic acid transport was measured at lower concentrations (0-200 µM) and tissue accumulation did not reach saturation. Putative amino acid transport systems were delineated upon confirmation of sodium dependence and competitive inhibition with threonine, glycine, and lysine. The interplay of nutrient combinations on the modulation of nutrient acquisition rates, which better mimics the complex composition of both a meal and the internal osmolytes, was next investigated. Here, the application of serosal oleic acid led to diminished mucosal disappearance of leucine. Feeding did not significantly alter transport rates, perhaps indicative of maximal transport of these energy sources whenever the substrate is available given their importance both as metabolic fuels and precursors to the osmolyte urea.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"53-65"},"PeriodicalIF":1.7,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143016297","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 : 2025-02-01Epub Date: 2024-10-08DOI: 10.1007/s00360-024-01585-x
Richard W Hill, Jacob J Manteuffel, Bradley A White
Nestling white-footed mice (Peromyscus leucopus) are born in the earliest days of spring in cold climates. If the nestlings are by accident exposed to ambient temperatures near freezing (0-7 °C) at early ages (2-10 days old), they may experience body temperatures (Tbs) equally low. During such hypothermia, although their heart keeps beating, they become apneic (cease inhaling and exhaling). However, they have an exceptional ability (e.g., compared to Mus musculus) to tolerate these conditions for at least several hours, after which they revive if rewarmed by parents. This paper addresses the physiology of the apneic period. We show that apneic, hypothermic nestlings undergo physiologically important exchanges of gases with the atmosphere. These gas exchanges do not occur across the skin. Instead they occur via the trachea and lungs even though the animals are apneic. Most significantly, when hypothermic neonates are in apnea in ordinary air, they take up O2 steadily from the atmosphere throughout the apneic period, and the evidence available indicates that this O2 uptake is essential for the nestlings' survival. At Tbs of 2-7 °C, the nestlings' rate of O2 consumption varies quasi-exponentially with Tb and averages 0.04 mL O2 g- 1 h- 1, closely similar to the rate expressed by adult mammalian hibernators in hibernation at similar Tbs. Morphometric analysis indicates that, at all focal ages, O2 transport along the full length of the trachea can take place by diffusion at rates adequate to meet the measured rates of metabolic O2 consumption.
{"title":"Apneic uptake of atmospheric O<sub>2</sub> by deeply hypothermic nestlings of the white-footed mouse (Peromyscus leucopus): circulation and lungs.","authors":"Richard W Hill, Jacob J Manteuffel, Bradley A White","doi":"10.1007/s00360-024-01585-x","DOIUrl":"10.1007/s00360-024-01585-x","url":null,"abstract":"<p><p>Nestling white-footed mice (Peromyscus leucopus) are born in the earliest days of spring in cold climates. If the nestlings are by accident exposed to ambient temperatures near freezing (0-7 °C) at early ages (2-10 days old), they may experience body temperatures (T<sub>b</sub>s) equally low. During such hypothermia, although their heart keeps beating, they become apneic (cease inhaling and exhaling). However, they have an exceptional ability (e.g., compared to Mus musculus) to tolerate these conditions for at least several hours, after which they revive if rewarmed by parents. This paper addresses the physiology of the apneic period. We show that apneic, hypothermic nestlings undergo physiologically important exchanges of gases with the atmosphere. These gas exchanges do not occur across the skin. Instead they occur via the trachea and lungs even though the animals are apneic. Most significantly, when hypothermic neonates are in apnea in ordinary air, they take up O<sub>2</sub> steadily from the atmosphere throughout the apneic period, and the evidence available indicates that this O<sub>2</sub> uptake is essential for the nestlings' survival. At T<sub>b</sub>s of 2-7 °C, the nestlings' rate of O<sub>2</sub> consumption varies quasi-exponentially with T<sub>b</sub> and averages 0.04 mL O<sub>2</sub> g<sup>- 1</sup> h<sup>- 1</sup>, closely similar to the rate expressed by adult mammalian hibernators in hibernation at similar T<sub>b</sub>s. Morphometric analysis indicates that, at all focal ages, O<sub>2</sub> transport along the full length of the trachea can take place by diffusion at rates adequate to meet the measured rates of metabolic O<sub>2</sub> consumption.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"123-139"},"PeriodicalIF":1.7,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11839856/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142395561","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}
The combined stresses of fasting and hypoxia are common events during the life history of freshwater fish species. Hypoxia tolerance is vital for survival in aquatic environments, which requires organisms to down-regulate their maintenance energetic expenditure while simultaneously preserving physiological features such as oxygen supply capacity under conditions of food deprivation. Generally, infrequent-feeding species who commonly experience food shortages might evolve more adaptive strategies to cope with food deprivation than frequent-feeding species. Thus, the present study aimed to test whether the response of hypoxia tolerance in fish to short-term fasting (2 weeks) varied with different foraging modes. Fasting resulted in similar decreases in maintenance energetic expenditure and similar decreases in Pcrit and Ploe between fishes with different foraging modes, whereas it resulted in decreased oxygen supply capacity only in frequent-feeding fishes. Furthermore, independent of foraging mode, fasting decreased Pcrit and Ploe in all Cypriniformes and Siluriformes species but not in Perciformes species. The mechanism for decreased Pcrit and Ploe in Cypriniformes and Siluriformes species is at least partially due to the downregulated metabolic demand and/or the maintenance of a high oxygen supply capacity while fasting. The present study found that the effect of fasting on hypoxia tolerance depends upon phylogeny in freshwater fish species. The information acquired in the present study is highly valuable in aquaculture industries and can be used for species conservation in the field.
{"title":"Whether hypoxia tolerance improved after short-term fasting is closely related to phylogeny but not to foraging mode in freshwater fish species.","authors":"Ke-Ren Huang, Qian-Ying Liu, Yong-Fei Zhang, Yu-Lian Luo, Cheng Fu, Xu Pang, Shi-Jian Fu","doi":"10.1007/s00360-024-01588-8","DOIUrl":"10.1007/s00360-024-01588-8","url":null,"abstract":"<p><p>The combined stresses of fasting and hypoxia are common events during the life history of freshwater fish species. Hypoxia tolerance is vital for survival in aquatic environments, which requires organisms to down-regulate their maintenance energetic expenditure while simultaneously preserving physiological features such as oxygen supply capacity under conditions of food deprivation. Generally, infrequent-feeding species who commonly experience food shortages might evolve more adaptive strategies to cope with food deprivation than frequent-feeding species. Thus, the present study aimed to test whether the response of hypoxia tolerance in fish to short-term fasting (2 weeks) varied with different foraging modes. Fasting resulted in similar decreases in maintenance energetic expenditure and similar decreases in P<sub>crit</sub> and P<sub>loe</sub> between fishes with different foraging modes, whereas it resulted in decreased oxygen supply capacity only in frequent-feeding fishes. Furthermore, independent of foraging mode, fasting decreased P<sub>crit</sub> and P<sub>loe</sub> in all Cypriniformes and Siluriformes species but not in Perciformes species. The mechanism for decreased P<sub>crit</sub> and P<sub>loe</sub> in Cypriniformes and Siluriformes species is at least partially due to the downregulated metabolic demand and/or the maintenance of a high oxygen supply capacity while fasting. The present study found that the effect of fasting on hypoxia tolerance depends upon phylogeny in freshwater fish species. The information acquired in the present study is highly valuable in aquaculture industries and can be used for species conservation in the field.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"843-853"},"PeriodicalIF":1.7,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142333104","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 : 2024-12-01Epub Date: 2024-07-31DOI: 10.1007/s00360-024-01577-x
Moises Silvestre de Azevedo Martins, William Franco Carneiro, Kianne Silva Monteiro, Stefania Priscilla de Souza, André Rodrigues da Cunha Barreto Vianna, Luis David Solis Murgas
The present study aimed to establish zebrafish as an experimental model for investigations into obesity and physical exercise, as well as to assess the effects of these factors on metabolism. The experiment spanned twelve weeks, comprising a feeding trial during which the last four weeks incorporated a physical exercise protocol. This protocol involved placing fifteen animals in a five-liter aquarium, where they were subjected to swimming at an approximate speed of 0.08 m/s for 30 min daily. Throughout the experiment, histological analyses of visceral, subcutaneous, and hepatic adipose tissues were conducted, along with biochemical analyses of total cholesterol and its fractions, triglycerides, glucose, lactate, and alanine aminotransferase (ALT) levels. Additionally, oxidative stress markers, such as reactive oxygen species (ROS) levels, superoxide dismutase (SOD) activity, and catalase activity and the formation of thiobarbituric acid-reactive substances, were investigated. The results revealed that the group fed a high-fat diet exhibited an increase in ROS production and SOD activity. In contrast, the group administered the high-fat diet and subjected to physical exercise demonstrated a notable reduction in visceral adipocyte area, hepatic steatosis levels, ALT levels, and SOD activity. These findings indicate that physical exercise has a positive effect on obesity and oxidative stress in zebrafish, providing promising evidence for future investigations in this field.
{"title":"Metabolic effects of physical exercise on zebrafish (Danio rerio) fed a high-fat diet.","authors":"Moises Silvestre de Azevedo Martins, William Franco Carneiro, Kianne Silva Monteiro, Stefania Priscilla de Souza, André Rodrigues da Cunha Barreto Vianna, Luis David Solis Murgas","doi":"10.1007/s00360-024-01577-x","DOIUrl":"10.1007/s00360-024-01577-x","url":null,"abstract":"<p><p>The present study aimed to establish zebrafish as an experimental model for investigations into obesity and physical exercise, as well as to assess the effects of these factors on metabolism. The experiment spanned twelve weeks, comprising a feeding trial during which the last four weeks incorporated a physical exercise protocol. This protocol involved placing fifteen animals in a five-liter aquarium, where they were subjected to swimming at an approximate speed of 0.08 m/s for 30 min daily. Throughout the experiment, histological analyses of visceral, subcutaneous, and hepatic adipose tissues were conducted, along with biochemical analyses of total cholesterol and its fractions, triglycerides, glucose, lactate, and alanine aminotransferase (ALT) levels. Additionally, oxidative stress markers, such as reactive oxygen species (ROS) levels, superoxide dismutase (SOD) activity, and catalase activity and the formation of thiobarbituric acid-reactive substances, were investigated. The results revealed that the group fed a high-fat diet exhibited an increase in ROS production and SOD activity. In contrast, the group administered the high-fat diet and subjected to physical exercise demonstrated a notable reduction in visceral adipocyte area, hepatic steatosis levels, ALT levels, and SOD activity. These findings indicate that physical exercise has a positive effect on obesity and oxidative stress in zebrafish, providing promising evidence for future investigations in this field.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"793-804"},"PeriodicalIF":1.7,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141861800","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 : 2024-12-01Epub Date: 2024-07-17DOI: 10.1007/s00360-024-01576-y
Matthias Nemeth, Susanna Fritscher, Klara Füreder, Bernard Wallner, Eva Millesi
An individual's energetic demands and hence metabolic rate can strongly change during adolescence, a phase characterized by profound morphological, physiological, and endocrine changes. Glucocorticoid hormones (e.g. cortisol) are released in response to hypothalamic-pituitary-adrenal-axis activity, modulate several metabolic processes, and can also be linked to increased metabolic rate. In domestic guinea pigs (Cavia aperea f. porcellus) housed in same-sex groups, cortisol concentrations increase during adolescence in males but remain stable in females, which was suggested to be related to different energetic demands by age. We therefore measured metabolic rate through oxygen (O2) consumption over 2.5 h in male and female guinea pigs housed in same-sex groups during adolescence at ages of 60, 120, and 180 days, which was paralleled by analyses of saliva cortisol concentrations before and after the measurement. The statistical analyses involved whole body metabolic rate (ml O2/h), body mass-corrected metabolic rate (ml O2/h/kg), and body mass-independent metabolic rate (ml O2/h statistically corrected for body mass). We found increasing cortisol concentrations with age in males only, but none of the three metabolic rate analyses revealed a sex difference by age. On the individual level, repeatability across ages was found in metabolic rate as well as in body mass and cortisol concentrations after the measurement, but not in "basal" cortisol concentrations. Our results suggest no sex-specific changes in metabolic rate and hence equal energetic demands in male and female guinea pigs during adolescence. Moreover, metabolic rate clearly represents a highly stable physiological trait already early in a guinea pig's life irrespective of rather fluctuating cortisol concentrations.
青春期是一个以形态、生理和内分泌的深刻变化为特征的阶段,在此期间,个体的能量需求和新陈代谢率会发生强烈变化。糖皮质激素(如皮质醇)会随着下丘脑-垂体-肾上腺轴的活动而释放,调节多个新陈代谢过程,也可能与新陈代谢率的增加有关。在同性饲养的家养豚鼠(Cavia aperea f. porcellus)中,雄性豚鼠的皮质醇浓度在青春期会增加,而雌性豚鼠的皮质醇浓度则保持稳定。因此,我们测量了同性饲养的雄性和雌性豚鼠在青春期60天、120天和180天2.5小时的氧气(O2)消耗代谢率,同时分析了测量前后唾液中皮质醇的浓度。统计分析涉及全身代谢率(毫升 O2/小时)、体重校正代谢率(毫升 O2/小时/千克)和与体重无关的代谢率(根据体重统计校正的毫升 O2/小时)。我们发现只有男性的皮质醇浓度随着年龄的增长而增加,但三种代谢率分析均未显示出年龄上的性别差异。就个体而言,新陈代谢率、体重和测量后皮质醇浓度在不同年龄段具有可重复性,但 "基础 "皮质醇浓度不具有可重复性。我们的研究结果表明,雌雄豚鼠的代谢率没有性别差异,因此在青春期对能量的需求相同。此外,无论皮质醇浓度如何波动,代谢率显然是豚鼠生命早期的一个高度稳定的生理特征。
{"title":"Metabolic rate and saliva cortisol concentrations in socially housed adolescent guinea pigs.","authors":"Matthias Nemeth, Susanna Fritscher, Klara Füreder, Bernard Wallner, Eva Millesi","doi":"10.1007/s00360-024-01576-y","DOIUrl":"10.1007/s00360-024-01576-y","url":null,"abstract":"<p><p>An individual's energetic demands and hence metabolic rate can strongly change during adolescence, a phase characterized by profound morphological, physiological, and endocrine changes. Glucocorticoid hormones (e.g. cortisol) are released in response to hypothalamic-pituitary-adrenal-axis activity, modulate several metabolic processes, and can also be linked to increased metabolic rate. In domestic guinea pigs (Cavia aperea f. porcellus) housed in same-sex groups, cortisol concentrations increase during adolescence in males but remain stable in females, which was suggested to be related to different energetic demands by age. We therefore measured metabolic rate through oxygen (O<sub>2</sub>) consumption over 2.5 h in male and female guinea pigs housed in same-sex groups during adolescence at ages of 60, 120, and 180 days, which was paralleled by analyses of saliva cortisol concentrations before and after the measurement. The statistical analyses involved whole body metabolic rate (ml O<sub>2</sub>/h), body mass-corrected metabolic rate (ml O<sub>2</sub>/h/kg), and body mass-independent metabolic rate (ml O<sub>2</sub>/h statistically corrected for body mass). We found increasing cortisol concentrations with age in males only, but none of the three metabolic rate analyses revealed a sex difference by age. On the individual level, repeatability across ages was found in metabolic rate as well as in body mass and cortisol concentrations after the measurement, but not in \"basal\" cortisol concentrations. Our results suggest no sex-specific changes in metabolic rate and hence equal energetic demands in male and female guinea pigs during adolescence. Moreover, metabolic rate clearly represents a highly stable physiological trait already early in a guinea pig's life irrespective of rather fluctuating cortisol concentrations.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"925-933"},"PeriodicalIF":1.7,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11511739/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141629379","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 : 2024-12-01Epub Date: 2024-07-12DOI: 10.1007/s00360-024-01572-2
Ana Gabriela Jiménez, Chelsi Marolf, David L Swanson
With climate change increasing not just mean temperatures but the frequency of cold snaps and heat waves, animals occupying thermally variable areas may be faced with thermal conditions for which they are not prepared. Studies of physiological adaptations of temperate resident birds to such thermal variability are largely lacking in the literature. To address this gap, we acclimated winter-phenotype house sparrows (Passer domesticus) to stable warm, stable cold, and fluctuating cold temperatures. We then measured several metrics of the oxidative stress (OS) system, including enzymatic and non-enzymatic antioxidants and lipid oxidative damage, in brain (post-mitotic), kidney (mitotic), liver (mitotic) and pectoralis muscle (post-mitotic). We predicted that high metabolic flexibility could be linked to increases in reactive oxygen damage. Alternatively, if variation in ROS production is not associated with metabolic flexibility, then we predict no antioxidant compensation with thermal variation. Our data suggest that ROS production is not associated with metabolic flexibility, as we found no differences across thermal treatment groups. However, we did find differences across tissues. Brain catalase activity demonstrated the lowest values compared with kidney, liver and muscle. In contrast, brain glutathione peroxidase (GPx) activities were higher than those in kidney and liver. Muscle GPx activities were intermediate to brain and kidney/liver. Lipid peroxidation damage was lowest in the kidney and highest in muscle tissue.
{"title":"Oxidative stress across multiple tissues in house sparrows (Passer domesticus) acclimated to warm, stable cold, and unpredictable cold thermal treatments.","authors":"Ana Gabriela Jiménez, Chelsi Marolf, David L Swanson","doi":"10.1007/s00360-024-01572-2","DOIUrl":"10.1007/s00360-024-01572-2","url":null,"abstract":"<p><p>With climate change increasing not just mean temperatures but the frequency of cold snaps and heat waves, animals occupying thermally variable areas may be faced with thermal conditions for which they are not prepared. Studies of physiological adaptations of temperate resident birds to such thermal variability are largely lacking in the literature. To address this gap, we acclimated winter-phenotype house sparrows (Passer domesticus) to stable warm, stable cold, and fluctuating cold temperatures. We then measured several metrics of the oxidative stress (OS) system, including enzymatic and non-enzymatic antioxidants and lipid oxidative damage, in brain (post-mitotic), kidney (mitotic), liver (mitotic) and pectoralis muscle (post-mitotic). We predicted that high metabolic flexibility could be linked to increases in reactive oxygen damage. Alternatively, if variation in ROS production is not associated with metabolic flexibility, then we predict no antioxidant compensation with thermal variation. Our data suggest that ROS production is not associated with metabolic flexibility, as we found no differences across thermal treatment groups. However, we did find differences across tissues. Brain catalase activity demonstrated the lowest values compared with kidney, liver and muscle. In contrast, brain glutathione peroxidase (GPx) activities were higher than those in kidney and liver. Muscle GPx activities were intermediate to brain and kidney/liver. Lipid peroxidation damage was lowest in the kidney and highest in muscle tissue.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"899-907"},"PeriodicalIF":1.6,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141592240","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 : 2024-12-01Epub Date: 2024-09-09DOI: 10.1007/s00360-024-01580-2
Carolyn Morris, Camila Martins, Samantha Zulian, D Scott Smith, Colin J Brauner, Chris M Wood
Many flatfish species are partially euryhaline, such as the Pacific sanddab which spawn and feed in highly dynamic estuaries ranging from seawater to near freshwater. With the rapid increase in saltwater invasion of freshwater habitats, it is very likely that in these estuaries, flatfish will be exposed to increasing levels of dissolved organic carbon (DOC) of freshwater origin at a range of salinities. As salinity fluctuations often coincide with changes in DOC concentration, two natural freshwater DOCs [Luther Marsh (LM, allochthonous) and Lake Ontario (LO, autochthonous) were investigated at salinities of 30 and 7.5 ppt. Optical characterization of the two natural DOC sources indicate salinity-dependent differences in their physicochemistry. LO and LM DOCs, as well as three model compounds [tannic acid (TA), sodium dodecyl sulfate (SDS) and bovine serum albumin (BSA)] representing key chemical moieties of DOC, were used to evaluate physiological effects on sanddabs. In the absence of added DOC, an acute decrease in salinity resulted in an increase in diffusive water flux (a proxy for transcellular water permeability), ammonia excretion and a change in TEP from positive (inside) to negative (inside). The effects of DOC (10 mg C L-1) were salinity and source-dependent, with generally more pronounced effects at 30 than 7.5 ppt, and greater potency of LM relative to LO. Both LM DOC and SDS increased diffusive water flux at 30 ppt but only SDS had an effect at 7.5 ppt. TA decreased ammonia excretion at 7.5 ppt. LO DOC decreased urea-N excretion at both salinities whereas the stimulatory effect of BSA occurred only at 30 ppt. Likewise, the effects of LM DOC and BSA to reduce TEP were present at 30 ppt but not 7.5 ppt. None of the treatments affected oxygen consumption rates. Our results demonstrate that DOCs and salinity interact to alter key physiological processes in marine flatfish, reflecting changes in both gill function and the physicochemistry of DOCs between 30 and 7.5 ppt.
{"title":"The effects of dissolved organic carbon and model compounds (DOC analogues) on diffusive water flux, oxygen consumption, nitrogenous waste excretion rates and gill transepithelial potential in Pacific sanddab (Citharichthys sordidus) at two salinities.","authors":"Carolyn Morris, Camila Martins, Samantha Zulian, D Scott Smith, Colin J Brauner, Chris M Wood","doi":"10.1007/s00360-024-01580-2","DOIUrl":"10.1007/s00360-024-01580-2","url":null,"abstract":"<p><p>Many flatfish species are partially euryhaline, such as the Pacific sanddab which spawn and feed in highly dynamic estuaries ranging from seawater to near freshwater. With the rapid increase in saltwater invasion of freshwater habitats, it is very likely that in these estuaries, flatfish will be exposed to increasing levels of dissolved organic carbon (DOC) of freshwater origin at a range of salinities. As salinity fluctuations often coincide with changes in DOC concentration, two natural freshwater DOCs [Luther Marsh (LM, allochthonous) and Lake Ontario (LO, autochthonous) were investigated at salinities of 30 and 7.5 ppt. Optical characterization of the two natural DOC sources indicate salinity-dependent differences in their physicochemistry. LO and LM DOCs, as well as three model compounds [tannic acid (TA), sodium dodecyl sulfate (SDS) and bovine serum albumin (BSA)] representing key chemical moieties of DOC, were used to evaluate physiological effects on sanddabs. In the absence of added DOC, an acute decrease in salinity resulted in an increase in diffusive water flux (a proxy for transcellular water permeability), ammonia excretion and a change in TEP from positive (inside) to negative (inside). The effects of DOC (10 mg C L<sup>-1</sup>) were salinity and source-dependent, with generally more pronounced effects at 30 than 7.5 ppt, and greater potency of LM relative to LO. Both LM DOC and SDS increased diffusive water flux at 30 ppt but only SDS had an effect at 7.5 ppt. TA decreased ammonia excretion at 7.5 ppt. LO DOC decreased urea-N excretion at both salinities whereas the stimulatory effect of BSA occurred only at 30 ppt. Likewise, the effects of LM DOC and BSA to reduce TEP were present at 30 ppt but not 7.5 ppt. None of the treatments affected oxygen consumption rates. Our results demonstrate that DOCs and salinity interact to alter key physiological processes in marine flatfish, reflecting changes in both gill function and the physicochemistry of DOCs between 30 and 7.5 ppt.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"805-825"},"PeriodicalIF":1.7,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142156767","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 : 2024-12-01Epub Date: 2024-09-05DOI: 10.1007/s00360-024-01579-9
Julita Sadowska, Karen M Carlson, C Loren Buck, Trixie N Lee, Khrystyne N Duddleston
Energy conservation associated with hibernation is maximized at the intersection of low body temperature (Tb), long torpor bouts, and few interbout arousals. In the arctic ground squirrel (Urocitellus parryii), energy conservation during hibernation is best achieved at ambient temperatures (Ta) around 0 °C; however, they spend the majority of hibernation at considerably lower Ta. Because arctic ground squirrels switch to mixed fuel metabolism, including protein catabolism, at extreme low Ta of hibernation, we sought to investigate how microbial urea-nitrogen recycling is used under different thermal conditions. Injecting squirrels with isotopically labeled urea (13C/15N) during hibernation at Ta's of - 16 °C and 2 °C and while active and euthermic allowed us to assess the ureolytic activity of gut microbes and the amount of liberated nitrogen incorporated into tissues. We found greater incorporation of microbially-liberated nitrogen into tissues of hibernating squirrels. Although ureolytic activity appears higher in euthermic squirrels, liberated nitrogen likely makes up a smaller percentage of the available nitrogen pool in active, fed animals. Because non-lipid fuel is a limiting factor for torpor at lower Ta in this species, we hypothesized there would be greater incorporation of liberated nitrogen in animals hibernating at - 16 °C. However, we found higher microbial-ureolytic activity and incorporation of microbially-liberated nitrogen, particularly in the liver, in squirrels hibernating at 2 °C. Likely this is because squirrels hibernating at 2 °C had higher Tb and longer interbout arousals, a combination of factors creating more favorable conditions for gut microbes to thrive and maintain greater activity while giving the host more time to absorb microbial metabolites.
{"title":"Microbial urea-nitrogen recycling in arctic ground squirrels: the effect of ambient temperature of hibernation.","authors":"Julita Sadowska, Karen M Carlson, C Loren Buck, Trixie N Lee, Khrystyne N Duddleston","doi":"10.1007/s00360-024-01579-9","DOIUrl":"10.1007/s00360-024-01579-9","url":null,"abstract":"<p><p>Energy conservation associated with hibernation is maximized at the intersection of low body temperature (T<sub>b</sub>), long torpor bouts, and few interbout arousals. In the arctic ground squirrel (Urocitellus parryii), energy conservation during hibernation is best achieved at ambient temperatures (T<sub>a</sub>) around 0 °C; however, they spend the majority of hibernation at considerably lower T<sub>a</sub>. Because arctic ground squirrels switch to mixed fuel metabolism, including protein catabolism, at extreme low T<sub>a</sub> of hibernation, we sought to investigate how microbial urea-nitrogen recycling is used under different thermal conditions. Injecting squirrels with isotopically labeled urea (<sup>13</sup>C/<sup>15</sup>N) during hibernation at T<sub>a</sub>'s of - 16 °C and 2 °C and while active and euthermic allowed us to assess the ureolytic activity of gut microbes and the amount of liberated nitrogen incorporated into tissues. We found greater incorporation of microbially-liberated nitrogen into tissues of hibernating squirrels. Although ureolytic activity appears higher in euthermic squirrels, liberated nitrogen likely makes up a smaller percentage of the available nitrogen pool in active, fed animals. Because non-lipid fuel is a limiting factor for torpor at lower T<sub>a</sub> in this species, we hypothesized there would be greater incorporation of liberated nitrogen in animals hibernating at - 16 °C. However, we found higher microbial-ureolytic activity and incorporation of microbially-liberated nitrogen, particularly in the liver, in squirrels hibernating at 2 °C. Likely this is because squirrels hibernating at 2 °C had higher T<sub>b</sub> and longer interbout arousals, a combination of factors creating more favorable conditions for gut microbes to thrive and maintain greater activity while giving the host more time to absorb microbial metabolites.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"909-924"},"PeriodicalIF":1.7,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11511772/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142141828","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 : 2024-12-01Epub Date: 2024-08-19DOI: 10.1007/s00360-024-01578-w
Fazul Nabi, Muhammad Asif Arain, Mohammad Farooque Hassan, Qurban Ali Shah, Mikhlid H Almutairi, Jameel Ahmed Buzdar
The current research was conducted to assess the effect of in ovo feeding (IOF) of selenium (Se) and zinc (Zn) on hatchability, production performance, liver, intestinal morphology, antioxidant levels and expression levels of immune-related genes in broiler chickens. A total of 400 fertilized eggs were equally divided into four groups: control (non-injected), sham (in ovo injection of 0.75% NaCl), Se (@ 1.5 µg/egg in ovo injection) and Zn (500 µg/egg in ovo injection) groups respectively. On the seventeenth day of incubation, treatment solutions were administered into amniotic fluid of fertilized eggs. The results revealed that Se and Zn supplementation significantly (P < 0.05) enhanced hatchability, post-hatch growth, organ development, and liver antioxidant capability. Histopathological examination revealed a typical hepatocyte morphology, well-arranged cells, and a significant (P < 0.05) decrease in apoptosis in both selenium and zinc groups. Additionally, selenium and zinc produced auspicious effects on intestinal epithelium and villi surface area. Interestingly, our results revealed that IOF of Se and Zn modulated the expression of immune-related genes in comparison to the control and sham groups. Conclusively, IOF of Se and Zn augmented health and productivity by enhancing the cellular immunity in the broiler chickens, thus IOF can be utilized as an effective strategy to promote health and immunity in broiler chickens.
{"title":"Effects of in ovo supplementation of selenium (Se) and zinc (zn) on hatchability and production performance of broiler chickens.","authors":"Fazul Nabi, Muhammad Asif Arain, Mohammad Farooque Hassan, Qurban Ali Shah, Mikhlid H Almutairi, Jameel Ahmed Buzdar","doi":"10.1007/s00360-024-01578-w","DOIUrl":"10.1007/s00360-024-01578-w","url":null,"abstract":"<p><p>The current research was conducted to assess the effect of in ovo feeding (IOF) of selenium (Se) and zinc (Zn) on hatchability, production performance, liver, intestinal morphology, antioxidant levels and expression levels of immune-related genes in broiler chickens. A total of 400 fertilized eggs were equally divided into four groups: control (non-injected), sham (in ovo injection of 0.75% NaCl), Se (@ 1.5 µg/egg in ovo injection) and Zn (500 µg/egg in ovo injection) groups respectively. On the seventeenth day of incubation, treatment solutions were administered into amniotic fluid of fertilized eggs. The results revealed that Se and Zn supplementation significantly (P < 0.05) enhanced hatchability, post-hatch growth, organ development, and liver antioxidant capability. Histopathological examination revealed a typical hepatocyte morphology, well-arranged cells, and a significant (P < 0.05) decrease in apoptosis in both selenium and zinc groups. Additionally, selenium and zinc produced auspicious effects on intestinal epithelium and villi surface area. Interestingly, our results revealed that IOF of Se and Zn modulated the expression of immune-related genes in comparison to the control and sham groups. Conclusively, IOF of Se and Zn augmented health and productivity by enhancing the cellular immunity in the broiler chickens, thus IOF can be utilized as an effective strategy to promote health and immunity in broiler chickens.</p>","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"887-897"},"PeriodicalIF":1.7,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142001448","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 : 2024-12-01Epub Date: 2024-10-07DOI: 10.1007/s00360-024-01587-9
Claudia Silva Rubio, Anne B Kim, William K Milsom, Matthew E Pamenter, Gilbecca Rae Smith, Frank van Breukelen
<p><p>Common tenrecs (Tenrec ecaudatus) are fossorial mammals that use burrows during both active and hibernating seasons in Madagascar and its neighboring islands. Prevailing thought was that tenrecs hibernate for 8-9 months individually, but 13 tenrecs were removed from the same sealed burrow 1 m deep from the surface. Such group hibernation in sealed burrows presumably creates a hypoxic and/or hypercapnic environment and suggests that this placental mammal may have an increased tolerance to hypoxia and hypercapnia. Higher tolerances to hypoxia and hypercapnia have been documented for other mammals capable of hibernation and to determine if this is the case for tenrecs, we exposed them to acute hypoxia (4 h of 16 or 7% O<sub>2</sub>), progressive hypoxia (2 h of 16, 10 and 4% O<sub>2</sub>), or progressive hypercapnia (2 h of 2, 5 and 10% CO<sub>2</sub>) at cold (16 °C) or warm (28 °C) ambient temperatures (T<sub>a</sub>). Oxygen equilibrium curves were also constructed on the whole blood of tenrecs at 10, 25, and 37 °C to determine if hemoglobin (Hb)-O<sub>2</sub> affinity contributes to hypoxia tolerance. In animals held at 16 °C, normoxic and normocapnic levels of oxygen consumption rate ( <math> <msub> <mrow><mover><mtext>V</mtext> <mo>˙</mo></mover> <mtext>O</mtext></mrow> <mn>2</mn></msub> </math> ), body temperature (T<sub>b</sub>), and heart rate (HR) were highly variable between individuals. This inter-individual variation was greatly reduced in animals held at 28 °C for oxygen consumption rate and body temperature. Both hypoxia (acute and progressive) and progressive hypercapnia led to decreases in <math> <msub> <mrow><mover><mtext>V</mtext> <mo>˙</mo></mover> <mtext>O</mtext></mrow> <mn>2</mn></msub> </math> as well as the variation in <math> <msub> <mrow><mover><mtext>V</mtext> <mo>˙</mo></mover> <mtext>O</mtext></mrow> <mn>2</mn></msub> </math> between animals held at 16 °C. The fall in oxygen consumption rate in 7% O<sub>2</sub> independent of changes in body temperature in tenrecs held at 16 °C is unique and not consistent with the typical hypoxic metabolic response seen in other hibernating species that depends on concomitant falls in T<sub>b</sub>. In animals held at 28 °C, exposure to O<sub>2</sub> levels as low as 4% and CO<sub>2</sub> levels as high as 10% had no significant effect on <math> <msub> <mrow><mover><mtext>V</mtext> <mo>˙</mo></mover> <mtext>O</mtext></mrow> <mn>2</mn></msub> </math> , HR, or T<sub>b</sub>, indicative of high tolerance to both hypoxia and hypercapnia. High variation in heart rate remained between individuals in all gas compositions and at all temperatures. Tenrec Hb-O<sub>2</sub> affinity was similar to other homeothermic placental mammals and likely does not contribute to the increased hypoxia tolerance. Ultimately, our results suggest changes in T<sub>a</sub> dictate physiological responses to hypoxia or hypercapnia in tenrecs, responses more characteristic of reptiles than of most placental ma
普通箭猪(Tenrec ecaudatus)是一种穴居哺乳动物,在马达加斯加及其邻近岛屿的活动和冬眠季节都使用洞穴。人们普遍认为恬莱鼠的个体冬眠期为 8-9 个月,但我们从距离地表 1 米深的同一密封洞穴中取出了 13 只恬莱鼠。这种在密封洞穴中的集体冬眠可能会造成缺氧和/或高碳酸环境,并表明这种有胎盘的哺乳动物可能对缺氧和高碳酸环境的耐受性更强。为了确定天牛的情况是否如此,我们让天牛在低温(16 °C)或高温(28 °C)环境下(Ta)暴露于急性缺氧(4 小时 16% 或 7% 的氧气)、渐进性缺氧(2 小时 16%、10% 和 4% 的氧气)或渐进性高碳酸血症(2 小时 2%、5% 和 10% 的二氧化碳)。此外,还在 10、25 和 37 °C条件下构建了腱鱼全血的氧平衡曲线,以确定血红蛋白(Hb)-O2 亲和力是否有助于耐缺氧性。在 16 °C的动物中,正常缺氧和正常碳酸血症水平下的耗氧率(V ˙ O 2)、体温(Tb)和心率(HR)在个体间存在很大差异。在 28 °C条件下,动物耗氧量和体温的个体间差异大大降低。缺氧(急性和进行性)和进行性高碳酸血症都会导致 V ˙ O 2 的下降,以及在 16 °C条件下动物之间 V ˙ O 2 的差异。在 7% O2 条件下,16 °C条件下滇金丝猴的耗氧率下降与体温变化无关,这种情况是独特的,与其他冬眠物种典型的缺氧代谢反应(取决于 Tb 的同时下降)不一致。在 28 °C下的动物,暴露于低至 4% 的氧气水平和高至 10% 的二氧化碳水平对 V ˙ O 2、心率或 Tb 没有显著影响,这表明它们对缺氧和高碳酸血症都有很高的耐受性。在所有气体成分和温度条件下,不同个体之间的心率仍存在很大差异。Tenrec的Hb-O2亲和力与其他胎盘哺乳动物相似,可能不会导致缺氧耐受性的提高。最终,我们的研究结果表明,Ta的变化决定了tenrecs对低氧或高碳酸血症的生理反应,这种反应是爬行动物的特征,而不是大多数胎盘哺乳动物的特征。鉴于鼩鼱的许多解剖学和生理学特征表明它们可能是祖先胎盘哺乳动物的代表,我们的研究结果表明典型的低氧代谢反应是在哺乳动物进化的后期演化而来的。
{"title":"Common tenrecs (Tenrec ecaudatus) reduce oxygen consumption in hypoxia and in hypercapnia without concordant changes to body temperature or heart rate.","authors":"Claudia Silva Rubio, Anne B Kim, William K Milsom, Matthew E Pamenter, Gilbecca Rae Smith, Frank van Breukelen","doi":"10.1007/s00360-024-01587-9","DOIUrl":"10.1007/s00360-024-01587-9","url":null,"abstract":"<p><p>Common tenrecs (Tenrec ecaudatus) are fossorial mammals that use burrows during both active and hibernating seasons in Madagascar and its neighboring islands. Prevailing thought was that tenrecs hibernate for 8-9 months individually, but 13 tenrecs were removed from the same sealed burrow 1 m deep from the surface. Such group hibernation in sealed burrows presumably creates a hypoxic and/or hypercapnic environment and suggests that this placental mammal may have an increased tolerance to hypoxia and hypercapnia. Higher tolerances to hypoxia and hypercapnia have been documented for other mammals capable of hibernation and to determine if this is the case for tenrecs, we exposed them to acute hypoxia (4 h of 16 or 7% O<sub>2</sub>), progressive hypoxia (2 h of 16, 10 and 4% O<sub>2</sub>), or progressive hypercapnia (2 h of 2, 5 and 10% CO<sub>2</sub>) at cold (16 °C) or warm (28 °C) ambient temperatures (T<sub>a</sub>). Oxygen equilibrium curves were also constructed on the whole blood of tenrecs at 10, 25, and 37 °C to determine if hemoglobin (Hb)-O<sub>2</sub> affinity contributes to hypoxia tolerance. In animals held at 16 °C, normoxic and normocapnic levels of oxygen consumption rate ( <math> <msub> <mrow><mover><mtext>V</mtext> <mo>˙</mo></mover> <mtext>O</mtext></mrow> <mn>2</mn></msub> </math> ), body temperature (T<sub>b</sub>), and heart rate (HR) were highly variable between individuals. This inter-individual variation was greatly reduced in animals held at 28 °C for oxygen consumption rate and body temperature. Both hypoxia (acute and progressive) and progressive hypercapnia led to decreases in <math> <msub> <mrow><mover><mtext>V</mtext> <mo>˙</mo></mover> <mtext>O</mtext></mrow> <mn>2</mn></msub> </math> as well as the variation in <math> <msub> <mrow><mover><mtext>V</mtext> <mo>˙</mo></mover> <mtext>O</mtext></mrow> <mn>2</mn></msub> </math> between animals held at 16 °C. The fall in oxygen consumption rate in 7% O<sub>2</sub> independent of changes in body temperature in tenrecs held at 16 °C is unique and not consistent with the typical hypoxic metabolic response seen in other hibernating species that depends on concomitant falls in T<sub>b</sub>. In animals held at 28 °C, exposure to O<sub>2</sub> levels as low as 4% and CO<sub>2</sub> levels as high as 10% had no significant effect on <math> <msub> <mrow><mover><mtext>V</mtext> <mo>˙</mo></mover> <mtext>O</mtext></mrow> <mn>2</mn></msub> </math> , HR, or T<sub>b</sub>, indicative of high tolerance to both hypoxia and hypercapnia. High variation in heart rate remained between individuals in all gas compositions and at all temperatures. Tenrec Hb-O<sub>2</sub> affinity was similar to other homeothermic placental mammals and likely does not contribute to the increased hypoxia tolerance. Ultimately, our results suggest changes in T<sub>a</sub> dictate physiological responses to hypoxia or hypercapnia in tenrecs, responses more characteristic of reptiles than of most placental ma","PeriodicalId":56033,"journal":{"name":"Journal of Comparative Physiology B-Biochemical Systems and Environmental Physiology","volume":" ","pages":"869-885"},"PeriodicalIF":1.7,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142382474","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}