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Mole-rats from higher altitudes have greater thermoregulatory capabilities
Abstract
Subterranean mammals (those that live and forage underground) inhabit a challenging microenvironment, with high levels of carbon dioxide and low levels of oxygen. Consequently, they have evolved specialised morphological and physiological adaptations. For small mammals that inhabit high altitudes, the effects of cold are compounded by low oxygen partial pressures. Hence, subterranean mammals living at high altitudes are faced with a uniquely demanding physiological environment, which presumably necessitates additional physiological adjustments. We examined the thermoregulatory capabilities of two populations of Lesotho mole-rat Cryptomys hottentotus mahali that inhabit a 'low' (1600 m) and a 'high' (3200 m) altitude. Mole-rats from the high altitude had a lower temperature of the lower critical point, a broader thermoneutral zone, a lower thermal conductance and greater regulatory non-shivering thermogenesis than animals from the lower altitude. However, minimum resting metabolic rate values were not significantly different between the populations and were low compared with allometric predictions. We suggest that thermoregulatory costs may in part be met by animals maintaining a low resting metabolic rate. High-altitude animals may adjust to their cooler, more oxygen-deficient environment by having an increased non-shivering thermogenesis whilst maintaining low thermal conductance.
... Individuals of the same species that inhabit grasslands at 3200 ma.s.l. showed a higher metabolic rate increase (~3.6 times) than low-elevation counterparts (Broekman et al., 2006). The increase in metabolism was also high (3.5 times) in the naked mole-rat Heterocephalus glaber, a species from the arid Afrotropics. ...
... As proposed earlier, increases in NST affect thermal balance in mole-rats (Haim & Fairall, 1986;Woodley & Buffenstein, 2002;Broekman et al., 2006). Hislop & Buffenstein (1994) evaluated NST in the naked mole-rat H. glaber and the Damaraland mole-rat F. damarensis and established its effect on T b . ...
... This difference may be associated with the relatively higher heat loss in H. glaber due to the absence of fur and its relatively high surface to volume ratio (Hislop & Buffenstein, 1994). Moreover, Broekman et al., (2006) found that high-elevation populations of C. h. mahali exhibited higher NST and higher T b compared to their low-altitude counterparts (3.23 mL O 2 g −1 h −1 vs. 2.16 mL O 2 g − 1 h −1 and 38.2°C vs. 36.1°C, ...
Many mammalian species are adapted to living in burrows for most of their lives. Inhabiting such thermally stable environments may influence the variation on the species thermogenic capacity, particularly non‐shivering thermogenesis (NST). African mole‐rats (Bathyergidae) are subterranean rodents occurring in fynbos, grassland and wooded savannas across sub‐Saharan Africa that vary in the complexity of their social systems, ranging from strictly solitary to highly social species. The presence and magnitude of NST are well known in social bathyergids, but no such data exist for their solitary counterparts. In this study, we quantified NST in three solitary mole‐rat species represented by three distinct genera together with one social species. Our results showed that NST in all species is functional. Maximum metabolic rate after norepinephrine injection was equivalent to 269% of resting values in the social giant mole‐rat Fukomys mechowii and 166%, 282% and 157% in the three solitary species: the silvery mole‐rat Heliophobius argenteocinereus, the Cape mole‐rat Georychus capensis and the Cape dune mole‐rat Bathyergus suillus, respectively. To test our prediction that NST capacity is higher in solitary bathyergids, we combined our data with those available for other members of this family. In contrast to our prediction, NST did not differ between social and solitary bathyergids. Body mass, as the main factor, and minimum air temperature (Tmin), accounts for more than 80% of NST variation in bathyergid mole‐rats.
... mahali from areas with larger differences in altitudes, 1600 vs. 3200 m a.s.l. (Broekman et al., 2006). The explanation regarding colder microenvironments at higher altitudes seems to be more plausible, especially if we consider that mole-rats from higher altitudes might face higher T a fluctuations, also due to the fact that nests are probably shallower because of the relatively thin layer of soil which is typical for mountain ecosystems (cf. ...
... mahali living at 3200 m a.s.l. Their TNZ was wider and with lower LCT than a population from a lower altitude (Broekman et al., 2006). This together with lower thermal conductance and greater thermogenic capacity (see below), while keeping the same RMR, is probably an adaptation for life in colder T a . ...
... Mole-rat responses to T a below the TNZ can also be very different between populations of the same species. In addition to the different TNZ, LCT and C, Broekman et al. (2006) found that metabolic rates in C. h. mahali far below the LCT (T a = 5°C) increased five times in individuals from low altitudes, but only twice in those from higher altitudes indicating better adaptation to cold in later ones. ...
... Zhao and his colleague (2010) argued that this species had seasonal fluctuations in metabolic rate and thermal conductance, by which narrower TNZ with higher upper critical temperature in summer enabled hamsters to survive the hot weather, and wider TNZ with higher metabolic thermogenesis likely increased the capacity to cope with cold winter [14,17]. It has been also reported that other animals living cold conditions have relatively low lower critical temperatures and show extremely wide TNZ than those from warm conditions [18][19][20]. This may indicate that a shift of TNZ occurs due to the changes in T a , suggesting a potential role of T a . ...
... A classic study on thermoneutrality performed by Scholander and his colleague showed that animals living in the arctic had very low lower critical temperatures and an extremely wide TNZ [18,20]. Lesotho mole-rat (Cryptomys hottentotus mahali) from the cold temperature at high altitude had a lower temperature of the lower critical point and a broader TNZ than animals from the lower altitude [19]. These results suggest that the thermoneutrality of an animal is possibly affected by T a . ...
... In addition, within TNZ coldacclimated hamsters showed higher metabolic rate and thermogenesis than those acclimated to hot condition. Similar results have been previously reported in seasonal acclimated striped hamsters [14][15][16][17] and other wild small mammals, as well as in laboratory rodents [13,[19][20][21]28,32,39,41,[54][55][56][57]. ...
Temperature affects all biological functions and will therefore modulate ecologically significant interactions between animals and their environment. Here, we examined the effect of ambient temperature (Ta) on the thermal biology and energy budget in striped hamsters acclimated to cold (5°C), warm (21°C) and hot temperatures (31°C). Thermoneutral zone (TNZ) was 22.5-32.5°C, 25-32.5°C and 30-32.5°C in the cold-, warm- and hot-acclimated hamsters, respectively. The cold acclimation decreased the lower critical temperature and made the TNZ wider, and hot exposure elevated the lower critical temperature, resulting in a narrow TNZ. Within the TNZ, cold-acclimated hamsters showed a significantly higher rate of metabolism and thermogenesis than those acclimated to hot temperature. Digestive enzymes activities, including intestinal sucrase, maltase, L-alanine aminopeptidase-N and leucine aminopeptidase were higher in the cold than in the hot. The changes in metabolic rate and thermogenesis at different temperatures were in parallel with cytochrome c oxidase activity and uncoupling protein 1 gene expression of brown adipose tissue. This suggests that the shift of the lower critical temperature of TNZ is possibly associated with the rate of metabolism and thermogenesis, as well as with the digestive capacity of the gastrointestinal tract at different Ta. The upper critical temperature of TNZ may be independent of the changes in Ta. The changes of lower critical temperature of TNZ are an important strategy in adaption to variations of Ta.
... Living underground offers thermal buffering to extreme temperature fluctuations with burrow depth varying with species ). Soil properties and food availability likely explain why tunnels are constructed at specific depths (Broekman et al. 2006, Lövy et al. 2015. The depth of tunnels and the nests are greatest for mole-rats inhabiting arid regions with sandy soils, like the Damaraland mole-rat (Fukomys damarensis), where foraging tunnels are between 30 -40 cm below ground, and nests may exceed 2 m in depth Painting 1987, Bennett et al. 1988). ...
... Natal mole-rats are among the few heterothermic mammals, exhibiting the lowest body temperatures of bathyergids, the narrowest thermal neutral zone, and one of the highest resting metabolic rates in bathyergids (Bennett et al. 1993c, Šumbera 2019, Oosthuizen et al. 2021). The thermal neutral zone of bathyergids may increase at higher altitudes, and a lower body temperature has been suggested to be an adaptation to colder environments, enabling animals to expend less energy maintaining their body temperature at lower ambient temperatures (Broekman et al. 2006). I found that soil temperatures in foraging tunnels vary between 5°C or 30°C below their thermal neutral zone during summer and winter, respectively, and these physiological adaptations may be an evolutionary response to shallow tunnels and the resultant seasonal climate fluctuations they experience. ...
The Natal mole-rat (Cryptomys hottentotus natalensis) is a social subspecies of African mole-rat related to the common mole-rat (Cryptomys hottentotus hottentotus). They inhabit mesic grassland in eastern South Africa from coastal regions to well over 2000m elevation. There have been a few studies on their physiology and reproductive suppression, but their ecology and life history has not been reported in detail. This study used capture-mark recapture methods to investigate life history, population demographics, behaviour, and gene flow in wild Natal mole-rats living at a high elevation site in the southern Drakensberg Mountains. I captured a total of 403 individuals across 52 family groups. Individuals were weighed, measured, sexed, and assigned a reproductive status on capture. Tissue samples were collected for genetic analysis and then they were implanted with a passive integrated transponder for identification at recapture. Groups were captured every six months over the course of 2 years.
Both environmental factors and population demographics can have far reaching effects on individual life history, including altering spatial arrangement, behaviour, body condition, and fecundity rates. I found that Natal mole-rats have reduced group sizes (mean 6) compared to the more arid dwelling African mole-rat species. Population wide sex ratios were evenly split between males and females. However, within-group adult sex ratios were skewed towards males, and this skew became more pronounced in larger groups. Sex ratios, group size, and group biomass did not show any seasonal differences. Small litter sizes (1.3), slow population growth rates (0.17), long maturation time (1.2 years) of females indicate a “slow” life history. I found strong sexual dimorphism, with males being larger than females. Male exhibited a faster growth rate compared to females, but growth rates were not affected by group size. This indicates that within-group competition is reduced or absent, likely due to the smaller mean group size or increased availability of food resources. Individual body condition varied between seasons and was affected by group size. During summer body condition increased with increasing group size, highlighting the benefits of collective foraging. But during winter body condition decreased with increasing group size, likely due to low quality of food and a necessity to continue foraging through winter. Interestingly, the body condition in reproductive females increased with group size during winter, when all others decreased. However, their fecundity did not appear to be affected by group size. The expected benefits of helping effects from larger groups may be reduced in Natal mole-rats.
Observations on subterranean mammals suggest that they exhibit diel rhythms despite the lack of visual cues in their underground burrows, but it is unknown how ambient temperature, photoperiod, or individual characteristics affects their activity. I used RFID technology to monitor daily activity patterns of wild mole-rats during the summer and winter seasons. I combined the activity data with satellite climate data to investigate how their activity patterns vary between seasons and whether their activity depends on individual characteristics such as body mass, sex and reproductive status. Individual characteristics, including reproductive status, did not affect general activity. This result suggests that reproductive and non-reproductive individuals contribute equally to cooperative behaviours unlike other mole-rats where reproductive individuals exhibit reduced contributions. I found that in winter, individuals were more active during mid-day to coincide with higher soil temperatures, whereas in summer, they showed a bimodal activity pattern during early morning and late afternoon coinciding with cooler soil temperatures. Activity patterns are therefore a behavioural adaptation to avoid extreme burrow temperatures and a mechanism to maintain a stable core body temperature. Thermoregulatory behavioural adaptations appear to be more important than differences in cooperative contributions to Natal mole-rats.
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I extracted DNA from tissue samples and then used custom designed microsatellite markers to assess spatial grouping and gene flow in the population. Population-level analyses, such as FST, focus on genetic relatedness among social groupings, while relatedness coefficients determine relatedness between individuals in the population. I found that pairwise-relatedness coefficients were surprisingly similar to the arid dwelling Damaraland mole-rat (Fukomys damarensis) in the southern Kalahari, despite assumptions that higher rainfall would provide more dispersal opportunities and higher immigration rates. Population level FST values indicated the presence of male-biased dispersal. Relatedly, females were more related to females in neighbouring family groups than males. The study site had three landscape features which may act as dispersal barriers, such as a road, a river, and a steep rocky hillside. A non-spatial Bayesian clustering analysis determined that these features did not pose major dispersal barriers to mole-rats. I estimated dispersal distances to be between 350 – 400m, with males having slightly higher dispersal distances compared to females. There was no evidence of isolation by distance, and gene flow is well maintained within the study site.
In conclusion this study found that Natal mole-rats continue to exhibit delayed dispersal and high levels of within-group relatedness despite increased annual rainfall. Their life history and physiological adaptations allow them to cope with living in an environment with extreme seasonal fluctuations. With the projected increased ambient temperatures due to climate change, mole-rats living at higher altitude may not cope well with very minor deviations from the conditions they have adapted to. I found that body mass appeared reduced compared to 20 years ago, and this decrease may be due to climate change or habitat alteration. The evolution of various physiological traits unique to Natal mole-rats means they may be more susceptible to the effects of climate change than other subterranean rodents. Previous labelling of Natal mole-rats as “less social” should be avoided and there is evidence to support the claim that they are singular cooperative breeders.
... Living underground offers thermal buffering to extreme temperature fluctuations with burrow depth varying with species (Bennett et al., 1988). Soil properties and food availability likely explain why tunnels are constructed at specific depths (Broekman et al., 2006;Lövy et al., 2015). The depth of tunnels and the nests are greatest for mole-rats inhabiting arid regions with sandy soils, where foraging tunnels are between 30 and 40 cm below ground, and nests may exceed 2 m in depth (Lovegrove and Painting, 1987;Bennett et al., 1988). ...
... Natal mole-rats are among the few heterothermic mammals, exhibiting the lowest body temperatures of bathyergids, the narrowest thermal neutral zone, and one of the highest resting metabolic rates in bathyergids (Bennett et al., 1993b;Šumbera, 2019;Oosthuizen et al., 2021). However, the thermal neutral zone of bathyergids may increase at higher altitudes, and a lower body temperature has been suggested to be an adaptation to colder environments, enabling animals to expend less energy maintaining their body temperature at lower ambient temperatures (Broekman et al., 2006). We found that soil temperatures in foraging tunnels vary between 5 and 30 • C below their thermal neutral zone during summer and winter, respectively, and these physiological adaptations may be an evolutionary response to shallow tunnels and the resultant seasonal climate fluctuations they experience. ...
Differences in individual locomotor activity patterns may be linked to a number of ecological factors, such as changes in ambient temperature or photoperiod. Observations on subterranean mammals suggest that they exhibit diel rhythms despite the lack of visual cues in their underground burrows, but it is unknown how seasonality and individual characteristics affect their activity. In this study we use RFID technology to monitor daily activity patterns of wild, social Natal mole-rats (Cryptomys hottentotus natalensis) during the summer and winter to investigate how their activity varies with season and whether their activity depends on individual characteristics such as body mass, sex and reproductive status. We found that in winter, individuals were more active during the time with the highest soil temperatures, whereas in summer, they showed a bimodal activity pattern during early morning and late afternoon coinciding with cooler soil temperatures. Individual characteristics, including reproductive status, did not affect general activity indicating that reproductive and non-reproductive individuals contribute equally to cooperative behaviors. We suggest that the activity patterns may be a behavioral adaptation to avoid extreme burrow temperatures and a mechanism to maintain a stable core body temperature. We highlight the advantages of RFID technology to study wild small mammal movements.
... The study of the subterranean family, the Bathyergidae (African mole-rats), has allowed for many essential revelations in mammalian evolution, behaviour, and physiology (Bennett and Faulkes 2000;Sherman et al. 2017). Furthermore, this family provides an important study system for the better understanding of how mammals adapt behaviourally, physiologically, and molecularly to their inhibiting environment (Broekman et al. 2006;Eigenbrod et al. 2019;Ivy et al. 2020;Logan et al. 2020;McGowan et al. 2020;Barker et al. 2021). ...
... The Mahali mole-rat shares a close genetic relatedness (Faulkes et al. 2004;Broekman et al. 2006) and a close distributional range, as well as similar climatic conditions, with those of the highveld mole-rat, except that in the former subspecies temperature is, on average, 5°C warmer and the area has 10% less humidity throughout the year (van Jaarsveld et al. 2019;Fagir et al. 2021;Wallace et al. 2021). The Mahali and highveld mole-rats experience distinct seasonal climates with wet, warm summers and cool, dry winters throughout their distributional range. ...
African mole-rats have provided great insight into mammalian evolution of sociality and reproductive strategy. However, some species have not received attention, and these may provide further insights into these evolutionary questions. The cooperatively breeding Mahali mole-rat (Cryptomys hottentotus mahali (Roberts, 1913)) is one such species. Body mass, reproductive-tract morphometrics, gonad histology, and plasma reproductive hormone concentrations were studied for breeding and non-breeding males and females over 1 year. This study aimed to discern if this species exhibits a seasonal or aseasonal breeding pattern and whether there is a relaxation of reproductive suppression at any point in the year in non-breeding animals. The pattern of reproductive relaxation during the wetter months is similar to other African mole-rat species. Interestingly, births and pregnant breeding females were recorded throughout the year, thus indicating an aseasonal breeding strategy, despite inhabiting a region that experiences seasonal rainfall. However, there were periods of the year favouring increased reproduction to enable an increased likelihood of offspring survival. This suggests that the Mahali mole-rat may be an opportunistic breeder possibly brought about by the benefits of living in a cooperatively breeding group and potentially moving into more arid environments that were previously unexploited by the genus Cryptomys Gray, 1864.
... Physiological adaptations can thus be expected to be highly distinctive. It has been reported that animals living under cold conditions have relatively lower critical temperatures and show a wider TNZ than those adapted to warmer conditions (Broekman et al., 2006;Zhao et al., 2014). Also, it has been proposed that insulative properties of the body and metabolic thermogenesis are involved in the shift of the TNZ in order to cope with cold stress (Broekman et al., 2006;Zhao et al., 2010b;a, 2014). ...
... It has been reported that animals living under cold conditions have relatively lower critical temperatures and show a wider TNZ than those adapted to warmer conditions (Broekman et al., 2006;Zhao et al., 2014). Also, it has been proposed that insulative properties of the body and metabolic thermogenesis are involved in the shift of the TNZ in order to cope with cold stress (Broekman et al., 2006;Zhao et al., 2010b;a, 2014). Consistent with these predictions, the thermal insulation of the snow vole's body was shown to be much better than that of the common vole (Microtus arvalis), a typical lowland rodent of the same family (Bienkowski & Marszalek, 1974). ...
Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass‐independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long‐term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni‐ and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass‐dependent and mass‐independent components, while accounting for measurement error. RMR varies among individuals, i.e. is repeatable (R=0.46), and strongly co‐varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass‐independent RMR is reduced by 41% to R=0.27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error, and decompose the relative importance of mass‐dependent and mass‐independent physiological variation.
... In adult deer-mice that have been captured at high altitude and thereafter maintained at low altitude for 6 weeks, the thermogenic capacity measured as maximum O2 consumption induced by cold exposure under hypoxia was about 60% higher than in lowland deer-mice (Cheviron et al., 2012), but it seems that this effect is determined by genetics rather than by development at high altitude. In high-altitude mole-rats (3,200m) the thermogenic response to cold exposure was less important than in low-altitude control mole-rats (Broekman et al., 2006), but high-altitude animals had lower thermal conductance (higher isolation or efficient behavioral response to limit heat loss during cold exposure), and their response to stimulation of non-shivering thermogensis by noradrenaline was more important (higher increased of metabolic rate and body temperature), showing overall greater thermoregulatory capabilities (Broekman et al., 2006). ...
... In adult deer-mice that have been captured at high altitude and thereafter maintained at low altitude for 6 weeks, the thermogenic capacity measured as maximum O2 consumption induced by cold exposure under hypoxia was about 60% higher than in lowland deer-mice (Cheviron et al., 2012), but it seems that this effect is determined by genetics rather than by development at high altitude. In high-altitude mole-rats (3,200m) the thermogenic response to cold exposure was less important than in low-altitude control mole-rats (Broekman et al., 2006), but high-altitude animals had lower thermal conductance (higher isolation or efficient behavioral response to limit heat loss during cold exposure), and their response to stimulation of non-shivering thermogensis by noradrenaline was more important (higher increased of metabolic rate and body temperature), showing overall greater thermoregulatory capabilities (Broekman et al., 2006). ...
High altitude is a challenging environment mostly characterized by a low pressure of oxygen but also by cold temperatures, air dryness, reduced protection against exposure to solar radiations, and more limited resources than at lower altitudes. During postnatal development, energy requirements are elevated, and reduction of oxygen supply (hypoxia) during this period has profound physiological consequences. Different models of exposure to hypoxia in newborn mammals have been used over the years and have helped to establish the effects of hypoxia during development on the cardiorespiratory system. Exposure to hypoxia during postnatal development has long-term consequences that manifest throughout the life span. These consequences of neonatal hypoxia might help the adults to better withstand the effects of the reduced oxygen pressure or on the contrary impair the subsequent responses to hypoxia. Most experimental research on development at high altitude focuses on the hypoxic environment, and the cardiorespiratory system, while only few data are available concerning thermoregulatory processes, and the interactions between cold and hypoxia during postnatal development at high altitude. In summary developmental hypoxia determines the ability of adult mammals to withstand life at high altitude, and the available data indicate that this might be an important driving force in short-term acclimatization and long-term adaptation to high altitude. Developmental physiology at high altitude should therefore be considered as a central element for physiology and adaptation to this specific environment.
... Mashona mole-rats (Fukomys darling) have also been shown to show greater heterothermy at lower T a 's, and T b can reduce significantly at T a below 25˚C, while this appears not to be the case for the highveld mole-rat [28,29]. Social mole-rat species employ behavioural thermoregulation to regulate body temperatures; they select deeper, warmer areas of the burrows for resting [30] and also huddle together to conserve heat [31,32]. ...
... A reduction in activity levels when the ambient temperature approaches the thermoneutral zone (TNZ) has also been reported for other species such as laboratory mice [41]. In social mole-rat species, the TNZ's typically range between 28-36˚C [6,29,32,42,43]. The TNZ of the highveld mole-rat is around 30-32˚C [44], thus 30˚C falls within this zone. ...
African mole-rats are strictly subterranean mammals that live in extensive burrow systems. High humidity levels in the burrows prevent mole-rats from thermoregulating using evaporative cooling. However, the relatively stable environment of the burrows promotes moderate temperatures and small daily temperature fluctuations. Mole-rats therefore display a relatively wide range of thermoregulation abilities. Some species cannot maintain their body temperatures at a constant level, whereas others employ behavioural thermoregulation. Here we test the effect of ambient temperature on locomotor activity and body temperature, and the relationship between the two parameters, in the highveld mole-rat. We exposed mole-rats to a 12L:12D and a DD light cycle at ambient temperatures of 30°C, 25°C and 20°C while locomotor activity and body temperature were measured simultaneously. In addition, we investigated the endogenous rhythms of locomotor activity and body temperature at different ambient temperatures. Mole-rats displayed nocturnal activity at all three ambient temperatures and were most active at 20°C, but least active at 30°C. Body temperature was highest at 30°C and lowest at 20°C, and the daily cycle was highly correlated with locomotor activity. We show that the mole-rats have endogenous rhythms for both locomotor activity and body temperature. However, the endogenous body temperature rhythm appears to be less robust compared to the locomotor activity rhythm. Female mole-rats appear to be more sensitive to temperature changes than males, increased heterothermy is evident at lower ambient temperatures, whilst males show smaller variation in their body temperatures with changing ambient temperatures. Mole-rats may rely more heavily on behavioural thermoregulation as it is more energy efficient in an already challenging environment.
... The authors supposed that the lower RMR is a consequence of lower partial pressure of oxygen in the atmosphere at higher altitudes. Nevertheless, Broekman et al. (2006) described an inverse relation in two populations of Cryptomys hottentotus mahali. Mole-rats from higher altitudes had higher body mass (130%), higher RMR (130%) and broader TNZ compared to mole-rats from lower altitudes. ...
... Nevertheless, we do not expect any remarkable differences in food supply because both localities have a similar precipitation pattern which is supposed to be a main determinant of food supply in African mole-rats (Bennett and Faulkes, 2000). It seems that there is still great uncertainty concerning the relationship between body size and RMR of African mole-rats to altitude and ecological factors (see Broekman et al., 2006. This needs further study. ...
... These authors speculated that this social mole-rat is not able to disperse and colonise colder environments at higher altitudes. Nevertheless, the fact that some social mole-rats also live at higher altitudes (Broekman et al., 2006), or some individuals live also for a long time alone (even for years) (Thorley et al., 2021), indicates that there is no general explanation and this phenomenon in African mole-rats deserves further attention. Temperatures in mole-rat burrows rarely reach or exceed a lower critical temperature (see Š umbera 2019 for review), which indicates that some energy needs to be allocated for thermogenesis. ...
African mole-rats (Bathyergidae) are strictly subterranean rodents distributed in sub-Saharan Africa. Although the soil layer provides a temperature buffer, the temperature in their burrows is usually below their thermoneutral zone and thermogenesis is necessary to maintain a stable body temperature. In social bathyergids, an important mechanism for decreasing the thermoregulatory cost is social thermoregulation in the form of huddling. The effect of huddling may be of special importance during forming of a new family as only two adults are present and social species are known for higher heat losses from their bodies compared to solitary mole-rats.
In our study, we measured the resting metabolic rate and energetic saving in three social bathyergid species which differ in body size. We compared animals that were housed individually and in pairs at two different ambient temperatures (Ta). At a temperature within their TNZ (Ta = 30 °C), no energetic savings were expected, whereas in Ta = 20 °C we expected energetic savings due to huddling.
We found no energetic savings at 30 °C in any of the species, but almost 20% in the two small bodied Fukomys species F. micklemi and F. anselli at 20 °C. In the largest species, F. mechowii, no significant energetic savings were observed. Our results confirm the importance of huddling for the energetic balance of social mole-rats and show that huddling with one partner can bring substantial energetic savings, which can be allocated to other activities such as extension of established burrow systems or reproduction to increase the workforce and fulfill the purpose of dispersal.
... An increase in thermogenic capacity is recognized as being one of the most effective mechanisms in small mammals enabling them to cope with low temperatures (Heldmaier 1971;Jansky et al. 1973;Heldmaier et al. 1982a;Haim & Zisapel 1999;Nespolo et al. 2001;Cannon & Nedergaard 2011). Studies on small mammals have demonstrated that increases in RMRt and NST are more related to cold acclimation than insulative adaptations (Gordon 1993(Gordon , 2012Broekman et al. 2006). Elevated RMRt and NST in cold-acclimated small mammals have been linked to the metabolic rate of specific active organs and tissues (Johnson et al. 2001;Krόl et al. 2003Krόl et al. , 2005. ...
The thermoneutral zone (TNZ) reflects the adaptation of mammals to their natural habitat. However, it remains unclear how TNZ shifts in response to variations in ambient temperature. To test the hypothesis that ambient temperature plays a key role in determining TNZ variations between seasons, we measured metabolic rate, body temperature, and cytochrome c oxidase (COX) activity of several visceral organs in striped hamsters (Cricetulus barabensis) either acclimated to semi‐natural conditions over a year, or subjected to a gradual decrease in mean temperature from 30±1°C to ‐15±1°C. The TNZ range in striped hamsters differed seasonally, with a wider TNZ and a lower lower‐critical temperature in winter compared to summer. The hamsters showed a considerable leftward shift of lower‐critical temperature from 30°C to 20°C after the ambient temperature of acclimation from 30°C down to ‐15°C, whereas the upper‐critical temperature of TNZ remained fixed at 32.5°C. The resting metabolic rate in thermoneutral zone (RMRt), nonshivering thermogenesis (NST), and COX activity of brown adipose tissue (BAT), liver, skeletal muscle, brain, and kidneys, increased significantly in hamsters acclimated at lower ambient temperatures. Following acute exposure to 5°C and ‐15°C, hamsters acclimated to 32.5°C had significantly lower maximal NST and lower serum thyroid tri‐iodothyronine (T3) levels compared to those kept at 23°C. These findings suggest that acclimation to the upper‐critical temperature of TNZ impairs the hamsters’ thermogenic capacity to cope with extreme cold temperature. Reduced ambient temperature was mainly responsible for the leftward shift of TNZ in striped hamsters, which reflects the adaptation to cold environments. This article is protected by copyright. All rights reserved
... African mole-rats are ideally suited to conduct behavioural, physiologically, and molecularly comparative studies as species of the family Batherygidae inhabit a wide array of environments and possess varying social structures, yet share many similar environmental conditions (i.e. burrow conditions), resulting in an ideal model family to investigate various adaptive and evolutionary changes in response to their experienced environment (Logan et al., 2020;Ivy et al., 2019;Eigenbrod et al., 2019;Kotze et al., 2008;Broekman et al., 2006). ...
The effect of the macro- and microclimate on small mammal thermoregulation in the past has been studied independently instead of investigating the dual effect of both the components. This study addresses this dearth in knowledge by exploring the dual effect of both micro- and macro-climate on the thermoregulatory responses of two subterranean rodent species belonging to the family Bathyergidae, namely the more arid dwelling Mahali mole-rat (Cryptomys hottentotus mahali) and less arid dwelling Highveld mole-rat (C. h. pretoriae). Open flow through respirometry was used to quantify resting metabolic rates (RMR), evaporative water loss (EWL), core body temperature (Tb), the ratio between the evaporative heat loss and metabolic heat production (EHL/MHP: evaporative cooling capacity) and conductance (Cdry) over a range of increasing ambient temperatures (Ta; 20–42 °C). Furthermore, RMR, EWL, Tb, EHL/MHP and Cdry were measured at the mole-rat's thermal maxima (43 °C). At cooler temperatures, the arid-dwelling C. h. mahali possesses a broader thermoneutral zone (∼5 °C; 27.2–32.1 °C), while the C. h. pretoriae possess a single thermoneutral point (33.6 °C). This is in response to the greater selection pressure to conserve energy in the more arid regions inhabited by C. h. mahali. Contrastingly, at hotter temperatures, there were no significant thermoregulatory differences in EWL, EHL/MHP or Cdry responses between the two sub-species, as expected due to the limitations bestowed by the buffered microclimates (burrow systems). Thus, neither macro-climate, nor micro-climate singularly moulds the thermoregulatory adaptations, but rather, it appears to be a combined effect from both climates. Other small endotherms may share this dual response, and therefore, it is crucial to incorporate the effect of both macro- and microclimates into future climate models when determining the ecological capabilities and persistence of a species.
... Indeed, their high hypoxia tolerance may even facilitate species like C. h. mahali living at a range of altitudes (1600-3200 m) (Broekman et al., 2006). ...
Mole-rats are champions of self-preservation, with increased longevity compared to other rodents their size, strong antioxidant capabilities, and specialized defenses against endogenous oxidative stress. However, how the brains of these subterranean mammals handle acute in vivo hypoxia is poorly understood. This study is the first to examine the molecular response to low oxygen in six different species of hypoxia-tolerant mole-rats from sub-Saharan Africa. Protein carbonylation, a known marker of DNA damage (hydroxy-2'-deoxyguanosine), and antioxidant capacity did not change following hypoxia but HIF-1 protein levels increased significantly in the brains of two species. Nearly 30 miRNAs known to play roles in hypoxia-tolerance were differentially regulated in a species-specific manner. The miRNAs exhibiting the strongest response to low oxygen stress inhibit apoptosis and regulate neuroinflammation, likely providing neuroprotection. A principal component analysis using a subset of the molecular targets assessed herein revealed differences between control and hypoxic groups for two solitary species (Georychus capensis and Bathyergus suillus), which are ecologically adapted to a normoxic environment, suggesting a heightened sensitivity to hypoxia relative to species that may experience hypoxia more regularly in nature. By contrast, all molecular data were included in the PCA to detect a difference between control and hypoxic populations of eusocial Heterocephalus glaber, indicating they may require many lower-fold changes in signaling pathways to adapt to low oxygen settings. Finally, none of the Cryptomys hottentotus subspecies showed a statistical difference between control and hypoxic groups, presumably due to hypoxia-tolerance derived from environmental pressures associated with a subterranean and social lifestyle.
... Physiological phenotypes are often direct expressions of environmental and climate adaptation (Haim and Borut, 1981;Louw and Seely, 1982;Broekman et al., 2006). In regions where ambient temperature (T a ) is lower than core body temperature (T b ), heat production should be increased in homeotherms, whilst heat loss should be reduced in order to prevent hypothermia. ...
Individuals and populations possess physiological adaptations to survive local environmental conditions. To occur in different regions where ambient temperature varies, animals must adopt appropriate thermoregulatory mechanisms. Failure to adjust to environmental challenges may result in species distributional range shifts or decreased viability. African mole-rats (Bathyergidae) occupy various habitats in sub-Saharan Africa from deserts to montane regions to mesic coastal areas. We examined thermoregulatory characteristics of three African mole-rat species originating from disparate (montane, savannah, and arid/semi-arid) habitats. Animals were exposed to various ambient temperatures, whilst core body temperature and the surface temperature of different body parts were measured. Oxygen consumption was determined as a measure of heat production. Core body temperatures of Natal (montane) mole-rats (Cryptomys hottentotus natalensis) increased significantly at ambient temperatures >24.5 °C, while those of the highveld (Cryptomys hottentotus pretoriae) (savannah) and Damaraland (Fukomys damarensis) (arid/semi-arid) mole-rats remained within narrower ranges. In terms of surface temperature variation, while pedal surfaces were important in regulating heat loss in Natal and Damaraland mole-rats at high ambient temperatures, the ventral surface was important for heat dissipation in Damaraland and highveld mole-rats. This study provides evidence of the variation and limitations of thermo-physiological mechanisms for three mole-rat species relative to their habitats. Information on physiological adaptations to particular habitats may inform predictive modelling of species movements, declines, and extinctions in response to a changing environment, such as climate change.
... On the other hand, our results show that capybaras seem to avoid waterlogged areas, preferring dry rocky areas, differently from what we would expect based on its lowland behaviour (Moreira et al. 2012a). In highlands, mammals, and more specifically rodents, may present differences in their physiology in response to the harsh conditions they find in these environments, and that may be reflected in their behaviour and ecology (Hammond et al. 2001;Broekman et al. 2006). In INP, both waterlogged and dry rocky areas have the resources (permanent water bodies and grassland) that capybaras require (Aximoff and Ribeiro 2012;Corriale and Herrera 2014), and although these areas consist of an association of flooded reeds and sedges (Safford 1999), lacking a sufficiently firm surface for an animal of the capybara's size (35-65 kg; Paglia et al. 2012), we would expect that capybaras use the waterlogged areas more, since they easily move through the water (Quintana 1999). ...
The capybara Hydrochoerus hydrochaeris is one of the largest and most widely distributed herbivores in the Neotropical lowlands. However, as yet, there are no records of its occurrence in highland environments. Our aim was to evaluate the environmental variables related to the capybara’s distribution and monitor the effects of its herbivory on the individuals and on the reproductive phenology of A. polyanthus, a common and important plant species of the high-altitude grasslands. Our results show that capybaras frequently occur in the high-altitude grasslands along the Campo Belo River, but they avoid waterlogged areas, occurring more frequently on the dry rocky areas. Capybara herbivory affected the number of A. polyanthus rosettes in flower, leading to the presence of inflorescence formation anomalies. High-altitude grasslands apparently provide capybaras with the three main components (food, shelter and water) required for their occurrence. However, although they seem to present a seasonal feeding strategy, which also happens in lowlands, their avoidance of the waterlogged areas suggests that in highlands the species may present different environmental preferences from those presented in lowlands. In addition, the impact of capybaras’ herbivory on A. polyanthus individuals indicates the potential impact that capybaras can represent on the plant community of the high-altitude grasslands. This appears to be a great opportunity to study the effect of the arrival of a large herbivore in a new environment and possible impacts on plant assemblages.
... Mole-rats are physiologically well adapted towards their lifestyle (Bennett & Faulkes, 2000), exhibiting substantially lower body temperatures and metabolic rates as well as higher thermal conductances when compared with surface dwelling rodents (Lovegrove, 1987;Bennett, Jarvis & Cotterill, 1993a;Bennett et al., 1994;Bennett, Cotterill & Spinks, 1996;Broekman et al., 2006;Bennett, 2009;Streicher et al., 2011). Nonetheless, a subterranean existence and the associated foraging is not only substantially more costly than aboveground living (Vleck, 1979;Lovegrove, 1989;Zelova et al., 2010), but also generates a significant amount of metabolic heat (Bozinovic, Carter & Ebensperger, 2005;Luna & Antinuchi, 2007). ...
The subterranean niche is a specialized environment that presents its inhabitants with a unique set of microclimatic conditions. African mole-rats are strictly subterranean and exhibit a continuum of sociality ranging from solitary to highly social. Colonies of the Damaraland mole-rat Fukomys damarensis comprise of a dominant breeding or reproductive female and one or two male consorts and a number of subordinate and non-reproductive individuals of both sexes. In this study, we investigated the locomotor activity patterns of reproductive and non-reproductive female Damaraland mole-rats with the intention to investigate daily timing of activity and activity levels with changes in ambient temperature and also whether activity would differ between the reproductive castes at different ambient temperatures. The Damaraland mole-rats displayed predominantly nocturnal activity at all three temperatures and the levels of activity were different for all three temperatures tested. Mole-rats exhibited the lowest levels of activity at 30°C; they are most active at 25°C while they display intermediate levels of activity at 20°C. Despite exhibiting the majority of their activity during the night, non-reproductive females display significantly more day-time activity compared with the reproductive females at all three temperatures. Nocturnal activity is comparable between reproductive and non-reproductive animals at 20 and 25°C, but not at 30°C. Daily locomotor activity rhythms of the Damaraland mole-rats appear to be relatively flexible and respond to comparatively small changes in ambient temperatures. Differences in daily activity between reproductive and non-reproductive animals may emphasize the existence of physiological and morphological castes in the Damaraland mole-rat.
... Seasonal acclimatization to cold in endothermic animals generally leads to an increase in their capacity to produce heat, and thus maintains body temperature (T b ) homeostasis. The primary mechanism for T b homeostasis typically includes an elevtion in metabolic heat production and increase in the insulative quality of the fur, leading to a reduction in the lower critical ambient temperature (Soriano et al., 2002;Jefimow et al., 2004;Broekman et al., 2006). ...
(1)Metabolic rate (MR), thermal neutral zone (TNZ), body temperature (Tb), and thermal conductance were measured in striped hamsters (Cricetulus barabensis) that were live-trapped in winter and summer.(2)TNZ of winter hamsters was 20.8–30.6 °C and that of summer hamsters was 27.5–32.9 °C. Mean MR within the TNZ was 3.89±0.13 ml O2/g h in winter and 2.58±0.07 ml O2/g h in summer. The seasonal effects on Tb were not significant (P=0.09).(3)The ecological physiology properties for the hamster were higher MR and wider TNZ in winter but a lower MR and narrower TNZ in summer, which were closely related to their living habits, characterized by a cold winter and hot, dry summer.
... This alternative hypothesis should be evaluated in future studies. In regard to the effect of altitude and latitude (hence, Po 2 and ambient temperature), no effect of altitude on BMR was observed for two subterranean rodent species by Bozinovic et al. (2005; for S. cyanus) or by Broekman et al. (2006; for Cryptomys hottentotus). Moreover, minimal metabolism in several subterranean species was not affected by varying experimental Po 2 conditions (Contreras 1983; Widmer et al. 1997); this had only a minimal response in semifossorial species (Frappell et al. 2002). ...
Subterranean mammals show lower mass-independent basal metabolic rates (BMRs). Several competing hypotheses were suggested to explain how microenvironmental conditions and underground life affect subterranean mammalian energetics. Two of these are the thermal stress and the cost-of-burrowing hypotheses. The thermal stress hypothesis posits that a lower mass-independent BMR reduces overheating in burrows where convective and evaporative heat loss is low, whereas the cost-of-burrowing hypothesis states that a lower mass-independent BMR may compensate for the high energy expenditure of digging. In this article, we assessed the relationship between BMR of Ctenomys and environmental variables through conventional statistics as well as independent contrasts. Moreover, we tested both the thermal stress and the cost-of-burrowing hypotheses at an interspecific level in a very homogeneous genus of subterranean rodents, the South American genus Ctenomys. We compared species from different geographic localities that have contrasting habitat conditions. We measured BMR through open-flow respirometry. After conventional as well as independent contrast analyses, our results support neither the thermal stress nor the cost-of-burrowing hypotheses. We observed that only body mass affects the variability in BMR. Contrasting climatic and soil conditions, habitat productivity, and net primary productivity were not correlated with BMR variability. We suggested that, because BMR and maximum metabolic rates (MMRs) are correlated, low BMRs among Ctenomys species could also be determined by factors that affect MMR rather than BMR.
Basal rate of metabolism (BMR) is a physiological parameter that should be measured under strictly defined experimental conditions. In comparative analyses among mammals BMR is widely used as an index of the intensity of the metabolic machinery or as a proxy for energy expenditure. Many databases with BMR values for mammals are available, but the criteria used to select metabolic data as BMR estimates have often varied and the potential effect of this variability has rarely been questioned. We provide a new, expanded BMR database reflecting compliance with standard criteria (resting, postabsorptive state; thermal neutrality; adult, non-reproductive status for females) and examine potential effects of differential selectivity on the results of comparative analyses. The database includes 1739 different entries for 817 species of mammals, compiled from the original sources. It provides information permitting assessment of the validity of each estimate and presents the value closest to a proper BMR for each entry. Using different selection criteria, several alternative data sets were extracted and used in comparative analyses of (i) the scaling of BMR to body mass and (ii) the relationship between brain mass and BMR. It was expected that results would be especially dependent on selection criteria with small sample sizes and with relatively weak relationships. Phylogenetically informed regression (phylogenetic generalized least squares, PGLS) was applied to the alternative data sets for several different clades (Mammalia, Eutheria, Metatheria, or individual orders). For Mammalia, a ‘subsampling procedure’ was also applied, in which random subsamples of different sample sizes were taken from each original data set and successively analysed. In each case, two data sets with identical sample size and species, but comprising BMR data with different degrees of reliability, were compared. Selection criteria had minor effects on scaling equations computed for large clades (Mammalia, Eutheria, Metatheria), although less-reliable estimates of BMR were generally about 12–20% larger than more-reliable ones. Larger effects were found with more-limited clades, such as sciuromorph rodents. For the relationship between BMR and brain mass the results of comparative analyses were found to depend strongly on the data set used, especially with more-limited, order-level clades. In fact, with small sample sizes (e.g. <100) results often appeared erratic. Subsampling revealed that sample size has a non-linear effect on the probability of a zero slope for a given relationship. Depending on the species included, results could differ dramatically, especially with small sample sizes. Overall, our findings indicate a need for due diligence when selecting BMR estimates and caution regarding results (even if seemingly significant) with small sample sizes.
Burrow, soil surface and ambient temperatures were compared in mesic and xeric climates in tropical and sub-tropical Africa. In all the areas studied there was a similar daily pattern of change in the temperature of the soil surface and the burrow air but the magnitude of the changes and the time of day at which maximal and minimal temperatures occurred varied. In all areas, changes in burrow temperature were of a lower amplitude than those above ground. Mean monthly subsoil temperatures show that the annual amplitude of temperature fluctuation is greatest at the soil surface and diminishes with increasing depth. At depths greater than 0,6 m mean annual soil temperatures vary minimally. The depth at which this occurs is to some extent dependent upon soil type and ground cover. The mean daily burrow temperatures also show that the daily amplitude of temperature fluctuation is less with increasing depth. The subtropics show marked seasonal changes in mean burrow and above-ground temperatures whereas the available information in the literature shows that little seasonality occurs in the tropics. We suggest that this regional difference in temperature profiles may lead to the seasonality in breeding and in moulting shown by rodent moles from the subtropics and for the absence of this seasonality in rodent moles from the tropics.Tonnel-, grondoppervlak- en lugtemperature word in matige en droe klimate in tropiese en subtropiese Afrika vergelyk. In al die gebiede wat bestudeer is, het ’n soortgelyke daaglikse patroon van verandering in die temperatuur van die grondoppervlak en die tonnellug voorgekom, maar die grootheid van die veranderinge en die tyd van die dag wanneer maksimum- en minimum-temperature voorgekom het, het verskil. In al die gebiede, was die veranderinge van tonneltemperature van ’n laer wydte as die van bogrondse temperature. Gemiddelde maandelikse ondergrondse temperature toon dat die jaariikse wydte van temperatuurfluktuasie die grootste op die grondoppervlak is en verminder met toenemende diepte. By dieptes van meer as 0,6 m, varieer die gemiddelde jaariikse grondtemperature minimaal. Die diepte waar dit gebeur hang, tot ’n sekere mate, van die grondtipe en gronddekking af. Die gemiddelde daaglikse tonneltemperatuur wys ook dat die daaglikse wydte van temperatuurfluktuasie minder word met toenemende diepte. Die subtrope het merkbare seisoenale veranderinge in gemiddelde tonnel- en bogrondse temperature getoon, terwyl die beskikbare inligting in die literatuur toon dat daar min seisoenaliteit in die trope voorkom. Ons stel voor dat hierdie streeksverskille in temperatuurprofiele mag lei tot seisoenaliteit by teling en verharing in knaagmolle van die subtrope en die afwesigheid van hierdie seisoenaliteit by knaagmolle van die trope.
Abstract The energetics of the lesser long-eared bat, Nyctophilus geoffroyi, at the southern limits of its distribution was,examined ,to determine ,whether ,this species shows ,any latitudinal variation in this ,aspect of its physiological ecology. Estimates of metabolic,rate were obtained from the oxygen,consumption,of adult bats in a ,non-reproductive condition. ,Values for the thermoneutral ,zone ,were ,similar but thermal conductance,was lower than for bats from mainland,of Australia. Euthermic body temperature,was higher (37.4 ±0.2 °C) and the ambient,temperature,at which N. geoffroyientered,torpor has a downward,shift of 10°C at the southern limits of its distribution. The basal metabolic rate (1.12 ±0.14 mL O2g ,). All of these differences are apparently adaptations to a cooler environment. ZO020 39 The rm al en er g et ics of Nyc to phi lusgeo ff ro yi K. J . Dix on a nd R . W.R ose
We outline a computer model of heat and mass transfer through flesh, fat and porous fur for endotherms of any dimensions. We then validate it with a series of laboratory studies. Finally, we explore applications of the model to Bergmann's rule, predicting the mouse-to-elephant curve, climate-disease-toxicant interactions, animal 'design' via genetic engineering and energetic constraints on community structure. As a first test of the model we present calculations and metabolic chamber measurements for mammals ranging in size from mice to Holstein calves. We then compare simultaneous measurements on deer mice, Peromyscus maniculatus, of oxygen consumption, doubly labelled water turnover and food consumption with calculations of metabolic rate using body temperature radio-telemetry as input to the endotherm model. The endotherm model derived in the Appendix requires data on allometry (body dimensions, surface area), fur properties, core temperature, air and radiant temperatures and wind speed. The model is useful for calculating energetic expenditure in different microclimates without the need for extensive physiological measurements in the laboratory. Model predictions of metabolic rate at 12-degrees-C and at 22-degrees-C were well correlated with each of the three empirical estimates. The model shows that the posture an animal assumes can influence measurements of metabolic rate. Model calculations of metabolic rate using postures ranging from a curled-up ball-like geometry to a sprawled-out, cylinder or ellipsoid geometry bracket all three sets of simultaneous empirical data taken on the same animals. Applications of the model show that it can be applied in a wide variety of circumstances to gain insight into physiological and ecological problems.
Free‐living animals make complex decisions associated with optimizing energy and nutrient intake. In environments where ambient temperatures fall below the thermoneutral zone, homeotherms must choose whether or not to forage, how long and what to forage for, and whether or not to perform activities that conserve energy.
Huddling in groups has long been thought of as a possible means of conserving energy. Laboratory studies have shown that at low ambient temperatures individuals in groups expend less energy than individuals by themselves. However, studies have yet to demonstrate that thermoregulatory savings can have an impact on the overall daily energy expenditure (DEE) of free‐living animals.
Here we show that, in the laboratory, African Four‐Striped Grass Mice ( Rhabdomys pumilio ) expend less energy per individual in large groups than smaller groups. We also show that when free‐living groups were experimentally reduced to one‐half of their original size, DEE and water turnover increased by 19% and 37%, respectively.
The magnitudes of the reduction in free‐living DEE were comparable with calculated energy savings from the laboratory. One of the reasons why this species may sometimes occur in groups is that energetic benefits can be gained through huddling in habitats in which food and water are scarce.
1.1.|Seasonal moult has major effects on coat insulation and solar heat gain in the three species of subarctic mammals that shift between white winter pelages and darker summer coats: Lepus americanus, Mustela erminea, and Phodopus sungorus.2.2.|At low wind speeds, coat thermal resistance is elevated 27% (Phodopus) to 87% (Lepus) in winter months compared to summer months.3.3.|In most cases, fractional solar heat gain to the skin is reduced in winter coats compared to summer coats.4.4.|The decrease in solar heat gain in winter coats is due largely to increased insulation and not to altered optical qualities. This is because the thermal effect of radiation penetrating more deeply into winter coats importantly counteracts the effects of these coat's higher reflectivity.
Mole rats (Spalax ehrenbergi superspecies) perform the heavy work of digging their subterranean burrows in Israel under highly hypoxic/hypercapnic conditions. Unlike most other mammals, they can achieve high levels of metabolic rate under these conditions, while their metabolic rate at low work rates is depressed. We explored, by comparing mole rats with white rats, whether and how this is related to adaptations in the design of the respiratory system, which determines the transfer of O2 from the lung to muscle mitochondria. At the same body mass, mole rats were found to have a significantly smaller total skeletal muscle mass than ordinary white rats (-22%). In contrast, the fractional volume of muscle mitochondria was larger by 46%. As a consequence, both species had the same total amount of mitochondria and achieved, under normoxia, the same V(O2max). Whereas the O2 transport capacity of the blood was not different, we found a larger capillary density (+31%) in the mole rat muscle, resulting in a reduced diffusion distance to mitochondria. The structural pulmonary diffusing capacity for O2 was greater in the mole rat (+44%), thus facilitating O2 uptake in hypoxia. We conclude that structural adaptations in lung and muscle tissue improve O2 diffusion conditions and serve to maintain high metabolic rates in hypoxia but have no consequences for achieving V(O2max) under normoxic conditions.
Many small mammals inhabiting fluctuating and cold environments display enhanced capacity for seasonal changes in nonshivering thermogenesis (NST) and thermoregulatory maximum metabolic rate (MMR). However, it is not known how this plasticity remains in a mammal that rarely experiences extreme thermal fluctuations. In order to answer this question, we determined body mass (m(b)), basal metabolic rate (BMR), NST, MMR, and minimum thermal conductance (C) on a Chilean fossorial caviomorph (Spalacopus cyanus) from a coastal population, acclimated to cold (15 degrees C) and warm (30 degrees C) conditions. NST was measured as the maximum response of metabolic rate (NST(max)) after injection of norepinephrine (NE) in thermoneutrality minus BMR. Maximum metabolic rate was assessed in animals exposed to enhanced heat-loss atmosphere (He-O2) connected with an open-flow respirometer. Body mass and metabolic variables increased significantly after cold acclimation with respect to warm acclimation but to a low extent (BMR, 26%; NST, 10%; and MMR, 12%). However, aerobic scope (MMR/BMR), calculated shivering thermogenesis (ST), and C did not change with acclimation regime. Our data suggest that physiological plasticity of S. cyanus is relatively low, which is in accordance with a fossorial mode of life. Although little is known about MMR and NST in fossorial mammals, S. cyanus has remarkably high NST; low MMR; and surprisingly, a nil capacity of ST when compared with other rodents.
The blind subterranean mole rat superspecies Spalax ehrenbergi has evolved adaptations that allow it to survive and carry out intensive activities in its highly hypoxic underground sealed burrows. A key component of this adaptation is a higher capillary density in some Spalax tissues, primarily in muscles used in digging and in other energetic activities, resulting in a shorter diffusion distance for oxygen. Vascular endothelial growth factor (VEGF) is an angiogenic factor that is critical for angiogenesis during development and is found in response to tissue ischemia. We demonstrate here that due to physiological differences, the Spalax muscle regulatory mechanism for VEGF is different than in Rattus muscle. In vivo, the constitutive level of the VEGF mRNA and the mRNA levels of its transcriptional regulator HIF-1alpha and its mRNA stabilizer HuR are significantly higher in Spalax muscle than in Rattus muscle. Furthermore, as opposed to Rattus, the mRNA levels of HIF-1alpha, HuR, VEGF, as well as that of LDH-A, the enzyme that catalyzes the production of lactate, an accepted marker of anaerobic metabolism, are not increased in Spalax after hypoxia. However, ex vivo, when oxygenation by blood vessels is no longer relevant, the expression pattern of all these genes is similar in the two rodents under both normoxic and hypoxic conditions. Our studies provide evidence that the highly vascularized muscle in Spalax, the most energy consuming tissue during digging, is resistant to the effects of oxygen deprivation. The significance of these results with respect to ischemic vascular disease is abundantly clear.
Thermal conductance is a measure of the ease with which heat is exchanged between a body and the environment. It may include or exclude evaporative heat loss. If evaporative heat loss is included, conductance in endotherms should be used only at temperatures below thermoneutrality because evaporation is of little importance only at these temperatures. The slope of the curve of metabolism on air temperature equals conductance if and only if the curve extrapolates to body temperature when the rate of metabolism is zero. Slopes fitted by the method of least squares () usually are less than the mean minimal conductance () calculated from individual measurements of metabolism below thermoneutrality, because most endotherms mix physical and chemical thermoregulation at temperatures below thermoneutrality. The extent to which an extrapolation of the fitted curve overestimates body temperature (δT) is related to the error by which fitted slopes estimate mean minimal conductance: . This relation can be used to correct fitted slopes in the literature to mean minimal conductances, as long as the mean air temperature at which minimal conductance is being estimated falls between 12 and 20 C and mean body temperature falls between 32 and 38 C.
The Barrow I. golden bandicoot (Isoodon auratus) is a small arid-adapted marsupial. It has a low and labile body temperature, a low basal metabolic rate, a low thermal conductance, and a low rate of evaporative water loss. Its metabolic, thermal and hygric physiology resembles that of another arid-adapted bandicoot, the bilby, and differs from temperate and tropical bandicoots.
In this paper we test the hypothesis that bats of the Andean highlands show distinctive metabolic responses compared with bats from lowland forests. We compared existing literature with new information on 3 bat species having the following food habits: a nectarivore (Anoura latidens), a frugivore (Sturnira erythromos), and an insectivore (Tadarida brasiliensis). Basal metabolic rate, as determined by oxygen consumption, thermal conductance, and body temperature were measured at ambient temperatures of 10–38°C. Some distinctive metabolic responses of these bat species, although varying with respect to food guild, allow us to separate them from counterpart species that are typically found in lowland forests. A. latidens is characterized by higher basal metabolic rate; however, thermal conductance and lower critical temperature values do not show an adaptation to cool environments, as expected. S. erythromos also increases its basal metabolic rate, but it maintains thermal conductance as expected, which implies a very important displacement of thermoneutral zone to lower temperatures. At temperatures below lower critical temperature, in addition to an endothermic response, S. erythromos sometimes expresses a hypothermic response or facultative torpor, independent of sex and body mass. T. brasiliensis has a lower basal metabolic rate and thermal conductance and also has its thermoneutral zone range displaced toward lower temperatures. Likewise, this species enters obligate torpor when ambient temperatures are below 22°C.
Thermoregulation of the mesic-habitat Cape mole rat, Georychus capensis (mean mass 193 g), was investigated, and the data was used to test the hypothesis that exceptionally low mass-specific rates of metabolism are common to the arid-habitat subterranean rodents only. The mean body temperature was 36.4 C, resting metabolic rate was 68% of that expected for rodents, and conductance was 62% of the predicted value. This mole rat maintained a constant body temperature independent of ambient temperatures between -0.5 and 28 C. The data refuted the above hypothesis. A possible explanation for the low rate of metabolism of G. capensis is given.
The lungs of the naked mole-rat Heterocephalus
glaber were morphologically (qualitatively) and morphometrically (quantitatively) investigated in adult captive in-burrow body-temperature-maintained (CBTMA) and captive cold-exposed animals (CCEA). The observations were compared with those of field (burrow-dwelling) animals (FA) examined in an earlier study. The lungs of the captive animals were morphologically (qualitatively) similar to those of the field mole-rats. Conspicuous paedomorphic features, i.e. a preponderant double pulmonary capillary arrangement, incomplete differentiation of alveolar pneumocytes, and extension of a cuboidal epithelium to the immediate vicinity of the alveoli, were observed. The prevalent pulmonary underdevelopment was attributed to the relatively low metabolic rate of the poikilothermic naked mole-rat, a species that has evolved in a thermally stable environment. Measurable differences and similarities were found between the lungs of the captive naked mole-rats themselves (i.e. the CBTMA and the CCEA) and between the captive and the field ones. Genetic factors may help explain the conserved pulmonary structural features while environmental (gaseous) change from a hypoxic–hypercapneic (an oxygen deficient–high carbon dioxide concentration) to a normoxic–normocapnic atmosphere and the thermal shift respectively may have enforced pulmonary transformations between the CBTMA and the FA and between the CCEA and the CBTMA. Paradoxically, the CCEA had a significantly lower mass-specific total morphometric pulmonary diffusing capacity of 0.024 compared with that of 0.102 mlO2.s−1.mbar−1.kg−1 in the CBTMA. The observed morphometric differences indicate that the lung of the naked mole-rat, though morphologically unchanged, is intrinsically tractable to environmental shifts in its habitat. Studies on captive naked mole-rats should not be indiscriminately taken to be representative of the species.
Temperature and respiratory gas (CO2 and O2) concentrations were measured in the foraging tunnels of burrows naturally inhabited by two species of southern African mole-rats, the Cape mole-rat Georhychus capensis and the Damaraland mole-rat Cryptomys damarensis. Both species are completely fossorial and inhabit closed burrow systems. Tunnels of G. capensis burrows had a mean diameter of 8.7 cm and a depth, measured to the roof of the tunnel, of 6.2 cm; those of C. damarensis had a mean diameter of 6.5 cm and depth of 40 cm. In both species, the mean concentration of CO2 was higher, and mean concentration of O2 lower, in burrows than in the surrounding soil or in ambient air. Mean and minimum values of O2 were 20.4% and 19.8%, respectively, in G. capensis and 20.4% and 19.9% in C. damarensis; mean and maximum values of CO2 were 0.4% and 1.2% in G. capensis and 0.4% and 6.0% in C. damarensis. Temperature varied between 18.5 and 24.2 °C in burrows of G. capensis by comparison with an ambient range of 16.9 to 26.8 °C; and from 19.6 to 29.3 °C in burrows of C. damarensis by comparison with an ambient range of 8.6 to 30.8 °C. Thus a burrowing habit seems to offer both species protection from extremes of temperature without entailing the cost of a grossly abnormal respiratory environment. From a review of the relevant literature, we conclude that average concentrations of CO2 and O2 in mammalian burrows often do not differ greatly from ambient values. However, more work is needed to determine the respiratory gas concentrations in the immediate vicinity of active, burrowing animals.
Species of the genus Gerbillus are very common among the rodent fauna inhabiting arid zones and dune habitats in the palaearctic region. In Israel G. nanus is distributed in extreme arid areas, while G. allenbyi is common in coastal plain dune habitats, of mesic and semi-arid areas. Therefore, their distribution pattern is considered allopatric.
Heat production, estimated by the oxygen consumption (Vo2), and body temperature (T
b) at various ambient temperatures were measured in both gerbils. The thermoneutral zone for G. allenbyi is between T
a=28–35° C (\(\dot V_{{\text{O}}_{\text{2}} } \)
T
b=36.3–38.3° C) and for G. nanus is at T
a=33±1° C (\(\dot V_{{\text{O}}_{\text{2}} } \), T
b=38.8° C). The \(\dot V_{{\text{O}}_{\text{2}} } \) values at thermoneutrality are 75.7% and 50.6% respectively of the calculated values for rodents with a mean body weight of 35.3 g and 28.4 g.
Nonshivering thermogenesis (NST) was measured in both species as the maximal response to an injection of noradrenaline (2.0 mg/Kg s.c.). NST magnitude was the same for both species.
The results show that both gerbils are adapted to arid environments. The difference in the thermoneutral zones of the two species is discussed in terms of its adaptive nature.
1.
A comparative study of heat production and heat dissipation in two populations of golden spiny mice (Acomys russatus) from two extremely different habitats was carried out.
2.
Mice from a hot environment, the shores of the Dead Sea (Ein Gedi, EG-mice) could not maintain body temperature (T
b) when exposed to ambient temperature (T
a) of 6 C in a cold room. Mice from a colder environment, the high mountains of South Sinai (S-mice), acclimated in the laboratory to 28 C or freshly captured, were able to thermoregulate in a cold room (T
a=6 C).
3.
Mice of both populations, acclimated to 28 C, had the same resting oxygen consumption (
[(V)\dot]O2 \dot V_{O_2 }
) in the thermoneutral zone (0.75 ml O2 (gh)–1 for 60 g mean body weight).
4.
[(V)\dot]O2 \dot V_{O_2 }
atT
a below 20 C showed differences. In S-mice it continued to rise and enough heat was generated to keep them euthermic. EG-mice showed a progressive decrease and could not maintainT
b.
5.
Continuous measurements ofT
b and
[(V)\dot]O2 \dot V_{O_2 }
in EG-mouse during cooling (T
a=6 C) and reheating (T
a=25 C) show smooth curves without any bursts of heat generating activity typical of rodents entering or coming out of torpor. The spiny mice have to be rewarmed by an external heat source.
6.
Thermal conductance was measured in live mice after acclimation to 28 C or in carcasses collected in the field at various seasons. Measurements failed to show any appreciable difference between the two populations where animals with similar body weight were compared.
7.
It is concluded that difference in heat production and not in heat conservation enableAcomys russatus to adapt to a colder habitat.
Japanese quail,Coturnix coturnix japonica, which were acclimated to a simulated altitude of 6100 m for six weeks were compared with control quail maintained at sea level. Body weight initially decreased in both groups, and by the end of six weeks the altitude quail weighed an average of 8% less than the control quail (Fig. 1). Compared with the controls, the altitude birds exhibited mean increases in hematocrit ratio and blood hemoglobin concentration of 31 and 37% respectively (Fig. 2). Blood volume was 36% higher in the altitude acclimated quail, while plasma volume was unchanged (Fig. 3). Exposure to chronic hypoxia resulted in hypertrophy of the right ventricle, while left ventricular mass was unchanged (Fig. 4). Rates of O2 consumption (VO2) at 5C were continuously recorded as ambient PO2 was slowly reduced from 155 to 30 torr. VO2 was significantly higher at any given PO2 in the altitude quail (Fig. 5). Exposure to reduced PO2 resulted in a significantly greater decrease in body temperature in the control quail than in the altitude acclimated birds (Fig. 6).
1.1. The following equation based on 230 conductance values for 192 species of mammals of body weights ranging from 3.5 to 150,000 g describes the relationship of conductance below thermal neutrality to body weight in mammals: C = 0.760 W−0.426, where C has units of mlO2/g·h·°C and W is body weight in g.2.2. Bats, order Chiroptera, have conductance values higher than predicted from body weight; conductance is predicted by the equation : C = 1.54 W−0.54.3.3. Heteromyid and cricetid rodents have conductance values below predicted and the following equations predict conductance in these two families. C = 0.62 W−0.44 and C = 1.03 W−0.54, respectively.
1.1. Resting metabolic rates (RMR) lower than those expected for body mass according to allometric equations have been recorded for species of rodents inhabiting arid and semi-arid environments. Such a phenomenon was also noted in non-arid rodent species which are adapted to various modes of life. Non-shivering thermogenesis (NST) is an important mechanism for heart production in small cold-acclimated mammals.2.2. The aim of this study was to try to assess the ecological significance of NST by comparing various parameters concerning NST, RMR and overall minimal thermal conductance. The analysis was carried out on data obtained from 21 species, 4 chromosomal types of Spalax ehrenbergi and 2 different populations of Acomys russatus. The studied species were from Israel and South Africa.3.3. The analysis revealed that RMR is an adaptive parameter and has an allometric relation with body mass. It depends on habitat and time of activity. Species which have low RMR values show high values of NST.
Microtus ochrogaster and Dicrostonyx groenlandicus are closely related species that share many life-history characteristics, but have different food habits; D. groenlandicus primarily eats dicots, such as evergreen and deciduous shrubs, while M. ochrogaster primarily eats forbs and grasses. We compared the size of gastrointestinal tracts of these two species acclimated to either 5 or 23°C. In both species, animals acclimated to cold ambient temperatures (5°C) had longer gastrointestinal tracts than did those acclimated to warmer temperatures (23°C). In addition, animals acclimated to colder temperatures also carried a greater mass of digesta in their gastrointestinal tracts. Only in M. ochrogaster did the wet mass of the tract increase in response to cold-temperature acclimation. In general, D. groenlandicus had larger and heavier tracts than did M. ochrogaster. The small intestine and cecum increased in size at cold temperatures, but this increase occurred differently in each species. The differences we observed can be attributed to differences in the additional food eaten by each species in the cold.
1. Non-shivering thermogenesis (NST) is a heat-production mechanism participating in the chemical thermoregulation of mammals.
2. NST is additional to shivering and takes place at temperatures close to the thermoneutral zone.
3. NST occurs in newborn mammals and in those that hibernate. In some adult mammals it can be induced by adaptation to cold.
4. In small mammals NST produces approximately the same amount of heat as shivering. It becomes less important with increasing body weight of the animals.
5. NST is regulated by the hypothalamus and it is based predominantly on the calorigenic action of noradrenaline released from sympathetic nerve-endings.
Participation of other calorigenic substances and of the specific dynamic action of food cannot be excluded.
6. NST is localized mainly in skeletal muscles and in brown adipose tissue. Small amounts of NST may come from liver, intestine, heart and brain.
7. The biochemical basis of the calorigenic action of noradrenaline has not yet been fully elucidated.
Thermoregulatory abilities, which may play a role in physiological adaptations, were compared between two field mouse species (Apodemus mystacinus and A. hermonensis) from Mount Hermon. While A. hermonensis is common at altitudes above 2100 m, A. mystacinus is common at 1650 m. The following variables were compared in mice acclimated to an ambient temperature of 24°C with a photoperiod of 12L:12D, body temperature during exposure to 4°C for 6 h, O2 consumption and body temperature at various ambient temperature, non-shivering thermogenesis measured as a response to a noradrenaline injection, and the daily rhythm of body temperature. Both species could regulate their body temperature at ambient temperatures between 6 and 34°C. The thermoneutral zone for A. mystacinus lies between 28 and 32°C, while for A. hermonensis a thermoneutral point is noted at 28°C. Both species increased O2 consumption and body temperature as a response to noradrenalin. However, maximal VO
2 consumption as an response to noradrenaline and non-shivering thermogenesis capacity were higher in A. mystacinus, even though A. hermonensis is half the size of A. mystacinus. The body temperature rhythm in A. hermonensis has a clear daily pattern, while A. mystacinus can be considered arhythmic. The results suggest that A. hermonensis is adapted to its environment by an increase in resting metabolic rate but also depends on behavioural thermoregulation. A. mystacinus depends more on an increased non-shivering thermogenesis capacity.
Why are sustained energy budgets of humans and other vertebrates limited to not more than about seven times resting metabolic rate? The answer to this question has potential applications to growth rates, foraging ecology, biogeography, plant metabolism, burn patients and sports medicine.
Individuals within a species, living across a wide range of habitats, often display a great deal of phenotypic plasticity for organ mass and function. We investigated the extent to which changes in organ mass are variable, corresponding to environmental demand, across an altitudinal gradient. Are there changes in the mass of oxygen delivery organs (heart and lungs) and other central processing organs (gut, liver, kidney) associated with an increased sustainable metabolic rate that results from decreased ambient temperatures and decreased oxygen availability along an altitudinal gradient? We measured food intake, resting metabolic rate (RMR), and organ mass in captive deer mice (Peromyscus maniculatus bairdii) at three sites from 1,200 to 3,800 m above sea level to determine whether energy demand was correlated with organ mass. We found that food intake, gut mass, and cardiopulmonary organ mass increased in mice living at high altitudes. RMR was not correlated with organ mass differences along the altitudinal gradient. While the conditions in this study were by no means extreme, these results show that mice living at high altitudes have higher levels of energy demand and possess larger cardiopulmonary and digestive organs than mice living at lower altitudes.
The naked mole-rat (Heterocephalus glaber) lives communally in a thermally buffered underground habitat. Here, it relies primarily on ectothermic (behavioral) mechanisms to maintain body temperature (T(b)). Outside this milieu, it is unable to effectively regulate T(b) and T(b) tracks that of ambient temperature (T(a)). Although naked mole-rats, in their natural habitat have little need for cold-tolerance, we questioned whether or not thermogenic capacity would change with prolonged (>1 year) exposure to cooler conditions. We hypothesized that these rodents would not conform to common mammalian patterns and that non-shivering thermogenic (NST) capacity would be unchanged with chronic cold exposure. The capacity for NST was assessed following noradrenaline administration (0.8 mg/kg, s.c.) to lightly anesthetized (pentobarbital 6% m/v 40 mg/kg) animals and monitoring the concomitant changes in oxygen consumption and T(b). Results concur with the null hypothesis in that prolonged cold exposure did not elicit any increase in NST capacity (1.52+/-0.17 ml O(2)/g/h, cold-acclimated; 1.73+/-0.31 ml O(2)/g/h, control; P>0.05). Rapid heat loss across their uninsulated integument may necessitate continuous maximal stimulation of brown adipose tissue (BAT), and as such, prevent any further increase in thermogenic capacity following cold exposure.
Subterranean mammals show lower than-allometrically expected-basal metabolic rates (BMR), and several competing hypotheses were suggested to explain how physical microenvironmental conditions and underground life affect subterranean mammalian energetics. Two of these are the thermal-stress and the cost-of-burrowing hypotheses. The thermal-stress hypothesis posits that a lower mass-independent BMR reduces overheating in burrows where convective and evaporative heat loss is low, whereas the cost-of-burrowing hypothesis states that a lower mass-independent BMR may compensate for the extremely high energy expenditure of digging during foraging activity. In this paper we tested both hypotheses at an intraspecific level. We compared seven populations of the subterranean rodent Spalacopus cyanus or cururo from different geographic localities with contrasting habitat conditions. We measured BMR and digging metabolic rate (DMR) through open flow respirometry. Our results support neither the thermal-stress nor the cost-of-burrowing hypothesis. Cururos from habitats with contrasting climatic and soil conditions exhibited similar BMR and DMR when measured under similar semi-natural conditions. It is possible that S. cyanus originated in Andean locations where it adapted to relatively hard soils. Later, when populations moved into coastal areas characterized by softer soils, they may have retained the original adaptation without further phenotypic changes.
Winter is an energetically stressful period for small mammals as increasing demands for thermoregulation are often coupled with shortages of food supply. In sub-tropical savannah, Hottentot golden moles (Ambysomus hottentottus longiceps) forage throughout the year and for long periods of each day. This may enable them to acquire sufficient resources from an insectivorous prey base that is both widely dispersed and energetically costly to obtain. However, they also inhabit much cooler regions; how their energy budgets are managed in these areas is unknown. We measured the daily energy expenditure (DEE), resting metabolic rate (RMR) and water turnover (WTO) of free-living golden moles during both winter and summer at high altitude (1500 m). We used measurements of deuterium dilution to estimate body fat during these two periods. DEE, WTO and body mass did not differ significantly between seasons. However, RMR values were higher during the winter than the summer and, in the latter case were also lower than allometric predictions. Body fat was also higher during the winter. Calculations show that during the winter they may restrict activity to shorter, more intense periods. This, together with an increase in thermal insulation, might enable them to survive the cold.
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