Physiological and Biochemical Zoology最新文献

AbstractTorpor, the temporary reduction of metabolic rate and body temperature, is a common energy-saving strategy in endotherms. Because of their small body size and energetically demanding life histories, hummingbirds have proven useful for understanding when and why endotherms use torpor. Previous studies of torpor in hummingbirds have been largely limited to tropical montane species or long-distance migrants that regularly experience challenging thermal conditions. Comparatively little is known, however, about the use of torpor in hummingbirds of the lowland tropics, where relatively high and stable year-round temperatures may at least partially negate the need for torpor. To fill this knowledge gap, we tested for the occurrence of torpor in tropical lowland hummingbirds ($n=37$ individuals of six species) from central Panama. In controlled experimental conditions simulating the local temperature regime, all six species used torpor to varying degrees and entered torpor at high ambient temperatures (i.e., ≥28°C), indicating that hummingbirds from the thermally stable lowland tropics regularly use torpor. Torpor reduced overnight mass loss, with individuals that spent more time in torpor losing less body mass during temperature experiments. Body mass was the best predictor of torpor depth and duration among and within species-smaller species and individuals tended to use torpor more frequently and enter deeper torpor. Average mass loss in our experiments (∼8%-10%) was greater than that reported in studies of hummingbirds from higher elevation sites (∼4%). We therefore posit that the energetic benefits accrued from torpor may be limited by relatively high nighttime temperatures in the lowland tropics, although further studies are needed to test this hypothesis.

AbstractHibernating golden-mantled ground squirrels, Spermophilus [Callospermophilus] lateralis, tolerate proapoptotic conditions, such as low body temperature, anorexia, acidosis, and ischemia/reperfusion. Avoiding widespread apoptosis is critical for hibernator survival. Caspase 3, the key executioner of apoptosis, cleaves a majority of apoptotic targets. Under proapoptotic conditions, inactive procaspase 3 (32 kDa) is activated when cleaved into 17- and 12-kDa fragments (p32, p17, and p12, respectively). Caspase 3 activation results in extreme enzymatic activation. Activity increases >10,000-fold followed by apoptotic execution. Is widespread apoptosis occurring during the proapoptotic hibernation season? Western blots showed p17 increased ∼2-fold during hibernation, indicating caspase 3 activation. However, in vitro caspase 3 activity assays found no extreme increases in activity. Downstream caspase 3 targets ICAD (inhibitor of caspase-activated deoxyribonuclease) and PARP (poly (ADP-ribose) polymerase) did not experience elevated cleavage during hibernation, which is inconsistent with caspase 3 activation. TUNEL (terminal deoxynucleotidyl transferase-mediated deoxyuridine triphosphate nick-end labeling) assays from multiple tissues found only 0.001%-0.009% of cells were TUNEL positive during winter, indicating negligible apoptosis during hibernation. Typically, caspase 3 activation generates a strong commitment toward apoptosis. We found that despite a ∼2-fold increase in active caspase 3, hibernators experience no downstream caspase 3 activity or widespread apoptosis. A systems-level approach suggests an incomplete signaling cascade wherein some caspase 3 activation during hibernation does not necessarily lead to bona fide apoptosis.

AbstractHibernation-like episodes would be particularly interesting for clinical and spatial use if they could be observed and induced in humans. As animal hibernation differs from hypothermia with its control by a temperature-dependent clock, we undertook to find evidence that human hypothermia might affect the circadian clock system. We revisited Siffre's 1962 abyss experiment. Deprived of temporal information and showing signs of chronic hypothermia, Siffre underestimated his stay underground by 22 d. We show that the temperature-dependent clock equation for classical hibernators accurately predicts Siffre's subjective times, and we list potential conditions to be further explored for inducing hibernation-like bouts in humans.

AbstractGiven the critical role of metabolism in the life history of all organisms, there is particular interest in understanding the relationship between individual metabolic phenotypes and the capacity to partition energy into competing life history traits. Such relationships could be predictive of individual phenotypic performances throughout life. Here, we were specifically interested in whether an individual fish's metabolic phenotype can shape its propensity to feed following a significant stressor (2-min exhaustive exercise challenge). Such a relationship would provide insight into previous intraspecific observations linking high metabolism with faster growth. Using a teleost fish, the barramundi (Lates calcarifer), we predicted that individuals with high standard metabolic rates (SMRs) and maximal metabolic rates (MMRs) would be faster to recover and resume feeding after exercise. Contrary to our prediction, neither SMR nor MMR was correlated with latency to feed after exercise (food was offered at 0.5, 1.5, 3, and 18 h after exercise). Only time after exercise and individual fish ID were significant predictors of latency to feed. Measurements of MMR from the same individuals (three measurements spaced 8-12 d apart) revealed a moderate degree of repeatability ($R=0.319$). We propose that interindividual differences in biochemical and endocrine processes may be more influential than whole-organism metabolic phenotype in mediating feeding latency after exercise.

AbstractBioelectrical impedance analysis (BIA) is gaining popularity in wildlife studies as a portable technology for immediate and nondestructive predictions of body composition components, such as fat-free and fat masses. Successful application of BIA for field-based research requires the identification and control of potential sources of error, as well as the creation of and adherence to a standardized protocol for measurement. The aim of our study was to determine sources of error and to provide a standardization protocol to improve measurement precision of BIA on juvenile green turtles (Chelonia mydas; $n=35$). We assessed the effects of altered environmental temperature (20°C-30°C), postprandial state (2-72 h), and time out of the water (2 h) on five impedance parameters (resistance at infinite frequency [R_inf], resistance at zero frequency [R₀], resistance at 50 kHz [R₅₀], phase angle at 50 kHz [PhA₅₀], and intracellular resistance [R_i]) using a bioimpedance spectroscopy device. Technical reproducibility of measurements and interanimal variability were also assessed. We found an inverse exponential relationship between change in environmental temperature and impedance parameters R_inf, R₀, and R₅₀. Postprandial state significantly increased R_inf and R_i 72 h after feeding. BIA measurements were reproducible within individual juvenile green turtles at temperatures from 20°C to 30°C. Significant variation in impedance values was found between animals at all temperatures, sampling times, and postprandial states, but the relative differences (%) were small in magnitude. Our study suggests that measurement precision is improved by measuring animals at consistent environmental temperatures close to their preferred thermal range. We propose a standardized protocol of measurement conditions to facilitate laboratory and field use of BIA for body composition assessment studies in turtles.

AbstractThe idea of putting astronauts into a hibernation-like state during interplanetary spaceflights has sparked new interest in the evolutionary roots of hibernation and torpor. In this context, it should be noted that mammalian fetuses and neonates respond to the environmental challenges in the perinatal period with a number of physiological mechanisms that bear striking similarity to hibernation and torpor. These include three main points: first, prenatal deviation from the overall metabolic size relationship, which adapts the fetus to the low-oxygen conditions in the womb and corresponds to the metabolic reduction during hibernation and estivation; second, intranatal diving bradycardia in response to shortened O₂ supply during birth, comparable to the decrease in heart rate preceding the drop in body temperature upon entry into torpor; and third, postnatal onset of nonshivering thermogenesis in the brown adipose tissue, along with the increase in basal metabolic rate up to the level expected from body size, such as during arousal from hibernation. The appearance of hibernation-like adaptations in the perinatal period suggests that, conversely, hibernation and torpor may be composed of mechanisms shared by all mammals around birth. This hypothesis sheds new light on the origins of hibernation and supports its potential accessibility to nonhibernating species, including humans.

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 (Petaurus norfolcensis) in a habitat with drastic climatic and ecological changes across seasons. To this end, we measured body temperature (T_b) and heart rate (f_H) simultaneously throughout the year using implanted data loggers. Squirrel gliders in our study experienced fluctuations in ambient temperature (T_a) 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 T_b during torpor dropped as low as 17.9°C. The f_H during torpor decreased below 50 bpm, which is about one-third of the basal level. The ability to record f_H alongside T_b enabled us to also report periods of low f_H during thermoconforming hyperthermia at T_a'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.

AbstractLeptin is recognized as an anorexigenic hormone. In its absence (e.g., in ob/ob 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, ob/ob 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, ob/ob mice have the ability to gain weight even when pair fed with leptin-treated ob/ob mice. This is understood as follows: In the leptin-treated ob/ob 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, ob/ob mice fed ad lib. do not enter torpor, so under normal conditions this mechanism does not contribute to the obesity found in the ob/ob mice. Second, neonatal ob/ob 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, ob/ob 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, ob/ob 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.

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 $8.26\pm 0.70\text{-fold}$ 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.