Kathrin H Dausmann, Gerhard Körtner, Yaara Aharon-Rotman, Shannon E Currie, Fritz Geiser
{"title":"Flexible Employment of Torpor in Squirrel Gliders (<i>Petaurus norfolcensis</i>): An Adaptation to Unpredictable Climate?","authors":"Kathrin H Dausmann, Gerhard Körtner, Yaara Aharon-Rotman, Shannon E Currie, Fritz Geiser","doi":"10.1086/722131","DOIUrl":"https://doi.org/10.1086/722131","url":null,"abstract":"<p><p>AbstractTorpor is a highly effective response to counter various ecological and physiological bottlenecks in endotherms. In this study, we examined interrelations between thermoregulatory responses and key environmental variables in free-living squirrel gliders (<i>Petaurus norfolcensis</i>) in a habitat with drastic climatic and ecological changes across seasons. To this end, we measured body temperature (<i>T</i><sub>b</sub>) and heart rate (<i>f</i><sub>H</sub>) simultaneously throughout the year using implanted data loggers. Squirrel gliders in our study experienced fluctuations in ambient temperature (<i>T</i><sub>a</sub>) between -4.0°C and 44.1°C and expressed torpor at different times during the year. In contrast to our expectations, torpor seemed to be employed flexibly, on demand, and most frequently in spring rather than during the coldest and/or hottest periods. Torpor bouts lasted, on average, about 5 h, and <i>T</i><sub>b</sub> during torpor dropped as low as 17.9°C. The <i>f</i><sub>H</sub> during torpor decreased below 50 bpm, which is about one-third of the basal level. The ability to record <i>f</i><sub>H</sub> alongside <i>T</i><sub>b</sub> enabled us to also report periods of low <i>f</i><sub>H</sub> during thermoconforming hyperthermia at <i>T</i><sub>a</sub>'s above 35°C that likely occurred to conserve energy and water. Our findings double the body size of Australian gliders for which data on torpor are available and advance our ecological understanding of the dynamics of torpor expression in wild mammals and of how animals cope with varying conditions. Moreover, they highlight that the flexibility of physiology and thermoregulatory responses are clearly more complex than previously thought.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10645599","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}
Jan Nedergaard, Alexander W Fischer, Barbara Cannon
{"title":"Leptin as an Antitorpor Hormone: An Explanation for the Increased Metabolic Efficiency and Cold Sensitivity of <i>ob/ob</i> Mice?","authors":"Jan Nedergaard, Alexander W Fischer, Barbara Cannon","doi":"10.1086/722135","DOIUrl":"https://doi.org/10.1086/722135","url":null,"abstract":"<p><p>AbstractLeptin is recognized as an anorexigenic hormone. In its absence (e.g., in <i>ob/ob</i> mutant mice), mice become obese, primarily as a result of hyperphagia. A recurrent question is whether, additionally, leptin is thermogenic and thus also an antiobesity hormone in this way. We have earlier reviewed available data and have concluded that most articles implying a thermogenic effect of leptin have based this on a misconstrued division by body weight. Here, we have collected evidence that the remaining observations that imply that leptin is a thermogenic hormone are better understood as implying that leptin is an antitorpor hormone. Leptin levels increase in proportion to the body's energy reserves (i.e., stored lipids in the adipose tissue), and leptin thus serves as an indicator of energy availability. In the absence of leptin, <i>ob/ob</i> mice are exceedingly prone to enter daily torpor, since the absence of leptin causes them to perceive a lack of body energy reserves that, in combination with restricted or no food, induces them to enter the torpid state to save energy. This antitorpor effect of leptin probably explains the following earlier observations. First, <i>ob/ob</i> mice have the ability to gain weight even when pair fed with leptin-treated <i>ob/ob</i> mice. This is understood as follows: In the leptin-treated <i>ob/ob</i> mice, food intake is reduced. Untreated pair-fed mice enter daily torpor, and this markedly lowers total daily energy expenditure; the resulting surplus food energy is then accumulated as fat in these mice. However, <i>ob/ob</i> mice fed ad lib. do not enter torpor, so under normal conditions this mechanism does not contribute to the obesity found in the <i>ob/ob</i> mice. Second, neonatal <i>ob/ob</i> mice have the ability to become obese despite eating the same amount as wild-type mice: this is understood as these mice similarly entering daily torpor. Third, <i>ob/ob</i> mice on the C57BL/6J background have a lower metabolic rate: these mice were examined in the absence of food, and torpor was thus probably induced. Fourth, <i>ob/ob</i> mice have apparent high cold sensitivity: these mice experienced cold in the absence of food and would immediately enter deep torpor. It is suggested that this novel explanation of how the antitorpor effects of leptin affect mouse energy metabolism can open new avenues for leptin research.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10645603","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}
Michael D Treat, Anthony J Marlon, Lorena Samentar, Nora Caberoy, Frank van Breukelen
{"title":"Mitigating Apoptotic and Inflammatory Signaling via Global Caspase Inhibition in Hibernating Ground Squirrels, <i>Spermophilus lateralis</i>.","authors":"Michael D Treat, Anthony J Marlon, Lorena Samentar, Nora Caberoy, Frank van Breukelen","doi":"10.1086/722133","DOIUrl":"https://doi.org/10.1086/722133","url":null,"abstract":"<p><p>AbstractIn most systems, the caspase cascade is activated during cellular stress and results in inflammation and apoptosis. Hibernators experience stressors such as extremely low body temperatures, bradycardia, possible ischemia and reperfusion, and acidosis. However, widespread inflammation and apoptosis would represent an energetic expense that is incompatible with hibernation. To better understand global caspase regulation during hibernation, we employed a systems-level approach and analyzed 11 caspases in ground squirrel liver that are involved in inflammatory (caspases 1, 4, 5, 11, and 12) and apoptotic (caspases 2, 6, 7, 8, 9, and 10) pathways. Western blots revealed liberation of active forms for two inflammatory (caspases 11 and 12) and two apoptotic (caspases 6 and 9) caspases during hibernation (e.g., p15, the most active fragment of caspase 6, increased <math><mrow><mn>8.26</mn><mo>±</mo><mn>0.70</mn><mtext>-fold</mtext></mrow></math> in interbout-aroused animals). We used specific peptide substrates to interrogate the four seemingly activated caspases and demonstrated no expected increases in proteolytic activity. Specific targets of these four caspases were similarly not cleaved, demonstrating that initiation of caspase activation may occur without concomitant downstream effects. Similarly, we found no evidence for upstream activation for caspase 9 signaling based on permeabilization of the outer mitochondrial membrane. We contend that these caspases are suppressed after seeming activation during hibernation. Incomplete caspase signaling is effectively mitigating the induction of widespread inflammation and apoptosis during hibernation.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10638946","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":"Sex-Specific Effects of Blood Serotonin on Reproductive Effort in a Small Passerine.","authors":"Vallo Tilgar","doi":"10.1086/722132","DOIUrl":"https://doi.org/10.1086/722132","url":null,"abstract":"<p><p>AbstractLaboratory animal models have shown that blood serotonin levels reflect consistent individual differences in behavioral decision-making and maternal behavior. Serotonin could also help to understand intraspecific variation in reproductive strategies, although the mechanisms are poorly understood. In this study, the relationships of plasma serotonin with breeding parameters and parental behavior were examined in wild great tits (<i>Parus major</i>). Females who laid eggs earlier had higher levels of serotonin in the second half of the nestling period, while no significant relationship of serotonin with clutch size, brood size, and body size was detected. In males, serotonin levels were negatively related to clutch size and brood size and positively related to body size. The association of serotonin with provisioning behavior was sex specific, and acute fear stress induced by a predator presentation did not change this relationship. Food provisioning was positively related to size-corrected serotonin levels in females and negatively related to size-corrected serotonin levels in males. These results suggest that peripheral serotonin is a sensitive marker of parental behavior and reproductive effort in wild birds, while the mechanisms linking this neurotransmitter to reproduction are probably mediated by interplay between the serotonergic system, sex hormones, and other neurotransmitters.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10645604","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}
Christopher J Clark, John R Hutchinson, Theodore Garland
{"title":"The Inverse Krogh Principle: All Organisms Are Worthy of Study.","authors":"Christopher J Clark, John R Hutchinson, Theodore Garland","doi":"10.1086/721620","DOIUrl":"https://doi.org/10.1086/721620","url":null,"abstract":"<p><p>AbstractKrogh's principle states, \"For such a large number of problems there will be some animal of choice, or a few such animals, on which it can be most conveniently studied.\" The downside of picking a question first and then finding an ideal organism on which to study it is that it will inevitably leave many organisms neglected. Here, we promote the inverse Krogh principle: all organisms are worthy of study. The inverse Krogh principle and the Krogh principle are not opposites. Rather, the inverse Krogh principle emphasizes a different starting point for research: start with a biological unit, such as an organism, clade, or specific organism trait, then seek or create tractable research questions. Even the hardest-to-study species have research questions that can be asked of them: Where does it fall within the tree of life? What resources does it need to survive and reproduce? How does it differ from close relatives? Does it have unique adaptations? The Krogh and inverse Krogh approaches are complementary, and many research programs naturally include both. Other considerations for picking a study species include extreme species, species informative for phylogenetic analyses, and the creation of models when a suitable species does not exist. The inverse Krogh principle also has pitfalls. A scientist that picks the organism first might choose a research question not really suited to the organism, and funding agencies rarely fund organism-centered grant proposals. The inverse Krogh principle does not call for all organisms to receive the same amount of research attention. As knowledge continues to accumulate, some organisms-models-will inevitably have more known about them than others. Rather, it urges a broader search across organismal diversity to find sources of inspiration for research questions and the motivation needed to pursue them.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10638945","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}
Grace A Casselberry, Joseph C Drake, Nicole Perlot, Steven J Cooke, Andy J Danylchuk, Robert J Lennox
{"title":"Allometric Scaling of Anaerobic Capacity Estimated from a Unique Field-Based Data Set of Fish Swimming.","authors":"Grace A Casselberry, Joseph C Drake, Nicole Perlot, Steven J Cooke, Andy J Danylchuk, Robert J Lennox","doi":"10.1086/722134","DOIUrl":"https://doi.org/10.1086/722134","url":null,"abstract":"<p><p>AbstractLocomotion is a defining characteristic that can dictate many aspects of an organism's life history in the pursuit of maximizing fitness, including escaping predators, capturing prey, and transitioning between habitats. Exhaustive exercise can have negative consequences for both short-term and long-term energetics and life history trade-offs, influencing fish survival and reproduction. Studies of swimming performance and exhaustive exercise in fish are often conducted on individual species, but few multispecies analyses exist and even fewer in field settings. In fish, swimming performance and exercise have historically been studied in the laboratory using swim tunnels, but an increasing body of work in recreational fisheries science provides a novel way to examine swimming capacity and exhaustion. Using fight time, the time it takes for a hooked fish to be landed on rod and reel fishing gear, as an opportunistic proxy for fish exhaustion, a multispecies meta-analysis of data from studies on recreational fisheries was conducted to elucidate the factors that most influence capacity for exhaustive exercise. Data from 39 species of freshwater and marine fish were aggregated, and negative binomial mixed effects models as well as phylogenetic least squares regression were used to identify the factors that most influenced exhaustive exercise in the field. Fish total length, aspect ratio of the caudal fin, and body form were significant factors in explaining the capacity for exhaustive exercise. Large migratory fish with high aspect ratios were able to fight, and therefore exercise, the longest. These results illustrate that body form and physiology are both deeply intertwined to inform function across fish species and point to angling fight time as a useful approximation of fish swimming capabilities that can be further developed for understanding the limits of fish exercise physiology.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10645600","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}
Kim Birnie-Gauvin, Carsten Berthelsen, Torben Larsen, Kim Aarestrup
{"title":"The Physiological Costs of Reproduction in a Capital Breeding Fish.","authors":"Kim Birnie-Gauvin, Carsten Berthelsen, Torben Larsen, Kim Aarestrup","doi":"10.1086/722136","DOIUrl":"https://doi.org/10.1086/722136","url":null,"abstract":"<p><p>AbstractReproduction represents the most energetically demanding period of life for many organisms. Capital breeders, such as anadromous sea trout (<i>Salmo trutta</i>), provide a particularly interesting group of organisms to study within the context of reproduction because they rely on energy stores accrued before breeding to reproduce and sustain all phenotypic and behavioral changes related to reproduction. Energy allocation into current reproduction therefore cannot be mitigated via food intake, resulting in an important life history trade-off. For this reason, exploring indexes related to energetics in salmonids can provide powerful insights into the physiological costs of reproduction. In this study, we sampled blood from and PIT tagged 232 fish captured in the wild before the spawning season. We recaptured and resampled 74 individuals (53 females and 21 males) at the end of the spawning season. Females were further divided into spawning phases (nonspawned, partially spawned, and spawned individuals), though males could not be classified as such. We compared nutritional correlates (triglycerides, cholesterol, calcium, inorganic phosphorus, and total protein), stress correlates (cortisol, sodium, potassium, chloride, and glucose), and indexes of tissue damage (aspartate aminotransferase) between initial capture and recapture as well as among spawning phases in females. We found that nutritional status decreased in all fish throughout the spawning season but that it was substantially lower in females that had spawned. We further found that spawning itself appears stressful, with elevated glucose in partially spawned females and elevated cortisol in male sea trout at recapture. Our findings thus support the idea that the cost of reproduction is energetically high and that incurred stress and a decrease in nutritional status are important physiological costs.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2023-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10645601","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":"Body Temperature Patterns and Energy Balance Hormones in Free-Living Thirteen-Lined Ground Squirrels (<i>Ictidomys tridecemlineatus</i>) from Different Latitudes.","authors":"Hallie Dickerson, Veronique Tessier, Emily Davis, Emma Solis, Taqwa Armstrong, Jessica Healy-La Price","doi":"10.1086/721443","DOIUrl":"https://doi.org/10.1086/721443","url":null,"abstract":"<p><p>AbstractThis article examines hormone concentrations and body temperature (<i>T</i><sub>b</sub>) patterns of free-living thirteen-lined ground squirrels (TLGSs) across the majority of their latitudinal range in the United States (from Texas to Minnesota). Free-living TLGSs (<math><mrow><mi>n</mi><mo>=</mo><mn>40</mn></mrow></math>) were implanted with <i>T</i><sub>b</sub>data loggers in 2019 before they entered hibernation. Three adult female TLGSs, one each from Oklahoma (low latitude), Iowa (middle latitude), and Minnesota (high latitude), were recaptured in 2020 after the hibernation season. Although this provides an <i>n</i> of 1 for each location and therefore no statistically supported conclusions can be drawn, the hibernation season was longest in the animal from the highest latitude with coldest winter soil temperatures (Minnesota) and shortest in the animal retrapped at the lowest latitude (Oklahoma). Torpor bouts were generally longer when soil temperatures were lower. The Iowa and Minnesota squirrels had a prolonged period of short torpor bouts with <i>T</i><sub>b</sub> near 20°C at the beginning of the hibernation season. Concentrations of the orexigenic hormone ghrelin and the sex hormones estradiol and testosterone were also compared in populations from different latitudes. In general, Minnesota males had higher testosterone than males from other populations, possibly due to a later breeding season relative to other squirrel populations. Animals trapped in early summer had significantly lower concentrations of ghrelin than those captured in midsummer, potentially driving the fat-storing period before the hibernation season. Together, these results suggest latitudinal variation in physiological regulation of circannual rhythms.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"33481820","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}
Oana Birceanu, Patricia Ferreira, James Neal, Julia Sunga, Shaun Anthony, Shannon M Davidson, Susan L Edwards, Jonathan M Wilson, John H Youson, Mathilakath M Vijayan, Michael P Wilkie
{"title":"Divergent Pathways of Ammonia and Urea Production and Excretion during the Life Cycle of the Sea Lamprey.","authors":"Oana Birceanu, Patricia Ferreira, James Neal, Julia Sunga, Shaun Anthony, Shannon M Davidson, Susan L Edwards, Jonathan M Wilson, John H Youson, Mathilakath M Vijayan, Michael P Wilkie","doi":"10.1086/721606","DOIUrl":"https://doi.org/10.1086/721606","url":null,"abstract":"<p><p>Little is known about nitrogenous waste (N waste) handling and excretion (<i>J</i><sub>N waste</sub>) during the complex life cycle of the sea lamprey (<i>Petromyzon marinus</i>), an extant jawless fish that undergoes a complete metamorphosis from a filter-feeding larva (ammocoete) into a parasitic juvenile that feeds on the blood of larger, jawed fishes. Here, we investigate the ammonia- and urea-handling profiles of sea lampreys before, during, and after metamorphosis. The rates of ammonia excretion (<i>J</i><sub>amm</sub>) and urea excretion (<i>J</i><sub>urea</sub>) significantly decreased after the onset of metamorphosis, with the lowest rates observed during midmetamorphosis. Near the completion of metamorphosis, rates of <i>J</i><sub>N waste</sub> (<math><mrow><msub><mrow><mi>J</mi></mrow><mrow><mi>N waste</mi></mrow></msub><mo>=</mo><msub><mrow><mi>J</mi></mrow><mrow><mstyle><mrow><mi>a</mi></mrow></mstyle><mi>mm</mi></mrow></msub><mo>+</mo><msub><mrow><mi>J</mi></mrow><mrow><mstyle><mrow><mi>u</mi></mrow></mstyle><mi>rea</mi></mrow></msub></mrow></math>) significantly increased as sea lampreys entered the juvenile period. Feeding juvenile lampreys had greater than 10- to 15-fold higher <i>J</i><sub>amm</sub> and fivefold higher <i>J</i><sub>urea</sub> compared to nonfed juveniles, which corresponded to higher postprandial (postfeeding) concentrations of plasma ammonia and urea. The routes of <i>J</i><sub>amm</sub> and <i>J</i><sub>urea</sub> completely diverged following metamorphosis. In larvae, <i>J</i><sub>amm</sub> was equally split between branchial (gills) and extrabranchial (skin plus renal) pathways, but following metamorphosis, >80% of ammonia was excreted via the gills in nonfeeding juvenile lampreys, and >95% of ammonia was excreted via the gills in adult sea lampreys. Urea, on the other hand, was predominantly excreted via extrabranchial routes and, to a lesser extent, the gills in larvae and in nonfeeding juveniles. In adults, however, virtually all urea was excreted via urine. Reverse transcription polymerase chain reaction and in silico analyses also indicated that a urea transporter encoded by a <i>slc4a2</i>-like gene is present in lampreys. The branchial expression of this transporter is modulated throughout sea lamprey life history, as it is higher in the larvae and steadily decreases until the adult stage. We conclude that the divergent pathways of <i>J</i><sub>amm</sub> and <i>J</i><sub>urea</sub> during the sea lamprey life cycle reflect changes in their habitat, lifestyle, and diet. Further, the near-complete reliance on renal routes for <i>J</i><sub>urea</sub> in adult sea lampreys is unique among fishes and may reflect the ancestral condition of how this N waste product was handled and excreted by the earliest vertebrates.</p>","PeriodicalId":54609,"journal":{"name":"Physiological and Biochemical Zoology","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2022-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40587652","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}