{"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":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":"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}
{"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":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":"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
{"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":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":"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}
{"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":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":"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}
Carlos Mejías, J. G. Navedo, P. Sabat, L. M. Franco, F. Bozinovic, R. Nespolo
{"title":"Body Composition and Energy Savings by Hibernation: Lessons from the South American Marsupial Dromiciops gliroides","authors":"Carlos Mejías, J. G. Navedo, P. Sabat, L. M. Franco, F. Bozinovic, R. Nespolo","doi":"10.1086/719932","DOIUrl":"https://doi.org/10.1086/719932","url":null,"abstract":"Hibernation (i.e., seasonal or multiday torpor) has been described in mammals from five continents and represents an important adaptation for energy economy. However, direct quantifications of energy savings by hibernation are challenging because of the complexities of estimating energy expenditure in the field. Here, we applied quantitative magnetic resonance to determine body fat and body composition in hibernating Dromiciops gliroides (monito del monte). During an experimental period of 31 d in winter, fat was significantly reduced by 5.72±0.45 g, and lean mass was significantly reduced by 2.05±0.14 g. This fat and lean mass consumption is equivalent to a daily energy expenditure of hibernation (DEEH) of 8.89±0.6 kJ d−1, representing 13.4% of basal metabolic rate, with a proportional contribution of fat and lean mass consumption to DEEH of 81% and 18%, respectively. During the deep heterothermic bouts of monitos, body temperature remained 0.41°C ± 0.2°C above ambient temperature, typical of hibernators. Animals shut down metabolism and passively cool down to a critical defended temperature of 5.0°C ± 0.1°C, where they begin thermoregulation in torpor. Using temperature data loggers, we obtained an empirical estimation of minimum thermal conductance of 3.37±0.19 J g−1 h−1 °C−1, which is 107% of the expectation by allometric equations. With this, we parameterized body temperature/ambient temperature time series to calculate torpor parameters and metabolic rates in euthermia and torpor. Whereas the acute metabolic fall in each torpor episode is about 96%, the energy saved by hibernation is 88% (compared with the DEE of active animals), which coincides with values from the literature at similar body mass. Thus, estimating body composition provides a simple method to measure the energy saved by hibernation in mammals.","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":"47554640","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}
M. Soares, F. Banha, Sónia C. Cardoso, M. Gama, R. Xavier, Laura Ribeiro, P. Anastácio
{"title":"Hemolymph Glycemia as an Environmental Stress Biomarker in the Invasive Red Swamp Crayfish (Procambarus clarkii)","authors":"M. Soares, F. Banha, Sónia C. Cardoso, M. Gama, R. Xavier, Laura Ribeiro, P. Anastácio","doi":"10.1086/719857","DOIUrl":"https://doi.org/10.1086/719857","url":null,"abstract":"Several freshwater crayfish species, including Procambarus clarkii, are both ecologically important and commercially important benthic macroinvertebrates, remarkable for their potential to adapt and reproduce but also for their unique abilities to face distinct abiotic and biotic environments and become successful invaders. While much work has been done to study crayfish introductions, less focus has been given to how crayfish cope with pollution and other environmental stressors, in terms of physiological responses, and whether crayfish responses can be used to assess the effective state of their living environment. Here, we used a mixed approach combining laboratory experiments with field data to validate the use of hemolymph glucose as a relevant biomarker of red swamp crayfish (Procambarus clarkii) stress response. Three meaningful sampling locations were chosen across southern Portugal that are representative of different environments where crayfish live and are frequently captured for human consumption but also correspond to different pollution levels. To reference field measurements of glucose levels, we performed two lab-based experiments: (a) crayfish were exposed to different levels of stress (stress challenge) and (b) crawfish were exposed to a maze dispersal test, with or without water. Crayfish glucose levels were responsive to induced stress but were not correlated with dispersal efforts. Wild crayfish’s body condition and stress levels responded differently to environmental conditions, with more challenged individuals showing higher glycemia levels but similar body condition. The glucose levels of the more stressed wild crayfish were visually similar to lab-based crayfish subjected to the higher stress levels (electric shocks), while the levels of glucose of crayfish at the less polluted site corresponded to those measured before the start of the challenge (baseline). The maintenance of high levels of glycemia in crayfish inhabiting more challenging habitats is revealing of their higher energetic demand state. Since P. clarkii ia globally distributed and easily sampled invasive species, quantifying its hemolymph glucose levels can be a particularly useful proxy for assessing environmental quality.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-03-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"42262930","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":"Small Alpine Marsupials Regulate Evaporative Water Loss, Suggesting a Thermoregulatory Role Rather than a Water Conservation Role","authors":"P. Withers, C. Cooper, G. Körtner, F. Geiser","doi":"10.1086/719735","DOIUrl":"https://doi.org/10.1086/719735","url":null,"abstract":"We show here that evaporative water loss (EWL) is constant over a wide range of ambient relative humidity for two species of small, mesic habitat dasyurid marsupials (Antechinus agilis and Antechinus swainsonii) below thermoneutrality (20°C) and within thermoneutrality (30°C). This independence of EWL from the water vapor pressure deficit between the animal and its environment indicates that EWL is physiologically controlled by both species. The magnitude of this control of EWL was similar to that of two other small marsupials from more arid habitats, which combined with the observation that there were no effects of relative humidity on body temperature or metabolic rate, suggests that control of EWL is a consequence of precise thermoregulation to maintain heat balance rather than a water-conserving strategy at low relative humidities. The antechinus appear to manipulate cutaneous EWL rather than respiratory EWL to control their total EWL by modifying their cutaneous resistance and/or skin temperature. We propose that there is a continuum between enhanced thermoregulatory EWL at high ambient temperature and so-called insensible EWL at and below thermoneutrality.","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-03-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"43541742","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":"Repeatability of Voluntary Thermal Maximum and Covariance with Water Loss Reveal Potential for Adaptation to Changing Climates.","authors":"Matthew R McTernan, Michael W Sears","doi":"10.1086/717938","DOIUrl":"https://doi.org/10.1086/717938","url":null,"abstract":"<p><p>AbstractAlthough climate warming poses a grave threat to amphibians, little is known about the capacity of this group to evolve in response to warming. The capacity of key traits to evolve depends on the presence of genetic variation on which selection can act. Here, we use repeatability estimates to estimate the potential upper bounds of heritable genetic variation in voluntary and critical thermal maxima of gray-cheeked salamanders (<i>Plethodon metcalfi</i>). Increases in thermal tolerance may also require concordant increases in resistance to water loss because hotter temperatures incur greater evaporative risk. Therefore, we also tested for a correlation between voluntary thermal maxima and resistance to water loss and conducted an acclimation study to test for covariation between these traits in response to warming. Voluntary thermal maxima exhibited low to moderate levels of repeatability (<math><mrow><mi>R</mi><mo>=</mo><mn>0.32</mn></mrow></math>, <math><mrow><mi>P</mi><mo>=</mo><mn>0.045</mn></mrow></math>), while critical thermal maxima exhibited no statistically significant repeatability (<math><mrow><mi>R</mi><mo>=</mo><mn>0.10</mn></mrow></math>, <math><mrow><mi>P</mi><mo>=</mo><mn>0.57</mn></mrow></math>). Voluntary thermal maxima also correlated positively with resistance to water loss (<math><mrow><mi>R</mi><mo>=</mo><mn>0.31</mn></mrow></math>, <math><mrow><mi>P</mi><mo>=</mo><mn>0.025</mn></mrow></math>) but only when controlling for body mass. Voluntary thermal maxima and resistance to water loss also exhibited different acclimatory responses across control (12°C-18°C) and warm (18°C-24°C) temperature regimes, indicating a potential decoupling of traits in different thermal environments. By addressing the repeatability of thermal tolerance and the potential for covariation with resistance to water loss, we begin to address some of the key requirements of amphibians to evolve in warming climates.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39647627","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}
Marina B Blanco, Lydia K Greene, Peter H Klopfer, Danielle Lynch, Jenna Browning, Erin E Ehmke, Anne D Yoder
{"title":"Body Mass and Tail Girth Predict Hibernation Expression in Captive Dwarf Lemurs.","authors":"Marina B Blanco, Lydia K Greene, Peter H Klopfer, Danielle Lynch, Jenna Browning, Erin E Ehmke, Anne D Yoder","doi":"10.1086/718222","DOIUrl":"https://doi.org/10.1086/718222","url":null,"abstract":"<p><p>AbstractHibernation, a metabolic strategy, allows individuals to reduce energetic demands in times of energetic deficits. Hibernation is pervasive in nature, occurring in all major mammalian lineages and geographical regions; however, its expression is variable across species, populations, and individuals, suggesting that trade-offs are at play. Whereas hibernation reduces energy expenditure, energetically expensive arousals may impose physiological burdens. The torpor optimization hypothesis posits that hibernation should be expressed according to energy availability. The greater the energy surplus, the lower the hibernation output. The thrifty female hypothesis, a variation of the torpor optimization hypothesis, states that females should conserve more energy because of their more substantial reproductive costs. Contrarily, if hibernation's benefits offset its costs, hibernation may be maximized rather than optimized (e.g., hibernators with greater fat reserves could afford to hibernate longer). We assessed torpor expression in captive dwarf lemurs, primates that are obligate, seasonal, and tropical hibernators. Across 4.5 mo in winter, we subjected eight individuals at the Duke Lemur Center to conditions conducive to hibernation, recorded estimates of skin temperature hourly (a proxy for torpor), and determined body mass and tail fat reserves bimonthly. Across and between consecutive weigh-ins, heavier dwarf lemurs spent less time in torpor and lost more body mass. At equivalent body mass, females spent more time torpid and better conserved energy than did males. Although preliminary, our results support the torpor optimization and thrifty female hypotheses, suggesting that individuals optimize rather than maximize torpor according to body mass. These patterns are consistent with hibernation phenology in Madagascar, where dwarf lemurs hibernate longer in more seasonal habitats.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39788475","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}
Simon Tapper, Joshua K R Tabh, Glenn J Tattersall, Gary Burness
{"title":"Changes in Body Surface Temperature Play an Underappreciated Role in the Avian Immune Response.","authors":"Simon Tapper, Joshua K R Tabh, Glenn J Tattersall, Gary Burness","doi":"10.1086/718410","DOIUrl":"https://doi.org/10.1086/718410","url":null,"abstract":"<p><p>AbstractFever and hypothermia are well-characterized components of systemic inflammation. However, our knowledge of the mechanisms underlying such changes in body temperature is largely limited to rodent models and other mammalian species. In mammals, high dosages of an inflammatory agent (e.g., lipopolysaccharide [LPS]) typically leads to hypothermia (decrease in body temperature below normothermic levels), which is largely driven by a reduction in thermogenesis and not changes in peripheral vasomotion (i.e., changes in blood vessel tone). In birds, however, hypothermia occurs frequently, even at lower dosages, but the thermoeffector mechanisms associated with the response remain unknown. We immune challenged zebra finches (<i>Taeniopygia guttata</i>) with LPS, monitored changes in subcutaneous temperature and energy balance (i.e., body mass, food intake), and assessed surface temperatures of and heat loss across the eye region, bill, and legs. We hypothesized that if birds employ thermoregulatory mechanisms similar to those of similarly sized mammals, LPS-injected individuals would reduce subcutaneous body temperature and maintain constant surface temperatures compared with saline-injected individuals. Instead, LPS-injected individuals showed a slight elevation in body temperature, and this response coincided with a reduction in peripheral heat loss, particularly across the legs, as opposed to changes in energy balance. However, we note that our interpretations should be taken with caution owing to small sample sizes within each treatment. We suggest that peripheral vasomotion, allowing for heat retention, is an underappreciated component of the sickness-induced thermoregulatory response of small birds.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39867539","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}