Arctic homeotherms counter challenges at high latitudes using a combination of seasonal adjustments in pelage/plumage, fat deposition and intricate thermoregulatory adaptations. However, there are ...still gaps in our understanding of their thermal responses to cold, particularly in Arctic birds. Here, we have studied the potential use of local heterothermy (i.e. tissue cooling that can contribute to significantly lower heat loss rate) in Svalbard ptarmigan (
) - the world's northernmost land bird. We exposed birds kept under simulated Svalbard photoperiod to low ambient temperatures (
; between 0 and -30°C) during three seasons (early winter, late winter, summer), whilst recording resting metabolic rate (RMR), core temperature (
) and several cutaneous temperatures. Leg skin temperature varied the most, but still only by up to ∼15°C, whereas body trunk skin temperature changed <1°C when
decreased from 0 to -30°C. At the same time,
increased by 0.9°C, concomitant with increased RMR. This was probably driven by the triggering of cerebral thermosensors in response to cooling of the poorly insulated head, the skin of which was 5.4°C colder at -30°C than at 0°C. Thermal conductance in winter was higher in yearlings, probably because they were time/resource constrained from acquiring a high-quality plumage and sufficient fat reserves as a result of concomitant body growth. In conclusion, Svalbard ptarmigan do not employ extensive local heterothermy for cold protection but instead rely on efficient thermogenesis combined with excellent body insulation. Hence, cold defence in the world's northernmost land bird is not mechanistically much different from that of its lower latitude relatives.
Animals in seasonal environments must prudently manage energy expenditure to survive the winter. This may be achieved through reductions in the allocation of energy for various purposes (e.g. ...thermoregulation, locomotion, etc.). We studied whether such trade-offs also include suppression of the innate immune response, by subjecting captive male Svalbard ptarmigan (
) to bacterial lipopolysaccharide (LPS) during exposure to either mild temperature (0°C) or cold snaps (acute exposure to -20°C), in constant winter darkness when birds were in energy-conserving mode, and in constant daylight in spring. The innate immune response was mostly unaffected by temperature. However, energy expenditure was below baseline when birds were immune challenged in winter, but significantly above baseline in spring. This suggests that the energetic component of the innate immune response was reduced in winter, possibly contributing to energy conservation. Immunological parameters decreased (agglutination, lysis, bacteriostatic capacity) or did not change (haptoglobin/PIT54) after the challenge, and behavioural modifications (anorexia, mass loss) were lengthy (9 days). While we did not study the mechanisms explaining these weak, or slow, responses, it is tempting to speculate they may reflect the consequences of having evolved in an environment where pathogen transmission rate is presumably low for most of the year. This is an important consideration if climate change and increased exploitation of the Arctic would alter pathogen communities at a pace outwith counter-adaption in wildlife.
While foraging, marine mammals undertake repetitive diving bouts. When the animal surfaces, reperfusion makes oxygen readily available for the electron transport chain, which leads to increased ...production of reactive oxygen species and risk of oxidative damage. In blood and several tissues, such as heart, lung, muscle and kidney, marine mammals generally exhibit an elevated antioxidant defence. However, the brain, whose functional integrity is critical to survival, has received little attention. We previously observed an enhanced expression of several antioxidant genes in cortical neurons of hooded seals (
). Here, we studied antioxidant gene expression and enzymatic activity in the visual cortex, cerebellum and hippocampus of harp seals (
) and hooded seals. Moreover, we tested several genes for positive selection. We found that antioxidants in the first line of defence, such as superoxide dismutase (SOD), glutathione peroxidase (GPX) and glutathione (GSH) were constitutively enhanced in the seal brain compared to mice (
), whereas the glutaredoxin and thioredoxin systems were not. Possibly, the activity of the latter systems is stress-induced rather than constitutively elevated. Further, some, but not all members, of the glutathione-s-transferase (GST) family appear more highly expressed. We found no signatures of positive selection, indicating that sequence and function of the studied antioxidants are conserved in pinnipeds.
Lipids make up more than half of the human brain's dry weight, yet the composition and function of the brain lipidome is not well characterized. Lipids not only provide the structural basis of cell ...membranes, but also take part in a wide variety of biochemical processes. In neurodegenerative diseases, lipids can facilitate neuroprotection and serve as diagnostic biomarkers. The study of organisms adapted to extreme environments may prove particularly valuable in understanding mechanisms that protect against stressful conditions and prevent neurodegeneration. The brain of the hooded seal (Cystophora cristata) exhibits a remarkable tolerance to low tissue oxygen levels (hypoxia). While neurons of most terrestrial mammals suffer irreversible damage after only short periods of hypoxia, in vitro experiments show that neurons of the hooded seal display prolonged functional integrity even in severe hypoxia. How the brain lipidome contributes to the hypoxia tolerance of marine mammals has been poorly studied. We performed an untargeted lipidomics analysis, which revealed that lipid species are significantly modulated in marine mammals compared with non-diving mammals. Increased levels of sphingomyelin species may have important implications for efficient signal transduction in the seal brain. Substrate assays also revealed elevated normoxic tissue levels of glucose and lactate, which suggests an enhanced glycolytic capacity. Additionally, concentrations of the neurotransmitters glutamate and glutamine were decreased, which may indicate reduced excitatory synaptic signaling in marine mammals. Analysis of hypoxia-exposed brain tissue suggests that these represent constitutive mechanisms rather than an induced response towards hypoxic conditions.
The heating and moistening of inhaled air, and the cooling and moisture removal from exhaled air, are crucial for the survival of animals under severe environmental conditions. Arctic mammals have ...evolved specific adaptive mechanisms to retain warmth and water and restrict heat loss during breathing. Here, the role of the porous turbinates of the nasal cavities of Arctic and subtropical seals is studied with this in mind. Mass and energy balance equations are used to compute the time-dependent temperature and water vapor profiles along the nasal passage. A quasi-1D model based on computed tomography images of seal nasal cavities is used in numerical simulations. Measured cross-sectional areas of the air channel and the perimeters of the computed tomography slices along the nasal cavities of the two seal species are used. The model includes coupled heat and vapor transfer at the air-mucus interface and heat transfer at the interfaces between the tissues and blood vessels. The model, which assumes constant blood flow to the nose, can be used to predict the temperature of the exhaled air as a function of ambient temperature. The energy dissipation (entropy production) in the nasal passages was used to measure the relative importance of structural parameters for heat and water recovery. We found that an increase in perimeter led to significant decreases in the total energy dissipation. This is explained by improved conditions for heat and water transfer with a larger complexity of turbinates. Owing to differences in their nasal cavity morphology, the Arctic seal is expected to be advantaged in these respects relative to the subtropical seal.
Stress-induced hyperthermia (SIH) is commonly observed during handling in homeotherms. However, in birds, handling in cold environments typically elicits hypothermia. It is unclear whether this ...indicates that SIH is differently regulated in this taxon or if it is due to size, because body temperature changes during handling in low temperatures have only been measured in small birds <0.03 kg (that are more likely to suffer high heat loss when handled). We have therefore studied thermal responses to handling stress in the intermediate-sized (0.5-1.0 kg) Svalbard ptarmigan (
) in 0°C and -20°C, in winter and spring. Handling caused elevated core body temperature and peripheral vasoconstriction that reduced back skin temperature. Core temperature increased less, and back skin temperature decreased more, in -20°C than in 0°C, probably because of higher heat-loss rate at the lower temperature. Responses were qualitatively consistent between seasons, despite higher body condition/insulation in winter and dramatic seasonal changes in photoperiod, both of which could possibly affect stress responsiveness. Our study supports the notion that SIH is a general thermoregulatory reaction to acute stressors in endotherms, but also suggests that body size and thermal environment should be taken into account when evaluating this response in birds.
The Svalbard Rock Ptarmigan,
Lagopus muta hyperborea,
is the only year-round resident terrestrial bird in the high Arctic. Many of the physiological and morphological adaptations permitting its ...winter endurance in this harsh environment are well understood. However, it remains unknown how the conspicuous moult from a greyish brown summer to a white winter plumage, and any underlying changes in plumage structure and feather morphology, contribute to seasonal acclimatisation. We used standard morphometric techniques to describe the seasonal change in plumage and feather characteristics in six body regions. Then, we investigated whether winter plumage traits differed between first-winter and adult (second winter, or older) birds, because a difference in coat insulation has been suggested as an explanation for why first-winter Svalbard Ptarmigan loose more heat than adults. Plumage feather density (i.e., feathers × cm
−2
) and mass density (i.e., mg feathers × cm
−2
) were higher in winter, particularly on the head and feet where individual feathers were also heavier, longer, and downier. Seasonal changes in other regions (back, tarsi) indicated acclimatisation primarily to resist physical wear and wind. First-winter and adult birds had similar feather densities. However, mass density in first-winter birds was significantly lower than in adults in all but one body region (back) because individual feathers weighed less. This can explain previous observations of higher heat loss rates in first-winter birds. Our study suggests that plumage acclimatisation contributes to optimising the winter phenotype of Svalbard Rock Ptarmigan, both through higher insulative capacity and by improved resistance to harsh weather. The extent of these adaptations may be determined by the time or energy available for feather growth, exemplified here by inferior insulation in first-winter birds.
The brain of diving mammals tolerates low oxygen conditions better than the brain of most terrestrial mammals. Previously, it has been demonstrated that the neurons in brain slices of the hooded seal ...(Cystophora cristata) withstand hypoxia longer than those of mouse, and also tolerate reduced glucose supply and high lactate concentrations. This tolerance appears to be accompanied by a shift in the oxidative energy metabolism to the astrocytes in the seal while in terrestrial mammals the aerobic energy production mainly takes place in neurons. Here, we used RNA-Seq to compare the effect of hypoxia and reoxygenation in vitro on brain slices from the visual cortex of hooded seals. We saw no general reduction of gene expression, suggesting that the response to hypoxia and reoxygenation is an actively regulated process. The treatments caused the preferential upregulation of genes related to inflammation, as found before e.g. in stroke studies using mammalian models. Gene ontology and KEGG pathway analyses showed a downregulation of genes involved in ion transport and other neuronal processes, indicative for a neuronal shutdown in response to a shortage of O2 supply. These differences may be interpreted in terms of an energy saving strategy in the seal's brain. We specifically analyzed the regulation of genes involved in energy metabolism. Hypoxia and reoxygenation caused a similar response, with upregulation of genes involved in glucose metabolism and downregulation of the components of the pyruvate dehydrogenase complex. We also observed upregulation of the monocarboxylate transporter Mct4, suggesting increased lactate efflux. Together, these data indicate that the seal brain responds to the hypoxic challenge by a relative increase in the anaerobic energy metabolism.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Many vertebrates are challenged by either chronic or acute episodes of low oxygen availability in their natural environments. Brain function is especially vulnerable to the effects of hypoxia and can ...be irreversibly impaired by even brief periods of low oxygen supply. This review describes recent research on physiological mechanisms that have evolved in certain vertebrate species to cope with brain hypoxia. Four model systems are considered: freshwater turtles that can survive for months trapped in frozen-over lakes, arctic ground squirrels that respire at extremely low rates during winter hibernation, seals and whales that undertake breath-hold dives lasting minutes to hours, and naked mole-rats that live in crowded burrows completely underground for their entire lives. These species exhibit remarkable specializations of brain physiology that adapt them for acute or chronic episodes of hypoxia. These specializations may be reactive in nature, involving modifications to the catastrophic sequelae of oxygen deprivation that occur in non-tolerant species, or preparatory in nature, preventing the activation of those sequelae altogether. Better understanding of the mechanisms used by these hypoxia-tolerant vertebrates will increase appreciation of how nervous systems are adapted for life in specific ecological niches as well as inform advances in therapy for neurological conditions such as stroke and epilepsy.
Regulation of mitochondrial oxidative phosphorylation is essential to match energy supply to changing cellular energy demands, and to cope with periods of hypoxia. Recent work implicates the ...circadian molecular clock in control of mitochondrial function and hypoxia sensing. Because diving mammals experience intermittent episodes of severe hypoxia, with diel patterning in dive depth and duration, it is interesting to consider circadian-mitochondrial interaction in this group. Here, we demonstrate that the hooded seal (Cystophora cristata), a deep-diving Arctic pinniped, shows strong daily patterning of diving behaviour in the wild. Cultures of hooded seal skin fibroblasts exhibit robust circadian oscillation of the core clock genes per2 and arntl. In liver tissue collected from captive hooded seals, expression of arntl was some 4-fold higher in the middle of the night than in the middle of the day. To explore the clock-mitochondria relationship, we measured the mitochondrial oxygen consumption in synchronized hooded seal skin fibroblasts and found a circadian variation in mitochondrial activity, with higher coupling efficiency of complex I coinciding with the trough of arntl expression. These results open the way for further studies of circadian-hypoxia interactions in pinnipeds during diving.
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