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Daily torpor during the active phase in free-ranging rock elephant shrews (Elephantulus myurus)
Journal of Zoology
Abstract
In highly seasonal environments animals that use daily torpor usually do so during the rest phase. In subtropical and tropical environments, however, daily torpor may not necessarily be confined to the animals' rest phase. Animals may display torpor during the active phase. We investigated the daily rhythms and seasonal rhythms of body temperature (Tb) in normothermic and torpid free-ranging rock elephant shrews Elephantulus
myurus at Weenen Game Reserve, KwaZulu-Natal, South Africa. Tbs were recorded using miniature dataloggers from May 2001 to May 2002. Daily patterns of Tb in normothermic E.
myurus suggested polyphasic Tb patterns that nevertheless suggested a rest phase that was coincident with the daytime. When the elephant shrews used torpor, the lowest Tbs were observed during the night-time, such that torpor was used during the coldest part of the night and arousal was associated with the 3-h period around sunrise. We suggest that the principal benefit of a flexible daily rhythm of Tb was that it facilitated arousal by passive exogenous heating using ambient temperature cycles.
... One of the most common ways of measuring the energy use of an animal is the measurement of metabolic rate (Willmer et al. 2005). Previous studies on thermoregulation and energetics extended our understanding of how animals are able to survive in their environments and how they are able to cope with changing or challenging environmental conditions (Geiser 2004; McKechnie & Lovegrove 2002; Mzilikazi & Lovegrove 2004). Some animals inhabit harsh environments characterised by extreme environmental temperatures, seasonally low productivity, as well as daily fluctuations in ambient temperature, for example the desert and karoo biomes of Southern Africa (Mucina & Rutherford 2006). ...
... Hibernation and daily torpor have been found to occur in both mammals and birds (Geiser 1998). Heterothermy has been reported in various mammalian taxa, including monotremes (Grigg et al. 2003), marsupials (Körtner & Geiser 2000), some members of the Afrotheria (Mzilikazi & Lovegrove 2004; Lovegrove et al. 1999), rodents ( Bozinovic et al. 2004) and primates (Dausmann et al. 2004; Schmid 2000; Nowack et al. 2010), as well as Xenarthra (Superina & Boily 2007 ), Pholidota, Eulipotyphla (Sayah et al. 2008) and Chiroptera (Willis & Brigham 2003). Studies focusing on mammals in the Afrotropics have mainly concentrated on rodents, presumably because of the ease with which they can be maintained in the laboratory (Lovegrove & Raman 1998; Mzilikazi & Lovegrove 2004; Perrin & Richardson 2004), Afrotherians, because of their intriguing phylogenetic placement (Jackson et al. 2009; Lovegrove & Génin 2008; Mzilikazi & Lovegrove 2004; Scantlebury et al. 2008) and primates, because of the interest that torpor in primates holds for medical applications (Dausmann et al. 2004; Nowack et al. 2010). ...
... Heterothermy has been reported in various mammalian taxa, including monotremes (Grigg et al. 2003), marsupials (Körtner & Geiser 2000), some members of the Afrotheria (Mzilikazi & Lovegrove 2004; Lovegrove et al. 1999), rodents ( Bozinovic et al. 2004) and primates (Dausmann et al. 2004; Schmid 2000; Nowack et al. 2010), as well as Xenarthra (Superina & Boily 2007 ), Pholidota, Eulipotyphla (Sayah et al. 2008) and Chiroptera (Willis & Brigham 2003). Studies focusing on mammals in the Afrotropics have mainly concentrated on rodents, presumably because of the ease with which they can be maintained in the laboratory (Lovegrove & Raman 1998; Mzilikazi & Lovegrove 2004; Perrin & Richardson 2004), Afrotherians, because of their intriguing phylogenetic placement (Jackson et al. 2009; Lovegrove & Génin 2008; Mzilikazi & Lovegrove 2004; Scantlebury et al. 2008) and primates, because of the interest that torpor in primates holds for medical applications (Dausmann et al. 2004; Nowack et al. 2010). Research into mammalian heterothermic responses has in the past been biased towards laboratory studies, even though their use under laboratory conditions may not be truly reflective of how these responses are expressed by animals in their natural environment (Geiser et al. 2000). ...
Animals that inhabit unfavourable habitats and experience seasons where the cost of maintenance exceeds the available energy resources have over time developed behavioural and physiological mechanisms to survive. These adaptations include changes in activity, improvement of cold tolerance by using nonshivering thermogenesis (NST), improvement of thermal conductance, reduction of body mass, or acclimation to colder temperatures (reduction of metabolic requirement). In addition some species exhibit heterothermy, in the form of either daily torpor or longer-term hibernation. The southern African hedgehog (Atelerix frontalis) is an excellent candidate to investigate the phenomenon of heterothermy because it is a small insectivore (summer body mass ca. 300 to 400g), burrows, inhabits harsh habitats and is not easy to find during the winter months.
In this study I aimed to investigate whether A. frontalis exhibits seasonal differences in metabolic rate and furthermore if this species exhibits heterothermy. The study was carried out in the Northern Cape Province, South Africa. Hedgehogs were hand captured and their metabolic rates were measured using indirect calorimetry. Individuals were implanted with temperature dataloggers for a summer period (November 2009-January 2010) and a winter period (May-August 2009).
The summer BMR of adult A. frontalis (0.448 ±0.035 mlO2/g/h, n=4) was significantly lower than their winter BMR (0.811 ±0.073 mlO2/g/h, n=4) and statistical analyses revealed that this was an affect caused by seasonal changes in the ambient environment. Individuals spent up to 84% of time during the measurement period torpid (-8°C <Ta<21°C). Body mass appears to be an important factor in determining the pattern of heterothermy (daily torpor versus hibernation) used in this species.
To my knowledge the extremely low body temperature (Tb min) of 1.0°C recorded for A. frontalis is the lowest Tb min recorded for a mainland Afrotropical mammal. This species displays classic up-regulation in metabolic rate during winter, resulting in an increase in the energetic requirements of the species. As a result, heterothermy appears to play a significant role in the energy balance of this species during winter, contributing to energy saving. Heterothermy may enable this species to survive in the face of global climate change.
... Interestingly, three individuals (including two of the individuals that only used torpor once) used torpor on the same day (19 June), a day with a moderate T a and no adverse weather conditions. The grand In both species, the minimum daily T b occurred almost exclusively at night or in the early morning (before 09:00), although on rare occasions, the T b peaks and lows were spread throughout the day, similar to the results reported by Mzilikazi and Lovegrove (2005) in eastern rock elephant shrews. ...
... Both species used torpor during our study, although western rock elephant shrews used it considerably more often. Torpor appears to be common in many of the Elephantulus elephant shrews studied to date (Lovegrove et al., 2001b;Mzilikazi and Lovegrove, 2005), so the fact that western rock elephant shrews use extensive torpor is not surprising. HI values for this species varied widely and were roughly similar to values from species traditionally classified as daily heterotherms (Boyles et al., 2011). ...
We measured body temperature (T(b)) in free-ranging individuals of two species of elephant shrews, namely western rock elephant shrews (Elephantulus rupestris) and Cape rock elephant shrews (E. edwardii), during winter in a winter-rainfall region of western South Africa. These syntopic species have similar ecologies and morphologies and thus potential for large overlaps in diet and habitat use. Unexpectedly, they displayed different T(b) patterns. Western rock elephant shrews were heterothermic, with all individuals decreasing T(b) below 30°C on at least 34% of nights. The level of heterothermy expressed was similar to other species traditionally defined as daily heterotherms and was inversely related to T(a), as is commonly seen in small heterothermic endotherms. In contrast, Cape rock elephant shrews rarely allowed their T(b) to decrease below 30°C. The level of heterothermy was similar to species traditionally defined as homeotherms and there was no relationship between the level of heterothermy expressed and T(a). In both species, the minimum daily T(b) was recorded almost exclusively at night, often shortly before sunrise, although in some individuals minimum T(b) occasionally occurred during the day. The interspecific variation in T(b) patterns among Elephantulus species recorded to date reiterates the importance of ecological determinants of heterothermy that interact with factors such as body mass and phylogeny.
... Animals were tracked using an R-1000 radio receiver attached to a 2-element Yagi antenna (African Wildlife Tracking cc, South Africa) with a maximum range of 150 m. Although sengis may be active during all hours (Mzilikazi & Lovegrove, 2005), the challenging terrain and the presence of nocturnal venomous snakes and arthropods prohibited night follows. Hence, observations were restricted to the daytime hours between 5:00 a.m. and 9:30 a.m., and 15:00 pm and 18:30 pm. ...
Limiting resources often differ between males and females. Reproductive success in females is constrained by resources such as food and shelter, while the availability of receptive females determines male reproductive success. In addition to limiting resources, low intra‐sexual tolerances among females can affect their spacing. High intolerances coinciding with low population densities have been suggested as a cause for the evolution of monogamy in mammals, but the evidence for female intolerance is limited. We investigated long‐term space use patterns (measured as home range sizes and centers of activity) in a wild population of eastern rock sengis (Elephantulus myurus) from Limpopo, South Africa. Between March 2012 and March 2016, we recorded capture locations for 93 sengis and home range size for 22 sengis and evaluated the contributions of study year, sex, and season on these measures. Sex had no significant effect on home range size, but ranges were significantly greater during the breeding compared to the non‐breeding season, consistent with the increased energetic demands during reproduction. We found corroborative support for the role of energetic demands on home range size fluctuations. The activity centers of female–female dyads were further apart than those of male–male or mixed‐sex dyads, suggesting lower female–female tolerances in the study species. Our results offer evidence that intolerances may affect female spacing behavior and may have contributed to the evolution of monogamy in sengis.
... Of note is that these ranges for T b are relatively moderate, with few animals experiencing variations of more than 8°C. Even in other afrotherians like elephant shrews, T b varied by only a few degrees during the active season (Mzilikazi and Lovegrove, 2004;Mzilikazi and Lovegrove, 2005;Oelkrug et al., 2012). We found ∼20°C variation in T b in both active and hibernating tenrecs. ...
Physiological plasticity allows organisms to respond to diverse conditions. However, can being too plastic actually be detrimental? Malagasy common tenrecs, Tenrec ecaudatus, have many plesiomorphic traits and may represent a basal placental mammal. We established a laboratory population of T. ecaudatus and found extreme plasticity in thermoregulation and metabolism, a novel hibernation form, variable annual timing, and remarkable growth and reproductive biology. For instance, tenrec body temperature (Tb) may approximate ambient temperature to as low as 12°C even when tenrecs are fully active. Conversely, tenrecs can hibernate with Tbs of 28°C. During the active season, oxygen consumption may vary 25-fold with little or no changes in Tb During the Austral winter, tenrecs are consistently torpid but the depth of torpor may be variable. A righting assay revealed that Tb contributes to but does not dictate activity status. Homeostatic processes are not always linked e.g. a hibernating tenrec experienced a ∼34% decrease in heart rate while maintaining constant body temperature and oxygen consumption rates. Tenrec growth rates vary but young may grow ∼40-fold in the 5 weeks until weaning and may possess indeterminate growth as adults. Despite all of this profound plasticity, tenrecs are surprisingly intolerant to extremes in ambient temperature (<8 or >34°C). We contend that while plasticity may confer numerous energetic advantages in consistently moderate environments, environmental extremes may have limited the success and distribution of plastic basal mammals.
... For experiment 1 (March–August 2005), 6 adult males of the 4 species were fitted with thermosensitive loggers (iButton Thermochron DS1921H, resolution 0.1258C, mass 3.1 g; Maxim Integrated Products, Sunnyvale, California). The accuracy and precision of the devices have been rigorously tested (Davidson et al. 2003; van Marken Lichtenbelt et al. 2006), and similar loggers have been used in mammals of a small body size (Mzilikazi and Lovegrove 2005; Korhonen et al. 2008). Loggers registered T b every 10 min, yielding approximately 1,860 data points per animal (1 iButton in a common vole malfunctioned and no data were retrieved). ...
Arvicoline voles do not possess sophisticated mechanisms to tolerate prolonged fasting and can starve to death in less than 24 h. Two experiments were performed to determine if the common vole (Microtus arvalis) and the tundra vole (M. oeconomus) have thermoregulatory adaptations to enhance survival during food deprivation or in winter, and to reveal the possible presence of ultradian body temperature (T b ) rhythms. Laboratory-bred voles (n = 5—6 for both species) were equipped with intra-abdominal data loggers that registered T b every 10 min and were subjected to 12-h fasting periods during photophase and scotophase. In addition, 10 animals of both species were placed in outdoor cages at natural ambient temperature (T a ) and their T b was registered at 3-h intervals between October and June. Fasted voles did not enter torpor, but the average 24-h T b decreased by 0.2—0.5°C in winter, yielding modest energy savings. The decrease in the T b correlated with T a but not photoperiod and could, thus, be interpreted as a response to cold. Tundra voles displayed short T b rhythms of 3—8 h in the laboratory and their individual T b fluctuations were synchronized. Arvicolines are suggested as promising models to study T b rhythms in small mammals.
... Radio-tagged animals actively foraged from midday onwards during daylight (Fig. 2) and continued to forage during the early part of the night, with torpor commencing around or soon after midnight (Geiser and Pavey 2007). Although entry into torpor during the active phase occurs in several placental mammals that passively rewarm during arousal (Schmid 2000; Mzilikazi and Lovegrove 2005) and seasonal shifts in activity periods within the active phase occur in other mammals (Kenagy et al. 2002), seasonal switching of the active phase as shown by P. macdonnellensis appears to be rare among mammals. The strategy employed by P. macdonnellensis should maximise energetic savings because animals are inactive during the period of lowest T a . ...
Several mammal species bask to passively rewarm during arousal from torpor, a strategy that can decrease energetic costs. Nothing is known about basking behaviour in these species or the trade-offs between energetic benefits of basking and potential costs associated with changes in activity patterns and increased predation risk. We assessed basking during winter in Pseudantechinus macdonnellensis, an Australian arid-zone marsupial that belongs to a family (Dasyuridae) that is typically nocturnal. Animals were implanted with temperature-sensitive transmitters to assess body temperatures and to assist in visually locating animals active during the day. Tagged animals regularly exhibited diurnal foraging. Foraging bouts occurred throughout the day; however, most bouts were observed within 3 h of sunset. By comparison, basking occurred much more frequently in the morning. Basking and a shift towards diurnal foraging in winter is associated with a decrease in richness and abundance of predators. P. macdonnellensis appears to compensate for the occurrence of torpor during the active phase (i.e. night) in winter by changing activity patterns such that foraging commences during what is usually the rest phase. These activity patterns are not expected to occur during the remainder of the year.
... Sengis are well known for their ability to lower their body temperature in response to low ambient temperatures (i.e. torpor, Mzilikazi & Lovegrove 2005) and lower body temperatures could also impair the feeding ability of ticks. In the study species, such torpor bouts increase in frequency and depth during cold periods (Mzilikazi & Lovegrove 2004) and consequently, the feeding duration of ticks may be prolonged during this period of the year. ...
Ticks are important vectors of pathogens of medical and veterinary importance worldwide. In spite of their economic importance, our current knowledge about the factors affecting tick prevalence and abundance in tropical and subtropical regions is rather limited. Both abiotic (e.g. temperature) as well as biotic variables (e.g. host sex) have been identified as key determinants of distributions. Eastern rock sengis or elephant shrews (Elephantulus myurus, Macroscelidea: Cacroscelididae, Thomas & Schwann) are widely distributed throughout Africa and can harbour a large number of tick species and substantial tick burdens. In the present study, we evaluated the contribution of climate and host factors on tick burdens of sengis. Throughout the year sengis carried high abundances of immature stages of a single tick species, Rhipicephalus sp. near warburtoni. There was no evidence that host parameters affected tick burdens. However, larval abundance decreased with increasing ambient temperatures and both larvae and nymphs were negatively affected by rainfall 2 months before the sampling month. In addition, nymphal burdens decreased with increasing minimum temperatures. Our results suggest that climate factors are the largest constraint for the immature stages of R. sp. near warburtoni and that eastern rock sengis could play a crucial role in the dynamics of tick-borne diseases as a result of the large tick burdens they can sustain.
... exhibits less variation) in placental mammals and passerine birds, compared with monotremes and ratites, respectively [16,71,72]. This pattern is also supported by more sophisticated comparisons, as well as in other traits [16,[72][73][74][75]. In fact, recent sequencing of the platypus genome revealed that many apparently reptilian phenotypic attributes (e.g. ...
During the past 30 years, the evolution of endothermy has been a topic of keen interest to palaeontologists and evolutionary physiologists. While palaeontologists have found abundant Permian and Triassic fossils, suggesting important clues regarding the timing of origin of endothermy, physiologists have proposed several plausible hypotheses of how the metabolic elevation leading to endothermy could have occurred. More recently, molecular biologists have developed powerful tools to infer past adaptive processes, and gene expression mechanisms that describe the organization of genomes into phenotypes. Here, we argue that the evolution of endothermy could now be elucidated based on a joint, and perhaps unprecedented, effort of researchers from the fields of genomics, physiology and evolution.
... One of the most striking features of D. gliroides that we have found, however, was the low consistency in the regulation of T B (see also Cortes et al. 2009) and the amplitude in T B it exhibits when normothermic. These patterns, together with the opportunistic torpor that Dromiciops exhibits, have also been observed in other species whose origins are located basally in the phylogeny of mammals, such as tenrecs (Echinops telfairi) (Lovegrove and Genin 2008), elephant shrews (Elephantus myurus) (Mzilikazi and Lovegrove 2005) and echidnas (Tachyglossus aculeatus) (Nicol and Andersen 2007). In fact, some authors have referred to these species as the ''protoendotherms'' (Lovegrove and Genin 2008; Mzilikazi and Lovegrove 2006), proposing that they could be good models for studying some aspects of the evolution of endothermy. ...
Torpor is the physiologically controlled reduction of metabolic rate and body temperature experienced by small birds and mammals when facing periods of low temperature and/or food shortage. In this study, we provide a first quantitative description of torpor in the relict marsupial Dromiciops gliroides by: (1) characterizing body temperature (T
B) and torpor patterns, (2) evaluating the combined effects of ambient temperature and different levels of food restriction on torpor incidence and (3) exploring the metabolic depression during torpor. D. gliroides exhibited short bouts of torpor on a daily basis, during which T
B decreased close to ambient temperature. During the active phase, T
B also exhibited pronounced variation (range 34–38°C). In order to evaluate the consistency of torpor, we computed the repeatability of T
B. Using the whole dataset, repeatability was significant (τ = 0.28). However, when torpid individuals were excluded from the analysis, repeatability was non-significant: some individuals were more prone to experience torpor than others. Our results indicate that this species also exhibits short bouts of daily torpor, whose depth and duration depends on the joint effects of T
A and food availability. At T
A = 20°C, the maximum torpor incidence was found at 70–80% food reduction, while at both extremes of the food continuum (100 and 0–10% food reduction) individuals were completely active, although considerable variation in T
B was recorded. At T
A = 10°C, individuals developed a deep form of torpor that was independent of the amount of food provided. On average, torpid D. gliroides reduced their metabolic rate up to 92% of their active values. In general, our results suggest that T
A was the most immediate determinant of torpor, followed by energy availability.
... Although possibly not a typical energy saving mechanism employed, it does suggest that this species is capable of tolerating and making use of the mechanism. A drop in T b during periods of activity particularly in winter would incur a similar energetic advantage to the drop during periods of inactivity and has been shown in elephant shrews[56], providing an energetic benefit by reducing the T b –T a gradient during the coldest part of the night[57]. We expected the R t to be greater than the value predicted by Ashoff's[8]allometric equation since some mammals may lower theirT b during their rest phase when exposed to low T a s[4]as a mechanism of conserving energy, resulting in increased amplitudes of T b. ...
Since Black-tailed Tree Rats, Thallomys nigricauda, face variable thermal environments in their extensive range in southern Africa, variation in their physiological and behavioural responses to the wide range of ambient temperatures (T(a)s) was expected to play a role in the success and range of the species. Body temperature (T(b)) and activity patterns of free-ranging Tree Rats were investigated during winter and summer at three study sites along an aridity gradient. We measured abdominal T(b) using implanted iButtons. All but three Tree Rats displayed significant 24h T(b) rhythmicity. The T(b) range for Tree Rats was 32.33-40.63 degrees C (n=13) and 32.69-40.15 degrees C (n=17) in winter and summer respectively. Although there was variation in T(b) profiles, Tree Rats generally displayed a bimodal distribution of T(b), with high and low T(b) values during scotophase and photophase respectively. Site had no effect on the range of T(b) in winter. Range in T(b) was significantly greater in winter, when Tree Rats reduced their minimum T(b). Maximum amplitudes of daily rhythms of T(b) were 259.7% of expected values. Temperatures of cavities were more stable compared with operative temperature. In winter male Tree Rats spent a significantly greater proportion of the active phase away from their home cavity compared with females. It is suggested that the energy savings in Tree Rats are a result of a combination of physiological and behavioural mechanisms allowing them to maintain nocturnal activity in winter and overall energy balance.
... During overcast/rainy weather when soil and burrows did not heat up during the day and passive rewarming was not possible, arousals were on average delayed, and then torpor was occasionally extended to dusk. The patterns of early arousal from torpor probably facilitated by high afternoon T a 's are shared by all arid zone dasyurids studied to date and also by some small African heterothermic mammals (Geiser 1986; Geiser and Baudinette 1988; Lovegrove and Raman 1998; Lovegrove et al. 1999; Schmid 2000; Geiser et al. 2002; Mzilikazi and Lovegrove 2005; Warnecke et al. 2008). After arousal, normothermic mulgaras could select mild, energy-conserving conditions along their burrow system, given that on sunny days T soil close to the surface continues to rise. ...
Little is known about the energy conservation strategies of free-ranging marsupials living in resource-poor Australian deserts. We studied activity patterns and torpor of free-living mulgaras (Dasycercus blythi) in arid central Australia during the winter of 2006. Mulgaras are small (approximately 75 g), nocturnal, insectivorous marsupials, with a patchy distribution in hummock grasslands. Mulgaras (six males, three females) were implanted intraperitoneally with temperature-sensitive transmitters and monitored for 6-55 d. Temperature profiles for different microhabitats and the thermal properties of soil and a number of burrows were also measured. Air temperature ranged from -3 degrees C at night to 30 degrees C during the day. Although burrows buffered temperature extremes, the thermal diffusivity of the sandy soil was high, and many burrows were shallow. Hence, soil and burrow temperatures averaged about 15 degrees C. The activity of mulgaras was often restricted to a few hours after sunset, before they retired into their burrows. Mulgaras employed torpor frequently, often entering torpor during the night and arousing around midday, with arousals occurring later on cooler days. Shallow burrows allowed cooling below mean T(soil). Consequently, body temperatures as low as 10.8 degrees C were observed. The longest torpor bout was 20.8 h. Torpor patterns changed seasonally and differed between males and females. From June to August, females entered torpor almost daily despite mating and gestation, but from the end of the gestation period onward, they remained normothermic. In contrast, males showed only shallow and short torpor during the mating season, but from mid-July, a transition to more frequent and deeper torpor resembling that of females was observed. Apparently, in both sexes, the reproductive effort entails energetic costs, but torpor, as an energy-saving mechanism, and reproduction are not exclusive in mulgaras. In a resource-poor environment during the least productive part of the year, frequent torpor seems to provide the means to compensate for the increased energetic costs associated with reproduction.
Core body temperature ( T c ) is a critical aspect of homeostasis in birds and mammals and is increasingly used as a biomarker of the fitness of an animal to its environment. Periodogram and cosinor analysis can be used to estimate the characteristics of the circadian rhythm of T c from data obtained on loggers that have limited memory capacity and battery life. The sampling interval can be manipulated to maximise the recording period, but the impact of sampling interval on the output of periodogram or cosinor analysis is unknown. Some basic guidelines are available from signal analysis theory, but those guidelines have never been tested on T c data. We obtained data at 1‐, 5‐ or 10‐min intervals from nine avian or mammalian species, and re‐sampled those data to simulate logging at up to 240‐min intervals. The period of the rhythm was first analysed using the Lomb–Scargle periodogram, and the mesor, amplitude, acrophase and adjusted coefficient of determination ( R ² ) from the original and the re‐sampled data were obtained using cosinor analysis. Sampling intervals longer than 60 min did not affect the average mesor, amplitude, acrophase or adjusted R ² , but did impact the estimation of the period of the rhythm. In most species, the period was not detectable when intervals longer than 120 min were used. In all individual profiles, a 30‐min sampling interval modified the values of the mesor and amplitude by less than 0.1°C, and the adjusted R ² by less than 0.1. At a 30‐min interval, the acrophase was accurate to within 15 min for all species except mice. The adjusted R ² increased as sampling frequency decreased. In most cases, a 30‐min sampling interval provides a reliable estimate of the circadian T c rhythm using periodogram and cosinor analysis. Our findings will help biologists to select sampling intervals to fit their research goals.
Hibernation is a widespread metabolic strategy among mammals for surviving periods of food scarcity. During hibernation, animals naturally alternate between metabolically depressed torpor bouts and energetically expensive arousals without ill effects. As a result, hibernators are promising models for investigating mechanisms that buffer against cellular stress, including telomere protection and restoration. In non-hibernators, telomeres, the protective structural ends of chromosomes, shorten with age and metabolic stress. In temperate hibernators, however, telomere shortening and elongation can occur in response to changing environmental conditions and associated metabolic state. We investigate telomere dynamics in a tropical hibernating primate, the fat-tailed dwarf lemur (Cheirogaleus medius). In captivity, these lemurs can hibernate when maintained under cold temperatures (11–15 °C) with limited food provisioning. We study telomere dynamics in eight fat-tailed dwarf lemurs at the Duke Lemur Center, USA, from samples collected before, during, and after the hibernation season and assayed via qPCR. Contrary to our predictions, we found that telomeres were maintained or even lengthened during hibernation, but shortened immediately thereafter. During hibernation, telomere lengthening was negatively correlated with time in euthermia. Although preliminary in scope, our findings suggest that there may be a preemptive, compensatory mechanism to maintain telomere integrity in dwarf lemurs during hibernation. Nevertheless, telomere shortening immediately afterward may broadly result in similar outcomes across seasons. Future studies could profitably investigate the mechanisms that offset telomere shortening within and outside of the hibernation season and whether those mechanisms are modulated by energy surplus or crises.
Given their relatively small body size, high thermoregulatory costs, and low metabolic rate, we tested the hypothesis that red squirrels (Tamiasciurus hudsonicus) would employ bouts of daily torpor to save energy during winter. We collected data on body temperature (T-b) using surgically implanted data loggers for squirrels in the Cypress Hills region of Saskatchewan, where extended periods of cold snowy weather make foraging difficult and should lead to high levels of energy expenditure. Based on over 8000 measurements from 4 animals over 3 winters, we found no evidence for torpor use. However, T-b was lowest in January and highest in September and May, and mean monthly T-b was correlated with mean monthly ambient temperature (T-a). Given that taxonomically related species can and do use torpor, it remains to be determined what makes heterothermy in this species costly to the extent that its use is precluded.
We investigated locomotor activity rhythms in the little‐studied wild‐caught eastern rock sengi (Elephantulus myurus) from Goro Game Reserve, Limpopo Province, South Africa. To assess whether locomotor activity is endogenously entrained by the light–dark cycle, animals (n = 13) were subjected to three different light‐cycle regimes: a 12 h light/12 h darkness (LD) cycle, a total darkness (DD) cycle and an inverse of the LD cycle (DL). Ten animals exhibited strong light entrainment under LD1 with the total percentage of activity during the light phase (56.5% ± 11.9%) significantly higher than during the dark phase (43.5% ± 11.9%). Eleven animals expressed distinct endogenous free‐running rhythms under DD (mean τ = 23.6 h ± 0.6 h; range: 22.9 h–24.5 h), with significant inter‐individual variation. Under DL, the total percentage of activity was approximately equal during the light (50.4% ± 7.8%) and dark phase (49.6% ± 7.8%). E. myurus was on average active 25% of the 24‐h day with a nocturnal–diurnal ratio of 0.8 under LD1 and exhibited locomotor activity under controlled conditions similar to that of closely related species in the wild. In 62% of the animals, activity was highest around dawn, lowest during the afternoon and intermittently expressed throughout the night. Little quantitative data are available on the daily locomotor activity rhythms of sengis particularly in response to the light–dark cycle. This study provides valuable quantitative data on locomotor activity rhythms in E. myurus.
Throughout the Cenozoic, the fitness benefits of the scrotum in placental mammals presumably outweighed the fitness costs through damage, yet a definitive hypothesis for its evolution remains elusive. Here, I present an hypothesis (Endothermic Pulses Hypothesis) which argues that the evolution of the scrotum was driven by Cenozoic pulses in endothermy, that is, increases in normothermic body temperature, which occurred in Boreotheria (rodents, primates, lagomorphs, carnivores, bats, lipotyphylans and ungulates) in response to factors such as cursoriality and climate adaptation. The model argues that stabilizing selection maintained an optimum temperature for spermatogenesis and sperm storage throughout the Cenozoic at the lower plesiomorphic levels of body temperature that prevailed in ancestral mammals for at least 163 million years. Evolutionary stasis may have been driven by reduced rates of germ-cell mutations at lower body temperatures. Following the extinction of the dinosaurs at the Cretaceous–Palaeogene boundary 65.5 mya, immediate pulses in endothermy occurred associated with the dramatic radiation of the modern placental mammal orders. The fitness advantages of an optimum temperature of spermatogenesis outweighed the potential costs of testes externalization and paved the way for the evolution of the scrotum. The scrotum evolved within several hundred thousand years of the K-Pg extinction, probably associated initially with the evolution of cursoriality, and arguably facilitated mid- and late Cenozoic metabolic adaptations to factors such as climate, flight in bats and sociality in primates.
Huddling is a behavioural energy conservation mechanism that is widely used by many small endotherms at low ambient temperatures. Huddling has many bene-fits, including decreasing the metabolic cost of maintaining body temperature (Tb), reducing the amount of heat lost to the environment, and increasing the local temperature of the nest. To test the effects of huddling on Tb , 10 rock hyrax, Procavia capensis, were housed in outside cages in four groups, varying from one to four individuals. iButtons ® were surgically implanted into each rock hyrax to record their Tb every 15 min from August to November. Despite considerable variations in ambient temperatures, the rock hyrax were found to display some degree of heterothermy by varying their mean Tb from 36.70 to 37.72°C (n = 10) but not allowing it to drop below 33.60°C or rise above 39.67°C. Contrary to what was predicted, rock hyrax did not display any significant effects of huddling on Tb , irrespective of group size.
Boyles et al. (this issue) argue against the use of body temperature (Tb) thresholds to quantify the expression of torpor in endotherms and our purpose is to provide a counterpoint argument. We contend that Tb thresholds provide valuable information about ecological factors influencing the evolution of thermoregulation. We also point out shortcomings of the so-called heterothermy index proposed as an alternative. However, to be clear, we do agree with Boyles et al. (this issue) that the use of torpor thresholds can limit some aspects of the study of thermoregulation and applaud the more widespread incorporation of theoretical underpinnings proposed by Boyles et al. (this issue) and others.
Torpor bouts of elephant shrews are intermediate in duration to those of daily heterotherms and hibernating mammals, but their body temperatures (T(b)s) and metabolic rates are very low and similar to those of hibernating mammals. We quantified the thermal physiology of the Cape rock elephant shrew (Elephantulus edwardii), a species endemic to high-altitude regions of South Africa, where winters are cold and wet, and tested whether it displays multiday torpor characteristic of hibernators at low ambient temperature (T(a)). E. edwardii regularly displayed torpor over a wide range of T(a)s. Occurrence of torpor and duration of torpor bouts increased with decreasing T(a). Whereas normothermic T(b) was stable, T(b) in torpid individuals fell with T(a). The mean T(b) - T(a) differential at the minimum T(b) was 0.7 degrees C, and the mean minimum T(b) at T(a) 8.9 degrees C was 9.3 degrees C. Duration of torpor bouts ranged from 6.5 to 44 h and was correlated negatively with T(a) and T(b) during torpor. Time required for the reduction of T(b) to a T(b) - T(a) differential of < 2.0 degrees C was faster for > 1-day torpor bouts than those lasting <= 1 day, suggesting that the duration of a bout might be determined at the beginning, not during, a bout. The nature of heterothermy in E. edwardii seems qualitatively similar to that of other elephant shrews, although torpor is somewhat deeper and longer in this species. Temporal patterns of torpor in E. edwardii differ from those of most cold-climate hibernators, likely for ecological rather than physiological reasons.
We report on the seasonal metabolic adjustments of a small-sized member of the phylogenetically ancient Afrotheria, the Western rock elephant shrew (Elephantulus rupestris). We recorded body temperature (T (b)) patterns and compared the capacity for adrenergically induced nonshivering thermogenesis (NST) in E. rupestris captured in the wild in summer and winter. Noradrenaline (NA) treatment (0.4-0.5 mg/kg, s.c.) induced a pronounced elevation in oxygen consumption compared to controls (saline), and the increase in oxygen consumption following injection of NA was 1.8-fold higher in winter compared to summer. This suggests that the smaller members of Afrotheria possess functional brown adipose tissue, which changes in thermogenic capacity depending on the season. Torpor was recorded in both seasons, but in winter the incidence of torpor was higher (n = 205 out of 448 observations) and minimal T (b) during torpor was lower (T (b)min: 11.9°C) than in summer (n = 24 out of 674 observations; T (b)min: 26°C). In addition to cold, high air humidity emerged as a likely predictor for torpor entry. Overall, E. rupestris showed a high degree of thermoregulatory plasticity, which was mainly reflected in a variable timing of torpor entry and arousal. We conclude that E. rupestris exhibits seasonal metabolic adjustments comparable to what has been long known for many Holarctic rodents.
The distribution of parasites is often characterised by substantial aggregation with a small proportion of hosts harbouring the majority of parasites. This pattern can be generated by abiotic and biotic factors that affect hosts and determine host exposure and susceptibility to parasites. Climate factors can change a host's investment in life-history traits (e.g. growth, reproduction) generating temporal patterns of parasite aggregation. Similarly, host age may affect such investment. Furthermore, sex-biased parasitism is common among vertebrates and has been linked to sexual dimorphism in morphology, behaviour and physiology. Studies exploring sex-biased parasitism have been almost exclusively conducted on polygynous species where dimorphic traits are often correlated. We investigated the effects of season and life-history traits on tick loads of the monogamous eastern rock sengi (Elephantulus myurus). We found larger tick burdens during the non-breeding season possibly as a result of energetic constraints and/or climate effects on the tick. Reproductive investment resulted in increased larval abundance for females but not males and may be linked to sex-specific life-history strategies. The costs of reproduction could also explain the observed age effect with yearling individuals harbouring lower larval burdens than adults. Although adult males had the greatest larval tick loads, host sex appears to play a minor role in generating the observed parasite heterogeneities. Our study suggests that reproductive investment plays a major role for parasite patterns in the study species.
Thermocron iButton dataloggers are widely used to measure thermal microclimates experienced by wild animals. The iBBat is a smaller version of the datalogger, also commercially available, that is used to measure animal skin or core body temperatures when attached externally or surgically implanted. Field observations of bats roosting under a bridge suggested that bats avoided locations with iButtons. A heterodyne bat detector revealed that the dataloggers emitted ultrasound which was detectable from a distance of up to 30 cm. We therefore recorded and quantified the acoustic properties [carrier frequency (Hz) and root mean square sound pressure level (dB SPL)] of iButton and iBBat dataloggers. All units emitted a 32.9 kHz pure tone that was readily picked up with a time expansion bat detector at a distance of 1 cm, and most were detected at a distance of 15 cm. The maximum amplitude of iButton dataloggers was 46.5 dB SPL at 1.0 cm-a level within the range of auditory sensitivity for most small mammals. Wrapping iButtons in plastic insulation severely attenuated the amplitude of ultrasound. Although there was a statistically significant reduction in rates of warming and cooling with insulation, this effect was small and we suggest that insulation may be a viable solution to eliminate unwanted ultrasonic noise in instances when small delays in thermal response dynamics are not a concern. We recommend behavioural studies to assess if the electronic signals emitted by iButtons are disturbing to small mammals.
The evolution of endothermy is thought to have been facilitated by the advent of endothermic energy sources such as brown adipose tissue (BAT), the principal site of non-shivering thermogenesis (NST). In marsupials, heat is primarily produced through shivering and NST in skeletal muscle because BAT is either absent or appears to be non-functional. The most basal group of the eutherian lineage are the Afrotheria. Rock elephant shrews, Elephantulus myurus are amongst the smallest members of the Afrotheria and are also known to use exogenous passive heating. The aim of this study was to determine whether the reliance on passive heating compromised the capacity for thermogenesis in E. myurus. We measured the thermogenic response to noradrenalin (NA) injection in E. myurus acclimated to short photoperiod. The thermogenic response at 25 degrees C was 1.58 ml O(2) g(-1) h(-1). We used phylogenetically independent analyses to establish how this thermogenic response compared to other eutherians that display classical NST. The thermogenic response of E. myurus was not significantly different from phylogenetically independent allometric predictions. However, it is unclear whether this thermogenic response is indicative of classical NST and molecular data are required to verify the presence of BAT and UCPs in elephant shrews.
Uncoupling protein 1 (UCP1) mediated nonshivering thermogenesis (NST) in brown adipose tissue (BAT) is an important avenue of thermoregulatory heat production in many mammalian species. Until recently, UCP1 was thought to occur exclusively in eutherians. In the light of the recent finding that UCP1 is already present in fish, it is of interest to investigate when UCP1 gained a thermogenic function in the vertebrate lineage. We elucidated the basis of NST in the rock elephant shrew, Elephantulus myurus (Afrotheria: Macroscelidea). We sequenced Ucp1 and detected Ucp1 mRNA and protein restricted to brown fat deposits. We found that cytochrome c oxidase activity was highest in these deposits when compared with liver and skeletal muscle. Consistent with a thermogenic function of UCP1 isolated BAT mitochondria showed increased state 4 respiration in the cold, as well as palmitate-induced, GDP-sensitive proton conductance, which was absent in liver mitochondria. On the whole animal level, evidence of thermogenic function was further corroborated by an increased metabolic response to norepinephrine (NE) injection. Cold acclimation (18 degrees C) led to an increased basal metabolic rate relative to warm acclimation (28 degrees C) in E. myurus, but there was no evidence of additional recruitment of NE-induced NST capacity in response to cold acclimation. In summary, we showed that BAT and functional UCP1 are already present in a member of the Afrotheria, but the seasonal regulation and adaptive value of NST in Afrotherians remain to be elucidated.
The patterns of heterothermy were measured in Lesser Hedgehog Tenrecs, Echinops telfairi, under semi-natural conditions in an outdoor enclosure during the austral mid-winter in southwestern Madagascar. The animals were implanted with miniaturized body temperature (T
b) loggers (iButtons) that measured body temperature every 42 min for 2 months (May and June). The tenrecs entered daily torpor on all 60 consecutive days of measurement, that is, on 100% of animal days, with body temperature closely tracking ambient temperature (T
a) during the ambient heating phase. The mean minimum daily T
b of the tenrecs was 18.44 ± 0.50°C (n = 174, N = 3), and never exceeded 25°C whereas, apart from a few hibernation bouts in one animal, the mean maximum daily T
b was 30.73 ± 0.15°C (n = 167, N = 3). Thus during winter, tenrecs display the lowest normothermic T
b of all placental mammals. E. telfairi showed afternoon and early evening arousals, but entered torpor before midnight and remained in torpor for 12–18 h each day. One animal hibernated on two occasions for periods of 2–4 days. We consider E. telfairi to be a protoendotherm, and discuss the relevance and potential of these data for testing models on the evolution of endothermy.
The maximum amplitudes of circadian rhythms of body temperature (R(t)) of three species of desert rodents inhabiting an arboreal-subterranean gradient were correlated with habitat-dependent thermoregulatory parameters such as minimal thermal conductance and the magnitude of ambient temperature tolerance by endotherms. It was shown that R(t) differed by 87-181% of expected values. The data for two rodents (Thallomys paedulcus and Aethomys namaquensis) that forage aboveground displayed higher-than-expected R(t) values, whereas the strictly subterranean species (Cryptomys damarensis) had lower-than-expected R(t) values. These data are interpreted in terms of the Endothermic Temperature Range Hypothesis, which argues that the large range of diel ambient temperature fluctuations found in desert habitats may account for the physiological parameters that generate the higher-than-expected body temperature rhythms, a low and fairly inflexible minimal thermal conductance and low resting metabolic rate. Further discussion centres on the possible functional significance of circadian energetic rhythms, particularly in terms of an endotherm's fitness. It is proposed that, at least, functions of the rhythms should be considered: diel thermoregulatory adjustments and energy conservation.
Hibernation and daily torpor are usually considered to be two distinct patterns
of heterothermia. In the present comparison we evaluated (1) whether physiologi- cal variables of torporfrom 104 avian and mammalian species warrant the dis- tinction betweenzhibernation and daily torpor as two different states of torpor and (2), if so, whether this distinction is best based on maximum torpor bout du- ration, minimum hody3temperature (Tb), minimum metabolic rate during tor-
por, or the reductionz of metabolic rate expressed aspercentage of basal metabo-
lism Initially, animals grouped into species displaying either daily (HBMR). uwere
torpor or prolonged torpor (bibernation) according to observations from original sources. Both cluster and discriminant analyses supported this division, and fur- ther analyses uwerethere/forebased on these tuwogroups. Frequency distributions
for all tvariables tested difiered significantly (P < 0.001i) between daily torpor and hibernation. The average maximum torpor bout duration was 355.3 h in hiber- nators and 11.2 h inzdaily heterotherms. Mean minimum Tb'swere lower in hi- bernators than inl daily heterotherms (5.80 C zs. 17.4 C) as were minimum meta- bolic rates measured as rate of oxygen consumption (Vo2; 0.037 vs. 0.535 mL 02 g~'h'), and the metabolic rate reduction expressed aspercentage ofBMR (5.1% vs. 29. 5%). Furthermore, mean body uweightswere significantly higher in hbiberna- tors (2384 g) than inzdaily heterotherms (253 g; P < 0.001). Thus, the compari- sons of sei eral phy3siological ,ariables appear to justify a distinction between the tu'o torporpatterns. Houweier, of all iariables tested, only thefrequency distribu- tions of maximum torpor bout duration (1. 5-22 hfor daily torpor; 96-1,080 hfor hibernationz) shouweda clear gap between daily heterotherms and hibernators.
Summary
1.
Body temperatures (T
b) and rates of oxygen consumption (
) during torpor of the insectivorous marsupialSminthopsis macroura were determined at different ambient temperatures (T
a) and photophases.
2.
Torpor was observed in the morning and usually commenced before the onset of dawn. In the afternoon animals were normothermic.
The duration of torpor was usually between 3 and 9 h with a maximum of 17 h and 15 min.
3.
All animals entered torpor spontaneously at aT
a of 13°C, but if food was withheld torpor was induced below 17°C.
4.
An increase in
andT
b during torpor was observed below aT
a of about 12°C. The body temperature below which endothermic arousal is no longer possible (the critical arousal temperature)
was less than 15.1°C.
5.
An eight hour phase shift of the dark-light cycle resulted in a corresponding shift in the diurnal torpor-activity cycle and
it appears that light is an important cue for the timing of daily torpor.
Circadian metabolic responses to food deprivation were measured in Black-shouldered Kites (Elanus caeruleus) at thermoneutral and cold ambient temperatures. The basal metabolic rate (BMR) of the kites was 60-70% of that predicted by various allo-metric equations. They displayed marked circadian rhvthms of BMR and bodv temuerature (T,). but did _ . ,,I not show any indication of metabolic depression or adaptive hypothermia in response to food deprivation. Instead, moderate reductions in metabolic rate and T, were observed, resulting in significant reductions in the daily energy expenditure. The conservative meta-bolic traits shown by the kites and their responses to food deprivation suggest tolerance of periodic, limited food supplies.
1.
Body temperatures (T
b), rates of oxygen consumption (
[(V)\dot]O2 \dot V_{O_2 }
) and the loss in body mass of the small insectivorous dasyurid marsupialAntechinomys laniger were determined at different ambient temperatures (T
a).
2.
Most animals entered torpor belowT
a 27C when food was witheld. Spontaneous torpor was observed frequently atT
a 19 and 12.5C.
3.
An increase in
[(V)\dot]O2 \dot V_{O_2 }
and [(V)\dot]O2 \dot V_{O_2 }
during torpor belowT
a 11C was parallel to theT
a related increased in metabolism of normothermic resting, active, and arousing animals.
5.
Torpor lasted between 2 and 16 h and the longest durations were observed atT
a 13–20C; below and above this temperature range torpor bouts were shorter.
6.
The lowest relative weight loss was observed at theT
a of the longest torpor bouts and lowest metabolism during torpor.
7.
Both the time of the activity peaks and onset of torpor were dependent onT
a and were observed later in the night at higherT
a. Torpor commenced before the onset of light.
8.
Arousal rates were rapid and the arousal times increased exponentially with decreasing Ta.
In the laboratory rock elephant shrews (Elephantulus myurus; mean body mass 56.6 g) displayed the lowest torpor T
b min yet recorded (ca. 5°C) in a placental daily heterotherm. It was unknown whether these low T
bs were characteristic of daily heterothermy in free-ranging animals. It was also unclear how cost effective these low T
bs were since considerable energy is required to arouse from low T
bs on a daily basis. We continuously measured body temperature once every hour for 85 days in 13 free-ranging E. myurus from May to August 2001 (winter) in Weenen Game Reserve, KwaZulu-Natal, South Africa. We recorded a total of 412 torpor bouts. Free-ranging E. myurus had a high propensity for torpor with females displaying higher torpor frequency than males. The lowest T
b recorded was 7.5°C at T
a=2.7°C and the minimum torpor T
b was strongly correlated with ambient temperature. Torpor arousal was tightly coupled with ambient temperature cycles. Low torpor T
b min at low T
as was therefore cost-effective because the animals offset the high cost of arousal through exogenous passive heating. Laboratory studies under constant ambient temperatures may therefore underestimate the energetic benefits of torpor in free-ranging small mammals that inhabit regions where seasonality is moderate.
Two species of the genus Acomys coexist in arid zones of southern Israel. Acomys russatus is distributed in extremely arid areas, while A. cahirinus is common in both Mediterranean and arid regions. Individuals of both species from a rodent community in the Ein Gedi Nature Reserve were implanted with temperature-sensitive transmitters. Body temperature (T
b) rhythms were recorded in free-ranging mice at four different seasons of the year. A. cahirinus (30–45 g) showed a nocturnal rhythm of T
b throughout the year. In the activity phase during the night T
b increased to 38.2°C. During the day T
b decreased to 34°C. This species displayed this pattern in summer also when ambient temperatures rose above T
b. The T
b of A. russatus (45–65 g) varied between 34.8 and 41°C during the hot season, showing a bimodal temperature rhythm with maximal values in the morning and in the evening. Measurements of activity in this species showed inactivity during the hottest period of a summer day. In winter A. russatus showed no clearly detectable diurnal or ultradian rhythm in T
b, which remained constant between narrow limits of 35.2 and 36.8°C.
The aim of this study was to describe the regular annual pattern of the daily melatonin synthesis in Djungarian hamsters, Phodopus sungorus sungorus. The hamsters were maintained from birth in natural photoperiodic conditions and in bimonthly intervals the day/night rhythms of pineal N-acetyltransferase (NAT) were measured. Analysis of the circadian profiles of NAT activity showed that the duration of elevated melatonin synthesis closely reflects the duration of the scotophase throughout the seasons. Thus the duration of elevated melatonin seems to represent a direct humoral signal transmitting the photoperiodic message. The duration of the nightly melatonin pulse appears to be influenced mainly by the time of dawn rather than by the time of dusk. Additional information about the time of year might be encoded in the total amount of melatonin synthesized per day, whereas the amplitude of the nightly melatonin peak seems to be of minor importance.
Patterns of spontaneous and induced daily torpor were measured in the Afrotropical pouched mouse (77-115 g), Saccostomus campestris, in response to photoperiod, temperature, and food deprivation, using temperature telemetry. Photoperiod had no influence on the incidence, depth, or duration of daily torpor in either males and females. Although the testis size index decreased in response to food deprivation and photoperiod by a maximum of 24%, full testis regression did not occur. Torpor bout duration was, on average, 5.3 h, independent of photoperiod and ambient temperature. Males did not enter torpor in response to food deprivation but did in response to low ambient temperature, though significantly less frequently than females. At normothermia, the body temperatures (daily minimum, mean, maximum) of males were significantly lower than those of females. Minimum body temperatures of both males and females during torpor did not fall below 20 degrees C at an ambient temperature of 15 degrees C. The patterns of torpor measured here differ from those observed in species from strongly seasonal environments. They suggest adaptation to an environment rendered unpredictable by the El Niño Southern Oscillations. As an aseasonal, opportunistic breeder capable of year-round adaptive hypothermia, the pouched mouse represents an excellent model animal for research on physiological and behavioral adaptations to unpredictable environments.
The costs of arousal from induced torpor were measured in the striped-faced dunnart (Sminthopsis macroura, ca. 25 g) under two experimental ambient temperature cycles. The sinusoidal-type temperature cycles were designed to evaluate the effects of passive, ambient temperature heating during arousal from torpor in these insectivorous marsupials. It was hypothesised that diel ambient temperature cycles may offer significant energy savings during arousal in animals that employ daily torpor in summer as a response to unpredictable food availability. The cost of arousal in animal in which passive, exogenous heating occurred was significantly lower than that in animals not exposed to an ambient temperature cycle. The total cost of all three phases of torpor (entry maintenance and arousal) was almost halved when animals were exposed to an ambient heating cycle from 15 degrees C to 25 degrees C over a 24-h period. In all animals, irrespective of the experimental ambient temperature cycle employed, the minimum torpor body temperature was 17-18 degrees C. The body temperature (Tb) of animals exposed to exogenous heating increased from the torpor Tb minimum to a mean value of 22.59 degrees C before endogenous heat production commenced. This relatively small increase in Tb of ca. 5 degrees C through 'free' passive heating was sufficient to account for the significant ca. three-fold decrease in the cost of arousal and may represent an important energetic aid to free-ranging animals.
The characteristics of daily torpor were measured in the round-eared elephant shrew Macroscelides proboscideus (Macroscelidea) in response to ambient temperature and food deprivation. Elephant shrews are an ancient mammal order within a superordinal African clade including hyraxes, elephants, dugongs and the aardvark. M. proboscideus only employed torpor when deprived of food; torpor did not occur under an ad libitum diet at ambient temperatures of 10, 15 and 25 degrees C. Torpor bout duration ranged from < 1 h to ca. 18 h. The times of entry into torpor were restricted to the scotophase, despite normothermic body temperature patterns indicating a rest phase coincident with the photophase. Full arousal was always achieved within the first 3 h of the photophase. When food deprived, the onset of the rest phase, and hence torpor, advanced with respect to the experimental photoperiod. The lowest torpor body temperature measured was 9.41 degrees C. Daily torpor in M. proboscideus confirms a pleisiomorphic origin of daily heterothermy. Torpor facilitates risk-averse foraging behaviour in these small omnivores by overcoming long-term energy shortfalls generated by the inherent variability of food availability in their semiarid, El Niño-afflicted habitats.
With the exception of some data for common poorwills (Phalaenoptilus nuttallii) and anecdotal reports for a few other species, knowledge about the use of torpor by free-ranging birds is limited. Our study was designed to assess the use of torpor by free-ranging Australian owlet-nightjars (Aegotheles cristatus). We selected this species for study because of their relatively small body size (50 g), arthropod diet, nocturnal sedentary nature, taxonomic affiliation with other birds for whom the use of torpor is well documented, use of cavity roosts, and because of the cold winter (mean July minimum ambient temperature [T(a)] of approximately 0 degrees C) in the study area. We tracked 12 owlet-nightjars carrying temperature-sensitive transmitters for a total of 906 bird-days (range of 15-115 d per individual). Five different individuals entered torpor on 96 d in total. Torpor bouts occurred only between May 8 and September 8, the coldest period of the year. The lowest skin temperature (T(skin)) recorded for any bird was 19.6 degrees C, and the lowest core temperature was 22.4 degrees C. Surprisingly, torpor was rarely used at night because birds usually foraged then. Instead, torpor typically began near dawn, even on cold nights. Torpor bouts beginning at dawn lasted approximately 4 h. On 36% of days when torpor was used at dawn, birds reentered torpor later in the day. Torpor was not used during the breeding season, but this period also corresponds to the warm part of the year. There were no distinct daily minimum, maximum, or mean T(a) thresholds that could be used to reliably distinguish days when dawn torpor was used from those when it was not, although torpor was commonly employed when daily minimum T(a) fell below 3.9 degrees C. Our results show that even though Australia is typically thought of as a warm continent, at least some of the avifauna use torpor as a regular means of saving energy. We hypothesise that the reasons for this species' use of torpor include its ability to remain active all night foraging, either for terrestrial arthropods while walking or for flying insects taken on the wing, and/or its habit of roosting in cavities, which allows them to remain hidden in the daytime.
Patterns of daily torpor were measured in response to photoperiod and food restriction at a constant temperature (18 degrees C) in two species of elephant shrew (Macroscelidea), Elephantulus rozeti (from Morocco) and Elephantulus myurus (from southern Africa). Body temperature was monitored continuously for ca. 3 months using temperature-sensitive telemeters. Under short photoperiods (8:16 L:D), both species entered spontaneous torpor on an ad libitum diet, but showed a higher frequency of induced torpor when food was restricted. Under long photoperiods (16:8 L:D), E. myurus could be induced to enter daily 'summer' torpor. A total of 378 torpor bouts were measured, none of which were longer in duration than 18 h. Under short photoperiods, arousal from torpor was associated with the onset of the photoperiod, whereas the time of entry was variable throughout the scotophase. However, E. myurus tended to phase shift torpor from the photophase to the scotophase under long photoperiods, despite displaying weak circadian amplitudes of body temperature indicative of a photophase rest phase. Both species lacked well-defined circadian amplitudes of body temperature, a pattern thought to be associated with polyphasic activity cycles characteristic of several Elephantuluis species. It was concluded that these and other patterns of torpor shown by Elephantulus show similarities with other small Afrotropical insectivores inhabiting semi-arid habitats or unpredictable environments.
The first mammals were small, nocturnal, and presumably had low metabolic rates and were therefore probably unable to maintain a constant high body temperature throughout cool nights. How these animals, without sufficient heat production for endogenous rewarming, were able to become warm and active again before the next activity period remains unresolved. However, we discovered that, similar to reptiles, the carnivorous marsupial mammal Pseudantechinus macdonnellensis (body mass 30.8 +/- 5.0 g) uses the morning sun to rewarm from low (26.3 +/- 4.5 degrees C) body temperatures during torpor. Our findings provide the first evidence of basking during rewarming from torpor in mammals and may provide an alternative explanation as to how ancestral mammals could have become nocturnal to avoid diurnal predators despite their small size and a low endogenous heat production.
Mechanisms that influence body temperature patterns in black-tailed prairie dogs are not well understood. Previous research on both free-ranging and laboratory populations of black-tailed prairie dogs (Cynomys ludovicianus) has suggested that reductions in ambient temperature and food and water deprivation are the primary factors that stimulate torpor in this species. In other species, however, torpor has been shown to be influenced by a multitude of factors, including innate circadian and circannual timing mechanisms, energy status, and reproductive behaviors. Our objective was to clarify the influence of weather, sex, and intrinsic timing mechanisms on the body temperature patterns of free-ranging black-tailed prairie dogs. We monitored body temperatures of eight adult (>1 yr) prairie dogs from November 1999 to June 2000. Prairie dogs showed distinct daily and seasonal body temperature patterns, which reflected changes in ambient temperatures that occurred during these periods. These patterns of daily and seasonal heterothermy suggest that body temperature patterns of black-tailed prairie dogs may be driven by an innate timing mechanism. All prairie dogs entered torpor intermittently throughout winter and spring. Torpor bouts appeared to be influenced by precipitation and reductions in ambient temperature. Our results also suggest that reproductive behaviors and circadian timing may influence torpor in this species.
Marsupials, unlike placental mammals, are believed to be unable to increase heat production and thermal performance after cold-acclimation. It has been suggested that this may be because marsupials lack functional brown fat, a thermogenic tissue, which proliferates during cold-acclimation in many placentals. However, arid zone marsupials have to cope with unpredictable, short-term and occasionally extreme changes in environmental conditions, and thus they would benefit from an appropriate physiological response. We therefore investigated whether a sequential two to four week acclimation in Sminthopsis macroura (body mass approx. 25 g) to both cold (16 degrees C) and warm (26 degrees C) ambient temperatures affects the thermal physiology of the species. Cold-acclimated S. macroura were able to significantly increase maximum heat production (by 27%) and could maintain a constant body temperature at significantly lower effective ambient temperatures (about 9 degrees C lower) than when warm-acclimated. Moreover, metabolic rates during torpor were increased following cold-acclimation in comparison to warm-acclimation. Our study shows that, despite the lack of functional brown fat, short-term acclimation can have significant effects on thermoenergetics of marsupials. It is likely that the rapid response in S. macroura reflects an adaptation to the unpredictability of the climate in their habitat.
The high expenditure of energy required for endogenous rewarming is one of the widely perceived disadvantages of torpor. However, recent evidence demonstrates that passive rewarming either by the increase of ambient temperature or by basking in the sun appears to be common in heterothermic birds and mammals. As it is presently unknown how radiant heat affects energy expenditure during rewarming from torpor and little is known about how it affects normothermic thermoregulation, we quantified the effects of radiant heat on body temperature and metabolic rate of the small (body mass 25 g) marsupial Sminthopsis macroura in the laboratory. Normothermic resting individuals exposed to radiant heat were able to maintain metabolic rates near basal levels (at 0.91 ml O(2) g(-1) h(-1)) and a constant body temperature down to an ambient temperature of 12 degrees C. In contrast, metabolic rates of individuals without access to radiant heat were 4.5-times higher at an ambient temperature of 12 degrees C and body temperature fell with ambient temperature. During radiant heat-assisted passive rewarming from torpor, animals did not employ shivering but appeared to maximise uptake of radiant heat. Their metabolic rate increased only 3.2-times with a 15- degrees C rise of body temperature (Q(10)=2.2), as predicted by Q(10) effects. In contrast, during active rewarming shivering was intensive and metabolic rates showed an 11.6-times increase. Although body temperature showed a similar absolute change between the beginning and the end of the rewarming process, the overall energetic cost during active rewarming was 6.3-times greater than that during passive, radiant heat-assisted rewarming. Our study demonstrates that energetic models assuming active rewarming from torpor at low ambient temperatures can substantially over-estimate energetic costs. The low energy expenditure during passive arousal provides an alternative explanation as to why daily torpor is common in sunny regions and suggests that the prevalence of torpor in low latitudes may have been under-estimated in the past.
The circadian pacemakers controlling activity rhythms in four species of rodents are compared, as freerunning systems in constant darkness. In analyzing their stability the distinction is made between spontaneous day to day instability of frequency, and a longer term lability, some of which is traceable to identified causes. Serial correlation analysis indicates that the precision (day to day stability) of the pacemaker's period is ca. twice as good (estimated s.d.=0.6% of mean tau in Mus musculus) as the already remarkable precision of the activity rhythm it drives (average s.d.=1.2% of mean tau). Identifiable causes of long term lability include age and several features of prior entrainment by light. The period and photoperiod of a light cycle have a predictable influence on the subsequent freerunning period (tau) of the pacemaker; they cause 'after effects'. So do single light pulses causing a phase shift in the freerunning system. Constant light also has an after effect opposite in sign from the after effect of long photoperiods. After effects of 'skeleton' periods support the hypothesis that the transitions of light to darkness vv. are involved in the entrainment process which leads to changes in tau. Both day to day instability and long term lability are most pronounced in species (Peromyscus maniculatus, Mus musculus) whose mean tau is considerably shorter than 24 h; they are least pronounced in hamsters whose mean tau is indistinguishably close to 24 h. The differences between the species in tau and its lability are paralleled by differences in pacemaker lability as measured in light induced after effects and in the extent of changes with age. The species evidently differ in the 'tightness' with which tau is homeostatically conserved.
For many years, investigators have questioned whether circadian rhythms continue to be expressed in mammals that hibernate when body temperature (Tb) is low. We have examined the circadian rhythm of Tb in marmots (Marmota flaviventris) under laboratory and field conditions during the winter hibernation period. Using temperature data loggers that were implanted in animals, Tb measurements were continuously recorded for up 2 years. We found that animals in the laboratory continued to manifest a circadian rhythm of Tb prior to hibernating, during deep hibernation, and after arousal from hibernation. Whereas animals in the field had robust circadian rhythms of Tb prior to hibernation, we were not able to detect a Tb rhythm during deep hibernation. We did find a diurnal rhythm of Tb once field animals had aroused for the last time in the spring and came above ground. In fact, we were able to determine when field animals must have been exposed to light, because they were entrained to the daily light-dark cycle. Our results suggest that in the laboratory, animals may be picking up cues and their Tb rhythm free-runs with a period close to 24hr. The fact that we found no circadian rhythm of Tb in our field animals that were in constant dark and very quiet conditions suggests that the circadian pacemaker is uncoupled from the Tb rhythm or is so damped that the output cannot be detected. We believe that circadian system is nonfunctional during deep hibernation under natural conditions.
This article argues that a positive engagement between Bourdieu’s sociology of practice and contemporary feminist theory would be mutually profitable. It compares Bourdieu’s account of the social construction of the human subject through practice with Butler’s account of subjectivity as performance. While the one, through the concept of habitus, tends towards an ‘overdetermined’ view of subjectivity in which subjective dispositions are too tightly tied to the social practices in which they were forged, the other pays insufficient attention to the social conditions of performative subversion. The second half of the paper looks at feminist studies of the relationship between class and gender which have drawn fruitfully on Bourdieu’s work, particularly on his concept of ‘cultural capital’, such as those of Moi and Skeggs.
1.1.|The circadian rhythm of rectal temperature and the sleep-wake cycle can persist independently of each other and of zeitgebers, and seem to be controlled by separate oscillators.2.2.|‘Masking’ of temperature by sleep or zeitgeber signals is to be distinguished from entrainment mechanisms.3.3.|Heat production and conductance coact in generating the temperature rhythm.4.4.|Circadian variations in system properties, as observed, e.g. in threshold, need to be confirmed in the absence of a sleep-wake (light-dark) cycle.
Circadian rhythms of metabolic rate and body temperature were measured in groups of huddling and solitary red-billed woodhoopoes (Phoeniculus
purpureus) as a function of ambient temperature. Basal metabolic rates were 30-60% lower than those of similar-sized birds of other species. As a consequence, circadian amplitudes of Tb and VO2 fluctuation between the rest and activity phases of non-huddling birds were also larger than expected. Circadian rhythms of metabolism save huddling and non-huddling woodhoopoes 19-34% of their potential daily energy expenditure. Birds huddling in groups conserved 12-29% of the daily energy expenditure of non-huddling birds at ambient temperatures of 20°C and below. However, at 30°C huddling birds used c. 12% more energy than non-huddling birds. The various avenues of energy conservation employed by woodhoopoes are suggested to be beneficial in: a) augmenting the proximate benefits of cooperative breeding; and b) optimizing fitness in the drought-prone sub-Saharan savannahs which are heavily influenced by the El Niño Southern Oscillations.
The activity patterns of six species of captive elephant shrews {Elephantulus (four species), Macroscelides and Petrodromus) were monitored electronically for periods of 48 h. Individual animals showed some significant differences in activity from one day to the next but generally followed the same pattern of diel activity. Intraspecific differences were observed in eight Elephantulus edwardii and seven Elephantulus myurus but all had a similar overall pattern of activity apart from a possibly diseased E. edwardii and two E. myurus , which had previously been exposed to a high level of human disturbance, and which showed increased nocturnal activity. All species were active, to varying degrees, both day and night. Interspecific differences in activity exhibited a continuum, with different species showing differing periods of peak activity. Differences in the nocturnal/diurnal ratio may be related to the amount of cover in the habitat and the degree of aridity experienced by each species. Significant seasonal differences in activity were noted in two species where sample sizes were adequate to permit their detection.
Résumé
On a surveilléélectroniquement le schéma d'activité de six espéces de rats à trompe en captivité par tranche de 48 h. Individuellement, les animaux présentent quelques différences significatives d'un jour à l'autre mais suivent généralement le même schéma d'activité. Des différences intraspécifiques furent observées chez huit Elephantulus edwardii et sept E. myurus mais tous avaient un schéma d'activités globalement similaire, aF l'exception d'un E. edwardii , peut‐être malade, et de deux E. myurus qui avaient ete auparavant soumis à de grands dérangements, et qui montraient un accroissement de l'activité nocturne. Toutes les espèces étaient actives, à des degrés divers, jour et nuit. Les différences interspécifiques étaient permanentes, les espèces présentant des périodes d'activité maximales diffeareés. Les différences du rapport diurne/nocturne peuvent être mises en relation avec le degré de couvertre de l'habitat et le degré d'aridité aux quels est soumise chaque espèce. On a noté des différences d'activité saisonnières significatives chez deux espèces dont la taille de l'echantillon permettait de les détecter.
Obviously, the activity behaviour in microtine rodents is extraordinarily flexible as far as small mammals are concerned.
This flexibility, which is not due an arrhythmic habit but to various distinct and interacting rhythms instead, must be seen
in relation to the specific living conditions of microtines, of which the high and ever present predation risk is probably
the most demanding. Other peculiarities are wide distribution ranges with consequent high diversity of ecological situations,
and the dramatically changing social environment in the course of the population cycles in the north. All this might require
high adaptability in general, which includes temporal strategies to maximise survival and fitness under various constraints.
The environment of any animal species is a complex set of both abiotic and biotic qualities. Dominant abiotic parameters are
light conditions, ambient temperature, relative humidity, precipitation, and wind speed. Biotic components may be classified
by the trophic levels at which they occur. On the same trophic level we find conspecifics as mates, as members of a social
group, and as competitors. On the same trophic level there are also competitors from other species. Biotic components from
different trophic levels are represented by prey, predators, and parasites. The combination of all these factors determines
how the world looks for an individual at a specific moment in time.
1.
Seasonal effects on daily activity patterns in the common vole were established by periodic trapping in the field and continuous year round recording of running wheel and freeding activity in cages exposed to natural meteorological conditions.
2.
Trapping revealed decreased nocturnality in winter as compared to summer. This was paralelled by a winter reduction in both nocturnal wheel running and feeding time in cages.
3.
Frequent trap checks revealed a 2 h rhythm in daytime catches in winter, not in summer. Cage feeding activity in daytime was always organized in c. 2 h intervals, but day-to-day variations in phase blurred the rhythm in summer in a summation of individual daily records. Thus both seasonal and short-term temporal patterns are consistent between field trappings and cage feeding records.
4.
Variables associated with the seasonal change in daily pattern were: reproductive state (sexually active voles more nocturnal), age (juveniles more nocturnal), temperature (cold days: less nocturnal), food (indicated by feeding experiments), habitat structure (more nocturnal in habitat with underground tunnels).
5.
Minor discrepancies between field trappings and cage feeding activity can be explained by assuming increased trappability of voles in winter. Cage wheel running is not predictive of field trapping patterns and is thought to reflect behavioral motivations not associated with feeding but with other activities (e.g., exploratory, escape, interactive behaviour) undetected by current methods, including radiotelemetry and passage-counting.
6.
Winter decrease in nocturnality appears to involve a reduction in nocturnal non-feeding and feeding behaviour and is interpreted primarily as an adaptation to reduce energy expenditure in adverse but socially stable winter conditions.
1.
In thefirst part of the paper, the model of non-parametric entrainment of circadian pacemakers is tested for the case of nocturnal rodents. The model makes use of the available data on freerunning period ([`(t)]\bar \tau
is close to 24 h. Thus the verycircadian nature of these pacemakers helps to conserve[`(t)]\bar \tau
=24 h. The effect of-instability is further reduced by entrainment with 2 pulses (dawn and dusk), made possible by the PRC's having both an advance and a delay section.
8.
To analyze the contributions to-conservation with seasonally changing photoperiod, we have assumed that it is of functional significance to conserve the phase of activity with respect to dusk (nocturnal animals) or to dawn (diurnal animals). We distinguish three contributions of nocturnal pacemaker behaviour to this type of-conservation: increased amplitude of the PRC (i), asymmetry in the PRC, such that the slope of the delay-part is steeper than the slope of the advance-part (ii), and a short freerunning period in DD (iii).
9.
A further contribution must derive from parametric effects of light, which are not traceable by the model, but certainly effective in preventing in complete photoperiods the-jump which is seen in skeleton photoperiods. The existence of parametric effects is further demonstrated by the change of with light intensity in LL, described by Aschoff's Rule, which presumably reflects differences in PRC-shape between nocturnal and diurnal animals (Daan and Pittendrigh, 1976b).
10.
The paper concludes with an attempt to distinguish the features of circadian clocks that are analytically necessary for entrainment to occur (i), or have functional meaning, either in the measurement of the lapse of time (ii) or in the identification of local time (iii).
Patterns of above-ground activity were recorded in two free-ranging populations of Microtus agrestis (L.) and one population of M. arvalis (Pall.) over several years by means of passage counters. Long-term variations of the circadian patterns were observed, but did not repeat themselves in a 12-month cycle. Variations in all three populations could be described by a sinusoidal function of an 18-month period. Maxima and minima of the sine-function were connected to distinct photoperiods (equinoxes and solstices). In a cyclic North Swedish population, the sine-function was superimposed by a second function which shows saturation behaviour. The relevance of these findings is discussed with respect to vole population cycles.
Daily activity patterns of shrews are controlled by metabolic requirements commensurate with their diminutive body mass and
resultant high surfaceto-mass ratios: they must forage often to avoid exhaustion of their energy stores. To remain homeothermic,
shrews must partition a 24-h period into multiple bouts of foraging, rest, and sleep.
Patterns and energetic consequences of spontaneous daily torpor were measured in the gray mouse lemur (Microcebus murinus) under natural conditions of ambient temperature and photoperiod in a dry deciduous forest in western Madagascar. Over a period of two consecutive dry seasons, oxygen consumption (VO2) and body temperature (T
b) were measured on ten individuals kept in outdoor enclosures. In all animals, spontaneous daily torpor occurred on a daily basis with torpor bouts lasting from 3.6 to 17.6 h, with a mean torpor bout duration of 9.3 h. On average, body temperatures in torpor were 17.3±4.9°C with a recorded minimum value of 7.8°C. Torpor was not restricted to the mouse lemurs’ diurnal resting phase: entries occurred throughout the night and arousals mainly around midday, coinciding with the daily ambient temperature maximum. Arousal from torpor was a two-phase process with a first passive, exogenous heating where the T
b of animals increased from the torpor T
b minimum to a mean value of 27.1°C before the second, endogenous heat production commenced to further raise T
b to normothermic values. Metabolic rate during torpor (28.6±13.2 ml O2 h–1) was significantly reduced by about 76% compared to resting metabolic rate (132.6±50.5 ml O2 h–1). On average, for all M. murinus individuals measured, hypometabolism during daily torpor reduced daily energy expenditure by about 38%. In conclusion, all these energy-conserving mechanisms of the nocturnal mouse lemurs, with passive exogenous heating during arousal from torpor, low minimum torpor T
bs, and extended torpor bouts into the activity phase, comprise an important and highly adapted mechanism to minimize energetic costs in response to unfavorable environmental conditions and may play a crucial role for individual fitness.
Female deer mice, Peromyscus maniculatus, and house mice, Mus domesticus=musculus, were challenged to reproduce while working for their food. Animals were subjected to one of several increasingly greater work requirements by using a caging system in which a food-pellet dispenser was controlled by wheel-running activity. Locomotor behaviour, food consumption and body weights were assessed continuously during pre-reproduction, pregnancy and lactation. Peromyscus and Mus differed in the magnitude and temporal dimensions of their locomotor effort; however, both species often ran far more wheel revolutions than necessary to generate the number of food pellets eaten, except during lactation when females invested all of their wheel-running into obtaining food. Peromyscus maintained greater body weights, supported greater litter masses, and produced more pups at weaning than their Mus counterparts, but Peromyscus also required less food per unit of mass than Mus. Most Peromyscus females maintained at the highest work levels did not attempt reproduction. Among Peromyscus that did become pregnant, litter size at birth and at weaning averaged five or six pups, regardless of feeding conditions. Peromyscus pups became increasingly stunted as females worked harder but obtained less food. Mus females allowed insemination and attempted lactation regardless of feeding conditions, but they routinely cannibalized offspring throughout the first 12 days of lactation. Thus, as litter size was reduced, most surviving Mus pups attained similar body weights at weaning. There was no evidence of sex-ratio adjustments in either species. In conclusion, Peromyscus females exhibited a rigid ‘all-or-nothing’ reproductive response, typically increasing their feeding effort to support large litters, whereas Mus females eliminated pups to stabilize the energy burdens of lactation. The divergent energy-allocation strategies employed by female Peromyscus and Mus appear correlated with their respective tendencies for seasonally oriented versus opportunistic breeding in the wild.
1.1. Oxygen consumption (VO2), thermal conductance (C), body temperature (Tb) and evaporative water loss (EWL) of Macroscelides proboscideus were measured at air temperatures from 5 to 38°C.2.2. The lowest VO2 was approximately that predicted for a eutherian of equal body weight. Minimal C was higher than predicted. EWL was high for an arid adapted small mammal. Tbs were stable between 10 to 25°C but increased above 30°C.3.3. Captive elephant shrew activity was predominantly nocturnal, although animals were active both day and night.4.4. Temperature regulation does not show the usual trends found in arid adapted small mammals.
1.1. The thermal characteristics of Petrodromus tetradactylus, Elephantulus intufi and E. brachyrhynchus were investigated and compared with other elephant-shrews that occur in the southern African subregion.2.2. E. intufi and E. brachyrhynchus appear to have lower than expected basal metabolic rates (1.1185 ± 0.1623 and 0.9649 ± 0.1638 ml O2 g−1 h−1, respectively) and high, narrow thermoneutral zones, similar to other elephant-shrews investigated previously. In contrast P. tetradactylus has a basal metabolic rate (0.871 ± 0.027 ml O2 g−1 h−1) close to expected for body mass, and a broad, low thermoneutral zone.3.3. The thermal biology of macroscelids is discussed in terms of their distribution, microhabitat and body size.
It is widely believed that torpor is mainly an adaptation of endotherms for cold stress and food limitation. We studied torpor use in the wild by a small tree-roosting microbat from a sub-tropical area during summer when food was abundant. Surprisingly, two torpor bouts per day were employed on each roost-day observed. The first bout occurred in the early morning and the second bout in the late afternoon, whilst a period of normothermia was maintained over the warmest part of the day. Torpor likely reduced energy expenditure substantially, and may be common in small microbats whose day-roosts are poorly insulated, even in sub-tropical climates.
Daily circadian rhythms of body temperature (Tb) and oxygen consumption (VO2) were measured in two murid species, which occupy extremely different habitats in Israel. The golden spiny mouse (Acomys russatus) is a diurnal murid distributed in arid and hot parts of the great Syrio-African Rift Valley, while the broad-toothed field mouse (Apodemus mystacinus) is a nocturnal species that inhabits the Mediterranean woodlands. In both species, the daily rhythms of Tb and VO2 are entrained by the photoperiod. Under laboratory experimental conditions (ambient temperature Ta = 33 degrees C and photoperiod regime of 12L:12D), Acomys russatus exhibits a tendency towards a nocturnal activity pattern, compared to the diurnal activity displayed by this species under natural conditions. Under the same photoperiod regime and at Ta = 28 degrees C, Apodemus mystacinus displays nocturnal activity, as observed under natural conditions. The maximal values of Tb were recorded in Acomys russatus at midnight (23:50 h), while the maximal values of VO2 were recorded at the beginning of the dark period (18:20 h). In Apodemus mystacinus, the maximal values of Tb and VO2 were recorded at 23:40 and 20:00 h, respectively. The ecophysiological significance of these results is discussed further.
This paper reviews the literature on the circadian rhythm of body temperature (CRT). The review starts with a brief discussion of methodological procedures followed by the description of known patterns of oscillation in body temperature, including ultradian and infradian rhythms. Special sections are devoted to issues of species differences, development and aging, and the relationships between the CRT and the circadian rhythm of locomotor activity, between the CRT and the thermoregulatory system, and between the CRT and states of disease. A section on the nervous control of the CRT is followed by summary and conclusions.
From earlier studies in the field of 24-hr rhythms, it has been concluded that the rhythm is an exogenous one, governed by social influences on behavior and, perhaps, by cosmic stimuli. Recently, new steps have been made in two directions: 1) the phase-relationships between many rhythmic functions have been described in detail; 2) it has been demonstrated that the rhythm is based on an endogenous, self-sustained oscillation. In conditions of isolation, subjects show a 'circadian' rhythm whose frequency deviates from that of the earth's rotation. In case of such free-running rhythms, it may happen that different functions show different frequencies (internal desynchronization), suggesting that there exists a multiplicity of oscillators in the organism. The implications of these findings for problems in applied physiology are exemplified by the results of experiments in which organisms were exposed to shifts of the entraining light-dark cycle (simulating flights in eastward or westward direction). Re-entrainment lasts longer (and hence also the time of diminished efficiency) after a westward than after an eastward flight.
The core apparatus that regulates circadian rhythm has been extensively studied over the past five years. A looming question remains, however, regarding how this apparatus is adjusted to maintain coordination between physiology and the changing environment. The diversity of stimuli and input pathways that gain access to the circadian clock are summarized. Cellular metabolic states could serve to link physiologic perception of the environment to the circadian oscillatory apparatus. A simple model, integrating biochemical, cellular, and physiologic data, is presented to account for the connection of cellular metabolism and circadian rhythm.
Perognathus longimembris, under a variety of conditions, demonstrated essentially a 24-hr rhythm in oxygen consumption. The amplitude, correlation with light cycle, and duration of periods of high and low metabolism varied. In September, mice provided with food and held at 22-24° C had a rhythm closely synchronized with a 12-hr light cycle (high in dark); mice were hypometabolic 12.5% of the days. In May, mice were more often out of synchrony and were hypometabolic 32.5% of the days. Without food at 22° C, mice became torpid every day; the first period of torpor began in the dark, and the rhythm of oxygen consumption was thereafter reversed. At 10° C without food, mice failed to arouse to a normal metabolic rate every day; sometimes they were deeply hypometabolic for 48-56 hr. A circadian rhythm of reduced amplitude continued, however, and arousals to normal rate occurred approximately on multiples of 24 hr. Arousals continued to occur in mice without food at 10° C despite exposure to or state of animals under the following conditions: constant darkness with or without sound, air with 4.5% CO2, obesity, 9 months' prior conditioning to 10° C, 1,400 R acute whole-body gamma radiation. Mice acclimatized to 10° C had the shortest periods of normal metabolism and obese mice the longest. In P. longimembris (mean wt 10.7 g), P. inornatus (14.6 g) and P. formosus (20.5 g) at 10° C without food, frequency and extent of hypometabolism varied inversely with body weight.
Under laboratory conditions, rock elephant shrews, Elephantulus myurus, use daily torpor under both short and long photoperiod acclimation. However, use of heterothermy often differs under field and laboratory conditions. We investigated the use of torpor in free-ranging elephant shrews from May 2001 to May 2002. The elephant shrews were capable of daily torpor throughout the year, with torpor most prevalent during winter. We recorded two torpor bouts during early summer (November). We recorded a total of 467 torpor bouts during the year. The mean torpor minimum body temperature (Tbmin) for the whole year was 15.3 degrees +/-4.4 degrees C, and the mean bout length was 8.6+/-3.5 h. These values were in the range expected for daily heterotherms. However, there was some marginal overlap with hibernation characteristics; a few torpor bouts were longer than 24 h in duration, and Tbmin decreased below 10 degrees C. Torpor was highly correlated with low ambient temperature and photoperiod. Torpor was also correlated with invertebrate abundance after controlling for photoperiod effects. During the year in which this study was conducted, the rainfall was 14% below long-term average. Historical rainfall records show that summer rainfall during strong El Nino years is up to 40% below the long-term average. During these drought years, the frequency of summer torpor may be higher, highlighting the need for long-term physiological data in free-ranging animals.
Oxygen consumption and torpor in mouse lemurs (Microcebus murinus and M. myoxinus): preliminary results of a study in western Madagascar
- J Schmid
Schmid, J. (1996). Oxygen consumption and torpor in mouse lemurs (Microcebus murinus and M. myoxinus): preliminary results of a study in western Madagascar. In Adaptations to the cold: 10th International Hibernation Symposium: 47–54.
Body temperature and torpor in a Malagasy small primate, the mouse lemur
- S Ortmann
- J Schmid
- J U Ganzhorn
- G Heldmaier
Ortmann, S., Schmid, J., Ganzhorn, J. U. & Heldmaier, G. (1996). Body temperature and torpor in a Malagasy small primate, the mouse lemur. In Adaptations to the cold: Tenth International Hibernation Symposium: 55–61.
Shrews – small insectivores
- J F Merritt
- S H Vessey
Merritt, J. F. & Vessey, S. H. (2000). Shrews – small insectivores