The relationship between hypoxia exposure and circulating cortisol levels in social and solitary African mole-rats: An initial report.

Hypoxemia from exposure to intermittent and/or acute environmental hypoxia (lower oxygen concentration) is a severe stressor for many animal species. The response to hypoxia of the hypothalamic-pituitary-adrenal axis (HPA-axis), which culminates in the release of glucocorticoids, has been well-studied in hypoxia-intolerant surface-dwelling mammals. Several group-living (social) subterranean species, including most African mole-rats, are hypoxia-tolerant, likely due to regular exposure to intermittent hypoxia in their underground burrows. Conversely, solitary mole-rat species, lack many adaptive mechanisms, making them less hypoxia-tolerant than the social genera. To date, the release of glucocorticoids in response to hypoxia has not been measured in hypoxia-tolerant mammalian species. Consequently, this study exposed three social African mole-rat species and two solitary mole-rat species to normoxia, or acute hypoxia and then measured their respective plasma glucocorticoid (cortisol) concentrations. Social mole-rats had lower plasma cortisol concentrations under normoxia than the solitary genera. Furthermore, individuals of all three of the social mole-rat species exhibited significantly increased plasma cortisol concentrations after hypoxia, similar to those of hypoxia-intolerant surface-dwelling species. By contrast, individuals of the two solitary species had a reduced plasma cortisol response to acute hypoxia, possibly due to increased plasma cortisol under normoxia. If placed in perspective with other closely related surface-dwelling species, the regular exposure of the social African mole-rats to hypoxia may have reduced the basal levels of the components for the adaptive mechanisms associated with hypoxia exposure, including circulating cortisol levels. Similarly, the influence of body mass on plasma cortisol levels cannot be ignored. This study demonstrates that both hypoxia-tolerant rodents and hypoxia-intolerant terrestrial laboratory-bred rodents may possess similar HPA-axis responses from exposure to hypoxia. Further research is required to confirm the results from this pilot study and to further confirm how the cortisol concentrations may influence responses to hypoxia in African mole-rats.

The hypoxia tolerance of eight related African mole-rat species rivals that of naked mole-rats, despite divergent ventilatory and metabolic strategies in severe hypoxia.

AIMS: Burrowing mammals tend to be more hypoxia tolerant than non-burrowing mammals and rely less on increases in ventilation and more on decreases in metabolic rate to tolerate hypoxia. Naked mole-rats (Heterocephalus glaber, NMRs), eusocial mammals that live in large colonies, are among the most hypoxia-tolerant mammals, and rely almost solely on decreases in metabolism with little change in ventilation during hypoxia. We hypothesized that the remarkable hypoxia tolerance of NMRs is an evolutionarily conserved trait derived from repeated exposure to severe hypoxia owing to their burrow environment and eusocial colony organization. METHODS: We used whole-body plethysmography and indirect calorimetry to measure the hypoxic ventilatory and metabolic responses of eight mole-rat species closely related to the NMR. RESULTS: We found that all eight species examined had a strong tolerance to hypoxia, with most species tolerating 3 kPa O2 , Heliophobius emini tolerating 2 kPa O2 and Bathyergus suillus tolerating 5 kPa O2 . All species examined employed a combination of increases in ventilation and decreases in metabolism in hypoxia, a response midway between that of the NMR and that of other fossorial species (larger ventilatory responses, lesser reductions in metabolism). We found that eusociality is not fundamental to the physiological response to hypoxia of NMRs as Fukomys damarensis, another eusocial species, was among this group. CONCLUSIONS: Our data suggest that, while the NMR is unique in the pattern of their physiological response to hypoxia, eight closely related mole-rat species share the ability to tolerate hypoxia like the current "hypoxia-tolerant champion," the NMR.

Divergent behavioural responses to acute hypoxia between individuals and groups of naked mole rats.

Most small rodents reduce energy demand in hypoxia via behavioural strategies. For example, animals may reduce their activity, and/or move to colder environments or alter huddling strategies to take advantage of anapyretical energy savings. Naked mole rats (NMRs) are among the most hypoxia tolerant mammals and are highly social; social interactions also have a significant impact on behaviour. Therefore, this species offers a fascinating model in which to study trade-offs between social interactions and energy conservation in hypoxia. We hypothesized that the need to conserve energy in hypoxia supersedes the impetus of sociality in this species and predicted that, in hypoxia, behaviour would not differ between individuals or groups of NMRs. To test this hypothesis, we placed awake, freely behaving NMRs, alone or in groups of 2 or 4, into a temperature-controlled apparatus and measured behavioural activity during 1 h each of normoxia (21% O2), acute hypoxia (7% O2), and normoxic recovery. We found that in normoxia, groups of 4 NMRs were significantly more active in all temperatures than were groups of 1-2 NMRs. When exposed to hypoxia, individual NMRs were ~50% less active and their speed was reduced relative to normoxic levels. Conversely, groups of 2 or 4 NMRs exhibited minor or insignificant decreases in time spent active and speed in hypoxia and huddling behaviour was not altered. Our findings suggest that social interactions influence behavioural strategies employed by NMRs in hypoxia.

Behavioural responses of naked mole rats to acute hypoxia and anoxia.

Naked mole rats (NMRs) are among the most hypoxia-tolerant mammals. Other species respond to hypoxia by either escaping the hypoxic environment or drastically decreasing behavioural activity and body temperature (Tb) to conserve energy. However, NMRs rarely leave their underground burrows, which are putatively hypoxic and thermally stable near the NMRs' preferred Tb Therefore, we asked whether NMRs are able to employ behavioural and thermoregulatory strategies in response to hypoxia despite their need to remain active and the minimal thermal scope in their burrows. We exposed NMRs to progressively deeper levels of hypoxia (from 21 to 0% O2) while measuring their behaviour and Tb Behavioural activity decreased 40-60% in hypoxia and Tb decreased slightly in moderate hypoxia (5-9%) and then further with deeper hypoxia (3% O2). However, even at 3% O2 NMRs remained somewhat active and warm, and continued to explore their environment. Remarkably, NMRs were active for greater than 90 s in acute anoxia and Tb and metabolic rate decreased rapidly. We conclude that NMRs are adapted to remain awake and functional even at the extremes of their hypoxia-tolerance. This adaptation likely reflects variable and challenging levels of environmental hypoxia in the natural habitat of this species.