Absence of Selective Brain Cooling in Free‐Ranging Zebras in Their Natural Habitat

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The main determinant of deep brain temperature, measured in or near the hypothalamus, is the temperature of the arterial blood supplying the brain (Hayward and Baker, 1968). In most mammals, therefore, brain temperature changes in parallel with carotid blood temperature but, because of its high metabolic rate, exceeds the temperature of arterial blood by 0.2-0.5°C (Hayward and Baker, 1969). However, some mammals, particularly artiodactyls and felids, are able to lower brain temperature below carotid blood temperature, a process termed selective brain cooling (for reviews, see Jessen, 2001;Mitchell et al., 2002). In these mammals, selective brain cooling is facilitated by the carotid rete, a bilateral network of intertwining arteries in the main arterial supply to the brain, situated on either side of the pituitary body within cool venous lakes derived from veins draining the nasal mucosa (Gillilan, 1974;Simoens et al., 1987). Moderate exercise on a treadmill or exposure to heat in a laboratory uncouples brain and carotid blood temperatures, so that the gradient between brain and blood temperatures narrows until, at a threshold temperature of approximately 39°C, brain temperature equals carotid blood temperature (Baker, 1982;Kuhnen and Jessen, 1991;Kuhnen and Mercer, 1993). Beyond that threshold, brain temperature rises at a slower rate than does blood temperature, establishing selective brain cooling with a magnitude, at most, of about 1°C.In mammals that are free-living in their natural habitat and exposed to a variety of complex stressors, however, a similar tight thermal relationship between brain and arterial blood temperatures is apparently absent. In free-ranging antelope, selective brain cooling occurs within the normothermic range of body temperature, and only sporadically in response to high heat loads (Jessen et al., 1994;Mitchell et al., 1997;Fuller et al., 1999b;Maloney et al., 2002). During high-intensity exercise, when brain temperatures reach their highest levels, selective brain cooling is abolished. Indeed, for any given blood temperature, brain temperature is highly variable and unpredictable. Large-amplitude, transient deviations in brain temperature, independent of any changes in the temperature of arterial blood supplying the brain, have also been observed in several laboratory animals in response to non-thermal stimuli (Fuller et al., 1999a;Maloney et al., 2001). This variability arises because the efferent arm of the control mechanism We used implanted miniature data loggers to measure brain (in or near the hypothalamus) and carotid arterial blood temperatures at 5 min intervals in six free-ranging ostriches Struthio camelus in their natural habitat, for a period of up to 14 days. Carotid blood temperature exhibited a large amplitude (3.0-4.6°C) circadian rhythm, and was positively correlated with air temperature. During the day, brain temperature exceeded carotid blood temperature by approx. 0.4°C, but there were episodes when brain temperature was lowered below blood temperature. Selecti...

Section: Discussionmentioning

confidence: 59%

Variability in brain and arterial blood temperatures in free-ranging ostriches in their natural habitat

Fuller

Kamerman

Maloney

et al. 2003

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“…Also, unrestrained springbok in a 4·ha paddock maintained abdominal temperature between 37.5 and 41.0°C, despite being subjected to summer air temperatures varying between 16 and 39°C and high solar radiation, and water deprivation for 17 days (Hofmeyr and Louw, 1987). The amplitude of the nychthemeral rhythm of body temperature of other free-ranging African ungulates, including black wildebeest Connochaetes gnou (Jessen et al, 1994), eland (Fuller et al, 1999), zebra Equus burchelli (Fuller et al, 2000) and oryx Oryx gazella , was also not related to environmental thermal load. In other words, none of these African ungulates exhibited the wide swings in body temperature characterising adaptive heterothermy, an adaptation widely considered to be crucial for the survival of ungulates in arid-zone habitats.…”

Section: Discussionmentioning

confidence: 93%

“…Although earlier studies yielded valuable insights, recent investigations employing miniature data loggers (Fuller et al, 1999(Fuller et al, , 2000Jessen et al, 1994;Lehmer et al, 2003;Maloney et al, 2002;Mitchell et al, 1997;Mzilikazi and Lovegrove, 2004) or radiotelemetry (Ostrowski et al, 2003;Zervanos and Salsbury, 2003) to record body temperatures in free-living mammals have demonstrated the importance of studying thermoregulatory responses in the natural environment, where animals are subjected to complex stressors that alter their behaviour and thermoregulatory mechanisms. Indeed, no African ungulate studied so far, free-living in its natural habitat, has employed adaptive heterothermy (for a review, see Mitchell et al, 2002).…”

mentioning

confidence: 99%

A year in the thermal life of a free-ranging herd of springbokAntidorcas marsupialis

Fuller

Kamerman

Maloney

et al. 2005

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We used miniature data loggers implanted in the abdominal cavity to measure core body temperatures at 30·min intervals in eight (three males, five females) adult free-ranging springbok Antidorcas marsupialis in their natural habitat, over a period of 11-13 months. The animals were subjected to a nychthemeral range of air temperature that often exceeded 20°C, with an absolute minimum temperature of -6°C and a maximum of 34°C. Abdominal temperature exhibited a low amplitude (~1.2°C) nychthemeral rhythm, with a temperature peak near sunset and a trough shortly after sunrise. The amplitude of the nychthemeral rhythm of body temperature was not correlated with the 24·h range of air temperature. Although mean 24·h body temperatures were positively correlated with corresponding air temperatures, mean daily body temperature increased, on average, by only 0.02°C per 1°C increase in air temperature, so that it was only ~0.3°C higher in summer than in winter. Mean monthly body temperatures were strongly positively correlated with photoperiod and, in parallel with changes in the time of sunrise, the times at which the minimum and maximum body temperatures occurred were shifted ~1.2·h earlier in summer than in winter. Annual and daily variations in body temperature of springbok, like those of other free-living African ungulates, therefore appear to reflect an endogenous rhythm, entrained by the light:dark cycle, but largely independent of fluctuations in the environmental thermal load. Springbok exhibit remarkable homeothermy and do not employ adaptive heterothermy to survive in their natural environment.

“…Conversely, as flapping flight is sustained in migrating bar-headed geese (Hawkes et al, 2011), heat and CO 2 will be added to capillary blood in the tissues, making the blood-O 2 equilibrium curve measured at 44°C and 7% CO 2 a reasonable estimate for blood in vessels draining locomotory muscle. Such values are not exceptional for animals during exercise (Bayly et al, 1989;Fuller et al, 2000;Irving, 1959;Mitchell et al, 2006;SchmidtNielsen et al, 1957;Taylor et al, 1998). Using the blood-O 2 equilibrium curve associated with cold, hypocapnic blood (as might be found in the lung) and warm, hypercapnic blood (as might be found in exercising muscle) to calculate arterial and venous O 2 contents, respectively, potential temperature-and pH-induced increases in O 2 loading and unloading were estimated at each altitude.…”

Section: Discussionmentioning

confidence: 99%

High thermal sensitivity of blood enhances oxygen delivery in the high-flying bar-headed goose

Meir

Milsom

2013

SUMMARYThe bar-headed goose (Anser indicus) crosses the Himalaya twice a year at altitudes where oxygen (O 2 ) levels are less than half those at sea level and temperatures are below −20°C. Although it has been known for over three decades that the major hemoglobin (Hb) component of bar-headed geese has an increased affinity for O 2 , enhancing O 2 uptake, the effects of temperature and interactions between temperature and pH on bar-headed goose Hb-O 2 affinity have not previously been determined. An increase in breathing of the hypoxic and extremely cold air experienced by a bar-headed goose at altitude (due to the enhanced hypoxic ventilatory response in this species) could result in both reduced temperature and reduced levels of CO 2 at the blood-gas interface in the lungs, enhancing O 2 loading. In addition, given the strenuous nature of flapping flight, particularly in thin air, blood leaving the exercising muscle should be warm and acidotic, facilitating O 2 unloading. To explore the possibility that features of blood biochemistry in this species could further enhance O 2 delivery, we determined the P 50 (the partial pressure of O 2 at which Hb is 50% saturated) of whole blood from bar-headed geese under conditions of varying temperature and [CO 2 ]. We found that blood-O 2 affinity was highly temperature sensitive in bar-headed geese compared with other birds and mammals. Based on our analysis, temperature and pH effects acting on blood-O 2 affinity (cold alkalotic lungs and warm acidotic muscle) could increase O 2 delivery by twofold during sustained flapping flight at high altitudes compared with what would be delivered by blood at constant temperature and pH.