AbstractThe Xizang plateau frog, Nanorana parkeri (Anura: Dicroglossidae), enters a dormant state in the winter in response to seasonal cold and lack of food. To investigate the physiological and ecological characteristics of overwintering in this species, we measured habitat conditions (hibernacula temperatures, body temperature, and water quality variables), morphology, metabolite concentrations, total antioxidant capacity (T-AOC), and bacteria-killing ability (BKA) of plasma during summer and winter. We found that N. parkeri hibernates underwater at the bottom of ponds (10-20-cm depth). Dissolved oxygen content in the water decreases significantly (by 12%) in the winter compared with summer, suggesting that overwintering N. parkeri may experience hypoxia. Body mass, body mass index, hepatosomatic index, and hepatic glycogen concentration all increased significantly in winter-collected frogs as compared to summer-collected individuals, indicating that overwintering N. parkeri accumulates high fuel/energy reserves to support prolonged periods of hibernation. A significant reduction in glucose, urea, and lactate concentrations in most organs may be closely related to metabolic depression in overwintering N. parkeri. Liver lactate concentration rose significantly in winter-collected frogs, suggesting that anaerobic metabolism dominates when this species overwinters. The T-AOC of plasma showed a significant reduction in winter, suggesting a reduced need for antioxidant defenses. Oppositely, the BKA of plasma increased significantly in winter versus summer, indicating that innate immunity was enhanced during overwintering. In summary, these behavioral (migrating to caves), physiological, and biochemical adjustments may be key for the successful overwintering of this high-altitude frog.
{"title":"Physiological Ecology of Winter Hibernation by the High-Altitude Frog <i>Nanorana parkeri</i>.","authors":"Yonggang Niu, Qiang Chen, Kenneth B Storey, Linhong Teng, Xiangyong Li, Tisen Xu, Haiying Zhang","doi":"10.1086/718764","DOIUrl":"https://doi.org/10.1086/718764","url":null,"abstract":"<p><p>AbstractThe Xizang plateau frog, <i>Nanorana parkeri</i> (Anura: Dicroglossidae), enters a dormant state in the winter in response to seasonal cold and lack of food. To investigate the physiological and ecological characteristics of overwintering in this species, we measured habitat conditions (hibernacula temperatures, body temperature, and water quality variables), morphology, metabolite concentrations, total antioxidant capacity (T-AOC), and bacteria-killing ability (BKA) of plasma during summer and winter. We found that <i>N. parkeri</i> hibernates underwater at the bottom of ponds (10-20-cm depth). Dissolved oxygen content in the water decreases significantly (by 12%) in the winter compared with summer, suggesting that overwintering <i>N. parkeri</i> may experience hypoxia. Body mass, body mass index, hepatosomatic index, and hepatic glycogen concentration all increased significantly in winter-collected frogs as compared to summer-collected individuals, indicating that overwintering <i>N. parkeri</i> accumulates high fuel/energy reserves to support prolonged periods of hibernation. A significant reduction in glucose, urea, and lactate concentrations in most organs may be closely related to metabolic depression in overwintering <i>N. parkeri</i>. Liver lactate concentration rose significantly in winter-collected frogs, suggesting that anaerobic metabolism dominates when this species overwinters. The T-AOC of plasma showed a significant reduction in winter, suggesting a reduced need for antioxidant defenses. Oppositely, the BKA of plasma increased significantly in winter versus summer, indicating that innate immunity was enhanced during overwintering. In summary, these behavioral (migrating to caves), physiological, and biochemical adjustments may be key for the successful overwintering of this high-altitude frog.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 3","pages":"201-211"},"PeriodicalIF":1.6,"publicationDate":"2022-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39807923","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}
A. R. Yilmaz, Adrianna Yoder, S. Diamond, R. Martin
The effects of chronic thermal stress during development on thermal performance traits are not well characterized under urban heat islands, despite these conditions being biologically relevant for how organisms experience the urban environment and the often strong linkages between thermal performance traits and fitness. Here we use the terrestrial isopod Oniscus asellus to examine the effects of chronic thermal stress during development on voluntary running speed of urban and rural isopods. We used a laboratory common-garden experiment design with two developmental acclimation temperature treatments (21°C, a benign treatment, and 29°C, a stressful treatment) and three test temperatures (19°C, 31°C, 40°C); we tested running speed of individuals from urban and rural populations under each of the temperature combinations. We found that for both urban and rural isopods, running speed across three test temperatures was reduced under developmental acclimation conditions of 29°C compared with 21°C. Importantly, however, urban isopods had a running speed advantage over the rural isopods under the 29°C developmental acclimation conditions at the lower two test temperatures. No population differences were detected under benign developmental acclimation conditions of 21°C. The evolution of higher heat tolerance in urban isopods further supported the interpretation of adaptation to heat stress. Convergence of urban and rural isopod running speed at the highest test temperature, however, suggests potential limits or constraints on adaptation. Our results indicate that thermal adaptation to urban heat islands can mitigate negative effects of chronic developmental thermal stress, even when overall performance is reduced compared with benign conditions.
{"title":"Adaptation to Urban Heat Islands Enhances Thermal Performance Following Development under Chronic Thermal Stress but Not Benign Conditions in the Terrestrial Isopod Oniscus asellus","authors":"A. R. Yilmaz, Adrianna Yoder, S. Diamond, R. Martin","doi":"10.1086/720333","DOIUrl":"https://doi.org/10.1086/720333","url":null,"abstract":"The effects of chronic thermal stress during development on thermal performance traits are not well characterized under urban heat islands, despite these conditions being biologically relevant for how organisms experience the urban environment and the often strong linkages between thermal performance traits and fitness. Here we use the terrestrial isopod Oniscus asellus to examine the effects of chronic thermal stress during development on voluntary running speed of urban and rural isopods. We used a laboratory common-garden experiment design with two developmental acclimation temperature treatments (21°C, a benign treatment, and 29°C, a stressful treatment) and three test temperatures (19°C, 31°C, 40°C); we tested running speed of individuals from urban and rural populations under each of the temperature combinations. We found that for both urban and rural isopods, running speed across three test temperatures was reduced under developmental acclimation conditions of 29°C compared with 21°C. Importantly, however, urban isopods had a running speed advantage over the rural isopods under the 29°C developmental acclimation conditions at the lower two test temperatures. No population differences were detected under benign developmental acclimation conditions of 21°C. The evolution of higher heat tolerance in urban isopods further supported the interpretation of adaptation to heat stress. Convergence of urban and rural isopod running speed at the highest test temperature, however, suggests potential limits or constraints on adaptation. Our results indicate that thermal adaptation to urban heat islands can mitigate negative effects of chronic developmental thermal stress, even when overall performance is reduced compared with benign conditions.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"302 - 316"},"PeriodicalIF":1.6,"publicationDate":"2022-04-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"44023438","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}
Antonio Brun, Yocelyn T. Gutiérrez-Guerrero, Melisa E. Magallanes, E. Caviedes-Vidal, W. Karasov, C. Martinez del Rio
Trehalose is a nonreducing disaccharide that is a primary storage and energy source in prokaryotes, yeasts, fungi, and invertebrates. Vertebrates digest trehalose with the intestinal brush border membrane (BBM) enzyme trehalase. Intestinal trehalase activity is reported to be either very low or absent in several bird species. We assayed trehalase activity in 19 avian species, used proteomic analysis to quantify its abundance in the intestinal BBM, and used analyses of available genomes to detect the presence of the gene that codes for trehalase (Treh). We found no intestinal trehalase activity in birds, trehalase was absent from the proteome of their intestinal BBM, and the gene coding for trehalase was absent in their genomes. Surveys of available transcriptomes support the hypothesis that Treh is absent in birds. The trehalase gene was found in the same conserved syntenic block within the genome of all vertebrates surveyed except birds. Our analysis suggests that Treh was lost in an inversion followed by a reinsertion of a large gene block. This event appears to have taken place after the split between crocodiles and birds and dinosaurs. Birds are unable to digest a common dietary sugar like trehalose because their ancestor lost the trehalase gene. The loss of this gene seems to represent an ecological cost, as insectivorous birds seem to be unable to digest a carbohydrate present in their prey. We also speculate that the paucity of mycophagy in birds is due to the presence of large amounts of this sugar in fungal tissues.
{"title":"Opportunities Lost? Evolutionary Causes and Ecological Consequences of the Absence of Trehalose Digestion in Birds","authors":"Antonio Brun, Yocelyn T. Gutiérrez-Guerrero, Melisa E. Magallanes, E. Caviedes-Vidal, W. Karasov, C. Martinez del Rio","doi":"10.1086/720232","DOIUrl":"https://doi.org/10.1086/720232","url":null,"abstract":"Trehalose is a nonreducing disaccharide that is a primary storage and energy source in prokaryotes, yeasts, fungi, and invertebrates. Vertebrates digest trehalose with the intestinal brush border membrane (BBM) enzyme trehalase. Intestinal trehalase activity is reported to be either very low or absent in several bird species. We assayed trehalase activity in 19 avian species, used proteomic analysis to quantify its abundance in the intestinal BBM, and used analyses of available genomes to detect the presence of the gene that codes for trehalase (Treh). We found no intestinal trehalase activity in birds, trehalase was absent from the proteome of their intestinal BBM, and the gene coding for trehalase was absent in their genomes. Surveys of available transcriptomes support the hypothesis that Treh is absent in birds. The trehalase gene was found in the same conserved syntenic block within the genome of all vertebrates surveyed except birds. Our analysis suggests that Treh was lost in an inversion followed by a reinsertion of a large gene block. This event appears to have taken place after the split between crocodiles and birds and dinosaurs. Birds are unable to digest a common dietary sugar like trehalose because their ancestor lost the trehalase gene. The loss of this gene seems to represent an ecological cost, as insectivorous birds seem to be unable to digest a carbohydrate present in their prey. We also speculate that the paucity of mycophagy in birds is due to the presence of large amounts of this sugar in fungal tissues.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"340 - 349"},"PeriodicalIF":1.6,"publicationDate":"2022-04-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"48322045","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}
Although heterothermy is employed by species at a global level within the order of Chiroptera (bats), the possibility of torpor being expressed in bat species inhabiting warmer climate zones has been explored only in the past couple decades. Recent studies suggest that the benefit of expressing torpor is not limited to saving energy during cold exposure or food shortage but may be just as important for saving water during heat waves. Thus, even if the physiological challenges faced by bats may depend on the habitat they live in, species expressing torpor should be found in any climate zone where employing torpor may yield benefits and increase their survival probability. Here, we summarize available data on torpor metabolic rates and daily skin temperature patterns of bats across climate zones, emphasizing similarities found in the data. We also present data that we have collected from a southern subtropical species (Nyctophilus bifax) and a northern subarctic species (Plecotus auritus) to illustrate specific examples of torpor expressions in two bat species living in highly different environments. Our findings highlight that torpor metabolic rates and skin temperature patterns of bats outside of the hibernation season can be universal across vastly different habitats, although arid environments indicate potential divergence in mean minimum torpor metabolic rates compared with measurements of populations inhabiting other climate zones.
{"title":"Universality of Torpor Expression in Bats","authors":"Mari Aas Fjelldal, Rune Sørås, Clare Stawski","doi":"10.1086/720273","DOIUrl":"https://doi.org/10.1086/720273","url":null,"abstract":"Although heterothermy is employed by species at a global level within the order of Chiroptera (bats), the possibility of torpor being expressed in bat species inhabiting warmer climate zones has been explored only in the past couple decades. Recent studies suggest that the benefit of expressing torpor is not limited to saving energy during cold exposure or food shortage but may be just as important for saving water during heat waves. Thus, even if the physiological challenges faced by bats may depend on the habitat they live in, species expressing torpor should be found in any climate zone where employing torpor may yield benefits and increase their survival probability. Here, we summarize available data on torpor metabolic rates and daily skin temperature patterns of bats across climate zones, emphasizing similarities found in the data. We also present data that we have collected from a southern subtropical species (Nyctophilus bifax) and a northern subarctic species (Plecotus auritus) to illustrate specific examples of torpor expressions in two bat species living in highly different environments. Our findings highlight that torpor metabolic rates and skin temperature patterns of bats outside of the hibernation season can be universal across vastly different habitats, although arid environments indicate potential divergence in mean minimum torpor metabolic rates compared with measurements of populations inhabiting other climate zones.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"326 - 339"},"PeriodicalIF":1.6,"publicationDate":"2022-04-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41953904","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}
Understanding the physiology of invasive species will contribute to better prediction and prevention measures to avoid the economic and environmental consequences of biological invasions. Predicting the future range of Potamopyrgus antipodarum, a globally invasive aquatic snail, relies on a comprehensive understanding of its physiological tolerances to individual and combined environmental stressors. We conducted a laboratory study to investigate the interacting effects of temperature and dissolved oxygen in shaping the abiotic niche of P. antipodarum. We generated thermal performance curves (7°C–35°C) for resting respiration rate and voluntary locomotor behaviors under normoxia and hypoxia to find the conditions that limited each performance. Extreme high (>30°C) and low (<12°C) temperatures limited respiration and activity, but respiration rate was most oxygen sensitive at low temperatures. Under hypoxic conditions, activity was less thermally sensitive. Increased activity under high temperatures (22°C–28°C) may be fueled by anaerobic metabolism. Relying on anaerobic energy is a time-limited survival strategy, so further warming and deoxygenation of freshwater systems may limit the spread of this very tolerant invasive species.
{"title":"Hypoxia Decreases Thermal Sensitivity and Increases Thermal Breadth of Locomotion in the Invasive Freshwater Snail Potamopyrgus antipodarum","authors":"E. E. King, C. Williams, J. Stillman","doi":"10.1086/719899","DOIUrl":"https://doi.org/10.1086/719899","url":null,"abstract":"Understanding the physiology of invasive species will contribute to better prediction and prevention measures to avoid the economic and environmental consequences of biological invasions. Predicting the future range of Potamopyrgus antipodarum, a globally invasive aquatic snail, relies on a comprehensive understanding of its physiological tolerances to individual and combined environmental stressors. We conducted a laboratory study to investigate the interacting effects of temperature and dissolved oxygen in shaping the abiotic niche of P. antipodarum. We generated thermal performance curves (7°C–35°C) for resting respiration rate and voluntary locomotor behaviors under normoxia and hypoxia to find the conditions that limited each performance. Extreme high (>30°C) and low (<12°C) temperatures limited respiration and activity, but respiration rate was most oxygen sensitive at low temperatures. Under hypoxic conditions, activity was less thermally sensitive. Increased activity under high temperatures (22°C–28°C) may be fueled by anaerobic metabolism. Relying on anaerobic energy is a time-limited survival strategy, so further warming and deoxygenation of freshwater systems may limit the spread of this very tolerant invasive species.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"251 - 264"},"PeriodicalIF":1.6,"publicationDate":"2022-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"48329415","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}
Chiara Morosinotto, S. Bensch, Maja Tarka, Patrik Karell
Relative telomere length (RTL), an indicator of senescence, has been shown to be heritable but can also be affected by environmental factors, such as parental effects. Investigating heritability as well as parental effects and rearing environment can help us to understand the factors affecting offspring telomeres. Moreover, how phenotypic parental traits linked with fitness can impact offspring RTL is still unclear. A phenotypic marker closely associated with physiological traits and fitness is melanin-based color polymorphism, which in tawny owl (Strix aluco) is highly heritable and strongly associated with adult telomere shortening and survival. We studied narrow-sense heritability (h2) of RTL, as well as the impact of parental age and color morph and their interaction on offspring RTL. Offspring RTL at fledging was strongly positively correlated with both mother RTL and father RTL at breeding. Offspring RTL was also negatively associated with father age, suggesting that older fathers sired offspring with shorter telomeres. Parental color morph did not explain offspring RTL, and there were no interactive effects of parental morph and age, despite previously documented morph-specific senescence patterns. Our results suggest that RTL is highly heritable and affected by paternal age but not related to color polymorphism. This suggests that either morph-specific telomere shortening as an adult does not result in significantly shorter telomeres in their gametes, or that parents compensate morph-specific senescence via parental care. Morph-specific patterns of telomere dynamics in polymorphic species may thus emerge from different life history strategies adopted in adulthood.
{"title":"Heritability and Parental Effects in Telomere Length in a Color Polymorphic Long-Lived Bird","authors":"Chiara Morosinotto, S. Bensch, Maja Tarka, Patrik Karell","doi":"10.1086/720161","DOIUrl":"https://doi.org/10.1086/720161","url":null,"abstract":"Relative telomere length (RTL), an indicator of senescence, has been shown to be heritable but can also be affected by environmental factors, such as parental effects. Investigating heritability as well as parental effects and rearing environment can help us to understand the factors affecting offspring telomeres. Moreover, how phenotypic parental traits linked with fitness can impact offspring RTL is still unclear. A phenotypic marker closely associated with physiological traits and fitness is melanin-based color polymorphism, which in tawny owl (Strix aluco) is highly heritable and strongly associated with adult telomere shortening and survival. We studied narrow-sense heritability (h2) of RTL, as well as the impact of parental age and color morph and their interaction on offspring RTL. Offspring RTL at fledging was strongly positively correlated with both mother RTL and father RTL at breeding. Offspring RTL was also negatively associated with father age, suggesting that older fathers sired offspring with shorter telomeres. Parental color morph did not explain offspring RTL, and there were no interactive effects of parental morph and age, despite previously documented morph-specific senescence patterns. Our results suggest that RTL is highly heritable and affected by paternal age but not related to color polymorphism. This suggests that either morph-specific telomere shortening as an adult does not result in significantly shorter telomeres in their gametes, or that parents compensate morph-specific senescence via parental care. Morph-specific patterns of telomere dynamics in polymorphic species may thus emerge from different life history strategies adopted in adulthood.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"350 - 364"},"PeriodicalIF":1.6,"publicationDate":"2022-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"42429399","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}
During hibernation, especially during arousal from torpor to interbout euthermia (IBE), blood flow changes drastically. In nonhibernating mammals, similar changes during ischemia/reperfusion lead to oxidative damage. We hypothesized that suppression of mitochondrial metabolism during hibernation protects against such damage. We compared markers of oxidative damage and total antioxidant capacity in eight tissues among summer, torpid, and IBE thirteen-lined ground squirrels. Overall, summer tissue had less lipid and protein oxidative damage than tissue from the hibernation season, but DNA damage (in four tissues) and total antioxidant capacity (in all eight tissues) were similar among all groups. During torpor, when mitochondrial metabolism is suppressed, lipid damage in heart, brown adipose tissue, and small intestine was lower than IBE by as much as fivefold. By contrast, oxidative damage to protein was at least twofold higher in liver and skeletal muscle in torpor compared with IBE. Our findings suggest that arousal from torpor creates oxidative damage similar to ischemia/reperfusion injury but that this damage is repaired during IBE. These differences cannot be explained by changes in antioxidant capacity, so they are likely due to differences is reactive oxygen species production among hibernation states that may relate to the well-characterized reversible suppression of mitochondrial metabolism during torpor.
{"title":"Arousal from Torpor Increases Oxidative Damage in the Hibernating Thirteen-Lined Ground Squirrel (Ictidomys tridecemlineatus)","authors":"Brynne Duffy, J. F. Staples","doi":"10.1086/719931","DOIUrl":"https://doi.org/10.1086/719931","url":null,"abstract":"During hibernation, especially during arousal from torpor to interbout euthermia (IBE), blood flow changes drastically. In nonhibernating mammals, similar changes during ischemia/reperfusion lead to oxidative damage. We hypothesized that suppression of mitochondrial metabolism during hibernation protects against such damage. We compared markers of oxidative damage and total antioxidant capacity in eight tissues among summer, torpid, and IBE thirteen-lined ground squirrels. Overall, summer tissue had less lipid and protein oxidative damage than tissue from the hibernation season, but DNA damage (in four tissues) and total antioxidant capacity (in all eight tissues) were similar among all groups. During torpor, when mitochondrial metabolism is suppressed, lipid damage in heart, brown adipose tissue, and small intestine was lower than IBE by as much as fivefold. By contrast, oxidative damage to protein was at least twofold higher in liver and skeletal muscle in torpor compared with IBE. Our findings suggest that arousal from torpor creates oxidative damage similar to ischemia/reperfusion injury but that this damage is repaired during IBE. These differences cannot be explained by changes in antioxidant capacity, so they are likely due to differences is reactive oxygen species production among hibernation states that may relate to the well-characterized reversible suppression of mitochondrial metabolism during torpor.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"229 - 238"},"PeriodicalIF":1.6,"publicationDate":"2022-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"43017290","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}
In oviparous reptiles, parental care is often limited to the energy allocated to embryos before oviposition. Reproducing females can allocate energy toward vitellogenesis, determining the number and size of eggs, fertilization, eggshell calcification, retention of eggs within the oviduct after fertilization (oviductal egg retention), and nesting activities. Oviductal egg retention in turtles ranges from 2 wk to half a year, permitting flexibility in the timing of oviposition. The energetic cost of oviductal egg retention in eastern musk turtles (Sternotherus odoratus) was investigated by measuring the metabolism of females before and after oviposition. Gravid female metabolic rates were elevated relative to male and nongravid female metabolic rates, indicating an associated energetic cost for egg retention. Metabolism of gravid females was 40% higher before oviposition than after oviposition, and it was relatively constant across the period of oviductal egg retention. Metabolic costs associated with egg retention were correlated with clutch mass and female body mass but not with clutch size or the number of days leading up to oviposition. These results suggest that the strategy of oviductal egg retention has considerable energetic costs for eastern musk turtles but that it likely provides critical flexibility in nesting phenology.
{"title":"Hold on for One More Day: Energetic Costs of Oviductal Egg Retention in Eastern Musk Turtles (Sternotherus odoratus)","authors":"Lyranda Rae Thiem, C. Gienger","doi":"10.1086/720159","DOIUrl":"https://doi.org/10.1086/720159","url":null,"abstract":"In oviparous reptiles, parental care is often limited to the energy allocated to embryos before oviposition. Reproducing females can allocate energy toward vitellogenesis, determining the number and size of eggs, fertilization, eggshell calcification, retention of eggs within the oviduct after fertilization (oviductal egg retention), and nesting activities. Oviductal egg retention in turtles ranges from 2 wk to half a year, permitting flexibility in the timing of oviposition. The energetic cost of oviductal egg retention in eastern musk turtles (Sternotherus odoratus) was investigated by measuring the metabolism of females before and after oviposition. Gravid female metabolic rates were elevated relative to male and nongravid female metabolic rates, indicating an associated energetic cost for egg retention. Metabolism of gravid females was 40% higher before oviposition than after oviposition, and it was relatively constant across the period of oviductal egg retention. Metabolic costs associated with egg retention were correlated with clutch mass and female body mass but not with clutch size or the number of days leading up to oviposition. These results suggest that the strategy of oviductal egg retention has considerable energetic costs for eastern musk turtles but that it likely provides critical flexibility in nesting phenology.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"279 - 287"},"PeriodicalIF":1.6,"publicationDate":"2022-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"47351656","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}
L. McGuire, Nathan W. Fuller, Catherine G Haase, Kirk A. Silas, S. Olson
Hibernation requires balancing energy and water demands over several months. Many studies have noted the importance of fat for hibernation energy budgets, but protein catabolism in hibernation has received less attention, and whole-animal changes in lean mass have not previously been considered. We used quantitative magnetic resonance body composition analysis to measure deposition of fat and lean mass of cave myotis (Myotis velifer) during the prehibernation period and decreases in fat and lean mass of Townsend’s big-eared bats (Corynorhinus townsendii) during hibernation. For cave myotis, lean mass represented 25% and 38% (female and male, respectively) of prehibernation mass gain. In hibernating Townsend’s big-eared bats, lean mass decrease was similar for females and males. We used values for Townsend’s big-eared bats to explore the functional implications of lean mass change for water and energy budgets. Lean mass accounted for a substantial proportion of mass change during hibernation (female: 18%, male: 35%), and although not accounting for a large proportion of the energy budget (female: 3%, male: 7%), lean mass catabolism represented an important contribution to water production (female: 14%, male: 29%). Although most mammals cannot rely on protein catabolism for metabolic water production because of the water cost of excreting urea, we propose a variation of the protein-for-water strategy whereby hibernators could temporally compartmentalize the benefits of protein catabolism to periods of torpor and the water cost to periodic arousals when free drinking water is typically available. Combined, our analyses demonstrate the importance of considering changes in lean mass during hibernation.
{"title":"Lean Mass Dynamics in Hibernating Bats and Implications for Energy and Water Budgets","authors":"L. McGuire, Nathan W. Fuller, Catherine G Haase, Kirk A. Silas, S. Olson","doi":"10.1086/720160","DOIUrl":"https://doi.org/10.1086/720160","url":null,"abstract":"Hibernation requires balancing energy and water demands over several months. Many studies have noted the importance of fat for hibernation energy budgets, but protein catabolism in hibernation has received less attention, and whole-animal changes in lean mass have not previously been considered. We used quantitative magnetic resonance body composition analysis to measure deposition of fat and lean mass of cave myotis (Myotis velifer) during the prehibernation period and decreases in fat and lean mass of Townsend’s big-eared bats (Corynorhinus townsendii) during hibernation. For cave myotis, lean mass represented 25% and 38% (female and male, respectively) of prehibernation mass gain. In hibernating Townsend’s big-eared bats, lean mass decrease was similar for females and males. We used values for Townsend’s big-eared bats to explore the functional implications of lean mass change for water and energy budgets. Lean mass accounted for a substantial proportion of mass change during hibernation (female: 18%, male: 35%), and although not accounting for a large proportion of the energy budget (female: 3%, male: 7%), lean mass catabolism represented an important contribution to water production (female: 14%, male: 29%). Although most mammals cannot rely on protein catabolism for metabolic water production because of the water cost of excreting urea, we propose a variation of the protein-for-water strategy whereby hibernators could temporally compartmentalize the benefits of protein catabolism to periods of torpor and the water cost to periodic arousals when free drinking water is typically available. Combined, our analyses demonstrate the importance of considering changes in lean mass during hibernation.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"317 - 325"},"PeriodicalIF":1.6,"publicationDate":"2022-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"45866717","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}
Mammals entering hibernation undergo drastic reductions in metabolic rate and body temperature (Tb; to as low as ∼2% of euthermic metabolic rate and 1°C to −2°C). Although ventilation (V˙E) is also greatly reduced in hibernating ground squirrels, their relative ventilatory response (%ΔV˙E) to increases in inspired CO2 (∼400% increase to 7% CO2) dwarfs that of euthermic squirrels (∼60% increase). On the basis of data from earlier studies on hypothermic animals, we hypothesized that this switch in apparent ventilatory sensitivity was the result of the change in state (from euthermic to hibernating) and not due to the change in core Tb. Thus, we used whole-body plethysmography to assess the hypercapnic ventilatory response (HCVR) in thirteen-lined ground squirrels in steady-state hibernation at 20°C, 15°C, 10°C, 7°C, and 5°C. With the transition into hibernation as Tb fell, the breathing pattern became irregular and then episodic. Total V˙E and the oxygen consumption rate (V˙O2) decreased progressively as Tb fell. Hibernating squirrels with a core Tb of 20°C increased V˙E by 150% from normocapnic levels when given 7% CO2 to breathe, while squirrels with a Tb of 7°C increased V˙E by 650% when exposed to the same inspired CO2. When Tb was cooled from 7°C to 5°C, however, the increase in the HCVR fell to 450% and was associated with a rise in V˙O2 and total V˙E. These results reveal progressive changes in breathing pattern and the HCVR with decreasing Tb and suggest that the effects of hibernation state may be Tb dependent. V˙E did not fall in proportion to metabolic rate, and the HCVR increased progressively in both absolute terms and relative terms until a Tb of 7°C, both of which potentially constrain the extent of the metabolic suppression.
{"title":"Ventilatory Sensitivity to Ambient CO2 at Different Hibernation Temperatures in Thirteen-Lined Ground Squirrels (Ictidomys tridecemlineatus)","authors":"Ryan J. Sprenger, W. Milsom","doi":"10.1086/720158","DOIUrl":"https://doi.org/10.1086/720158","url":null,"abstract":"Mammals entering hibernation undergo drastic reductions in metabolic rate and body temperature (Tb; to as low as ∼2% of euthermic metabolic rate and 1°C to −2°C). Although ventilation (V˙E) is also greatly reduced in hibernating ground squirrels, their relative ventilatory response (%ΔV˙E) to increases in inspired CO2 (∼400% increase to 7% CO2) dwarfs that of euthermic squirrels (∼60% increase). On the basis of data from earlier studies on hypothermic animals, we hypothesized that this switch in apparent ventilatory sensitivity was the result of the change in state (from euthermic to hibernating) and not due to the change in core Tb. Thus, we used whole-body plethysmography to assess the hypercapnic ventilatory response (HCVR) in thirteen-lined ground squirrels in steady-state hibernation at 20°C, 15°C, 10°C, 7°C, and 5°C. With the transition into hibernation as Tb fell, the breathing pattern became irregular and then episodic. Total V˙E and the oxygen consumption rate (V˙O2) decreased progressively as Tb fell. Hibernating squirrels with a core Tb of 20°C increased V˙E by 150% from normocapnic levels when given 7% CO2 to breathe, while squirrels with a Tb of 7°C increased V˙E by 650% when exposed to the same inspired CO2. When Tb was cooled from 7°C to 5°C, however, the increase in the HCVR fell to 450% and was associated with a rise in V˙O2 and total V˙E. These results reveal progressive changes in breathing pattern and the HCVR with decreasing Tb and suggest that the effects of hibernation state may be Tb dependent. V˙E did not fall in proportion to metabolic rate, and the HCVR increased progressively in both absolute terms and relative terms until a Tb of 7°C, both of which potentially constrain the extent of the metabolic suppression.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":"95 1","pages":"288 - 301"},"PeriodicalIF":1.6,"publicationDate":"2022-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"48852391","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}
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