Emily Hensleigh, Andrew S Murtishaw, Michael D Treat, Chelcie F Heaney, Monica M Bolton, Jonathan J Sabbagh, Kirsten N Calvin, Jefferson W Kinney, Frank van Breukelen
{"title":"Torpor Does Not Influence Spatial Memory in Hibernating Golden-Mantled Ground Squirrels (<i>Spermophilus [Callospermophilus] lateralis</i>).","authors":"Emily Hensleigh, Andrew S Murtishaw, Michael D Treat, Chelcie F Heaney, Monica M Bolton, Jonathan J Sabbagh, Kirsten N Calvin, Jefferson W Kinney, Frank van Breukelen","doi":"10.1086/721185","DOIUrl":"https://doi.org/10.1086/721185","url":null,"abstract":"<p><p>AbstractMammalian hibernation in ground squirrels is characterized by periods of torpor wherein body temperature approaches ambient temperature and metabolism is reduced to as low as 1/100th of active rates. It is unclear how hibernation affects long-term spatial memory, as tremendous remodeling of neurons is associated with torpor use. Given the suspected links between remodeling and memory formation and retention, we examined long-term spatial memory retention throughout a hibernation season. Animals were trained on a Barnes maze before entering torpor. Animals were tested for memory retention once a month throughout a hibernation season. Results indicate marked variation between individuals. Some squirrels retained memory across multiple torpor bouts, while other squirrels did not. No relationship was found between the number of torpor bouts, duration of bouts, or time spent torpid on long-term memory retention. However, that some squirrels successfully retain memory suggests that the profound remodeling of dendritic spines during torpor does not always lead to memory loss.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40604020","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}
Alex E Forlenza, Heather S Galbraith, Carrie J Blakeslee, Douglas S Glazier
{"title":"Ontogenetic Changes in Body Shape and the Scaling of Metabolic Rate in the American Eel (<i>Anguilla rostrata</i>).","authors":"Alex E Forlenza, Heather S Galbraith, Carrie J Blakeslee, Douglas S Glazier","doi":"10.1086/721189","DOIUrl":"https://doi.org/10.1086/721189","url":null,"abstract":"<p><p>AbstractThe body mass (<i>M</i>) scaling of resting metabolic rate (RMR) may vary significantly throughout ontogeny for multiple reasons that are not perfectly understood. To compare two major geometric theories of metabolic scaling, surface area (SA) theory and resource transport network (RTN) theory, we tested whether ontogenetic shifts in metabolic scaling relate to changes in body shape in the American eel (<i>Anguilla rostrata</i>). To do so, we compared the log-linear scaling exponents of RMR to <i>M</i> (<i>b</i><sub>R</sub>) and <i>M</i> to body length (<i>b</i><sub>L</sub>) in juvenile and subadult eels (glass and yellow eel life stages, respectively). Glass eels exhibited a <math><mrow><msub><mrow><mi>b</mi></mrow><mrow><mi>L</mi></mrow></msub><mo>></mo><mn>3</mn></mrow></math> and <i>b</i><sub>R</sub> significantly <2/3, as predicted by SA theory. Yellow eels also had a <math><mrow><msub><mrow><mi>b</mi></mrow><mrow><mi>L</mi></mrow></msub><mo>></mo><mn>3</mn></mrow></math>, but their <i>b</i><sub>R</sub> was not significantly different from 2/3 or 3/4. We hypothesize that two developmental changes contribute to <i>b</i><sub>R</sub> being higher for yellow eels: (1) a greater reliance on branchial respiration than body-surface-dependent cutaneous respiration and (2) a lower rate of thickening during subadult growth. An ontogenetic decrease in the ratio of cutaneous to gill respiration may have increased the relative importance of the physical constraints of a single-pump, closed circulatory system on the body-size-dependent rate of resource supply to metabolizing tissues (as predicted by RTN theory) in subadult eels. Future research is needed to quantify these developmental changes and their potential mechanistic effects on metabolic scaling, especially in the elver, a critical life stage between the glass and yellow eel stages, that was not analyzed in this study.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40613521","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}
Laura Magaly Charlanne, Sebastian Vetter, Joy Einwaller, Johanna Painer, Caroline Gilbert, Sylvain Giroud
{"title":"Sticking Together: Energetic Consequences of Huddling Behavior in Hibernating Juvenile Garden Dormice.","authors":"Laura Magaly Charlanne, Sebastian Vetter, Joy Einwaller, Johanna Painer, Caroline Gilbert, Sylvain Giroud","doi":"10.1086/721184","DOIUrl":"10.1086/721184","url":null,"abstract":"<p><p>AbstractHibernation, or multiday torpor, allows individuals to save energy via substantial reductions of metabolism and body temperature but is regularly interrupted by euthermic phases called arousals. Social thermoregulation, or \"huddling,\" can act in synergy with torpor in reducing individuals' energy and heat losses. In the wild, the garden dormouse (<i>Eliomys quercinus</i>) combines both strategies, which are crucial for winter survival of juveniles with limited prehibernation body fat reserves. We investigated via thermographic and temperature measurements (i) the energetic impact of huddling during an arousal from deep torpor, (ii) the dynamics of huddling behavior during hibernation, and (iii) its consequences during the entire winter in juvenile garden dormice. Thermographic images revealed a significant effect of huddling on torpor energetics, as it reduced heat exchange and mass loss by two-thirds in huddling versus single individuals during arousal. Our investigation of the dynamics of huddling further revealed a \"random-like mechanistic\" behavior during winter hibernation, as arousals from torpor were not always initiated by the same individuals. Animals took turns in initiating rewarming within a group, and the individual with highest body temperature during arousal entered into torpor later than the others within the huddle. The animals share both costs and benefits of huddling during arousals, without any energetic benefit of huddling over the entire winter on an individual level. We conclude that the dynamics of social thermoregulation during hibernation seems to counterbalance its benefit of reducing energetic costs associated against the energy-demanding process of rewarming from torpor.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.8,"publicationDate":"2022-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40604021","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}
Kaitlin M Baudier, Madeleine M Ostwald, Brian R Haney, Juliana M Calixto, Frank J Cossio, Jennifer H Fewell
{"title":"Social Factors in Heat Survival: Multiqueen Desert Ant Colonies Have Higher and More Uniform Heat Tolerance.","authors":"Kaitlin M Baudier, Madeleine M Ostwald, Brian R Haney, Juliana M Calixto, Frank J Cossio, Jennifer H Fewell","doi":"10.1086/721251","DOIUrl":"https://doi.org/10.1086/721251","url":null,"abstract":"<p><p>AbstractInvestigations of thermally adaptive behavioral phenotypes are critical for both understanding climate as a selective force and predicting global species distributions under climate change conditions. Cooperative nest founding is a common strategy in harsh environments for many species and can enhance growth and competitive advantage, but whether this social strategy has direct effects on thermal tolerance was previously unknown. We examined the effects of alternative social strategies on thermal tolerance in a facultatively polygynous (multiqueen) desert ant, <i>Pogonomyrmex californicus</i>, asking whether and how queen number affects worker thermal tolerances. We established and reared lab colonies with one to four queens, then quantified all colony member heat tolerances (maximum critical temperature [CT<sub>max</sub>]). Workers from colonies with more queens had higher and less variant CT<sub>max</sub>. Our findings resemble weak link patterns, in which colony group thermal performance is improved by reducing frequencies of the most temperature-vulnerable individuals. Using ambient temperatures from our collection site, we show that multiqueen colonies have thermal tolerance distributions that enable increased midday foraging in hot desert environments. Our results suggest advantages to polygyny under climate change scenarios and raise the question of whether improved thermal tolerance is a factor that has enabled the success of polygyne species in other climatically extreme environments.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40573490","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}
{"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":null,"pages":null},"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
{"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":null,"pages":null},"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
{"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":null,"pages":null},"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}
{"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":null,"pages":null},"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}
{"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":null,"pages":null},"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
{"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":null,"pages":null},"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}