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Seasonal variation in energy expenditure in a rodent inhabiting a winter-rainfall desert

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Rebecca Rimbach at University of Münster
Rebecca Rimbach
Stéphane Blanc
Stéphane Blanc
Stéphane Blanc
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Alexandre Zahariev at French National Centre for Scientific Research
Alexandre Zahariev
Maria Gatta at University of the Witwatersrand
Maria Gatta
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Abstract and Figures

Animals that spend more energy than they obtain risk entering allostatic overload, reducing survival and fitness. They are predicted to adjust their daily energy expenditure (DEE) during periods of food scarcity. Adjustments of DEE to changes in food availability have been well-studied in species in temperate zones during winter, but less so in species enduring seasonal droughts. Likely mechanisms regulating DEE involve adjustments of activity and maintenance metabolism. Species that experience seasonal droughts and changes in food availability, like the African striped mouse (Rhabdomys pumilio), are appropriate model organisms to study the regulation of seasonal changes of DEE. We quantified DEE using the ‘doubly labelled water’ method, measured resting metabolic rate (RMR), and concomitantly determined activity levels using all-day focal observations of 69 free-living striped mice in the cold moist season with high food availability and the hot dry season with low food availability. Striped mice decreased their DEE in the food scarce dry season using multiple mechanisms, especially reductions in RMR, and reduced overall physical activity. This was further facilitated passively by reduced thermoregulatory costs. Our study demonstrates that animals reduce DEE via active and passive mechanisms in food-restricted environments, and highlights that several environmental factors should be considered simultaneously when aiming to understand how animals cope with harsh environments.
Changes in physiological, behavioural and environmental factors. Panels show a food availability (N = 69), bTDEE (N = 69), c residual DEE (N = 69), d residual RMR (N = 69), e % of time spent active (N = 35), f distance travelled (N = 35), g physical activity level (N = 69) and h body mass (N = 69) of striped mice in the dry season and moist season (black lines indicate the median, notches show the 95% confidence intervals, whiskers show minimum and maximum values of non-outlier data and open circles show outliers). Significant differences are illustrated (*P < 0.05; **P < 0.01, ***P < 0.001)
Changes in physiological, behavioural and environmental factors. Panels show a food availability (N = 69), bTDEE (N = 69), c residual DEE (N = 69), d residual RMR (N = 69), e % of time spent active (N = 35), f distance travelled (N = 35), g physical activity level (N = 69) and h body mass (N = 69) of striped mice in the dry season and moist season (black lines indicate the median, notches show the 95% confidence intervals, whiskers show minimum and maximum values of non-outlier data and open circles show outliers). Significant differences are illustrated (*P < 0.05; **P < 0.01, ***P < 0.001)
… 
Relationship between residual DEE and PAL at a cold temperatures (below the average of 21.4 °C) and b warm temperatures (above the average of 21.4 °C) in striped mice. At cold temperatures PAL and DEE positively correlated (Pearson’s product-moment correlation t = 9.25, df = 23, N = 25, P < 0.0001, r = 0.88), whereas there was no relationship at warm temperatures (t = − 0.33, df = 42, N = 44, P = 0.73, r = − 0.05)
Relationship between residual DEE and PAL at a cold temperatures (below the average of 21.4 °C) and b warm temperatures (above the average of 21.4 °C) in striped mice. At cold temperatures PAL and DEE positively correlated (Pearson’s product-moment correlation t = 9.25, df = 23, N = 25, P < 0.0001, r = 0.88), whereas there was no relationship at warm temperatures (t = − 0.33, df = 42, N = 44, P = 0.73, r = − 0.05)
… 
a Relationship between residual RMR and residual DEE (Pearson’s product-moment correlation dry season: t37 = 0.95, P = 0.34, r = 0.15; moist season: t28 = − 1.15, P = 0.25, r = − 0.21) and b relationship between RMR and PAL (Pearson’s product-moment correlation: t67 = − 3.05, P = 0.003, r = − 0.35). Filled circles represent the dry season (N = 39) and open triangles the moist season (N = 30)
a Relationship between residual RMR and residual DEE (Pearson’s product-moment correlation dry season: t37 = 0.95, P = 0.34, r = 0.15; moist season: t28 = − 1.15, P = 0.25, r = − 0.21) and b relationship between RMR and PAL (Pearson’s product-moment correlation: t67 = − 3.05, P = 0.003, r = − 0.35). Filled circles represent the dry season (N = 39) and open triangles the moist season (N = 30)
… 
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Vol.:(0123456789)
1 3
Journal of Comparative Physiology B (2018) 188:877–888
https://doi.org/10.1007/s00360-018-1168-z
ORIGINAL PAPER
Seasonal variation inenergy expenditure inarodent inhabiting
awinter-rainfall desert
RebeccaRimbach1 · StéphaneBlanc2· AlexandreZahariev2· MariaGatta1,3· NevillePillay1· CarstenSchradin1,2
Received: 12 January 2018 / Revised: 23 May 2018 / Accepted: 29 May 2018 / Published online: 8 June 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Animals that spend more energy than they obtain risk entering allostatic overload, reducing survival and fitness. They are
predicted to adjust their daily energy expenditure (DEE) during periods of food scarcity. Adjustments of DEE to changes
in food availability have been well-studied in species in temperate zones during winter, but less so in species enduring sea-
sonal droughts. Likely mechanisms regulating DEE involve adjustments of activity and maintenance metabolism. Species
that experience seasonal droughts and changes in food availability, like the African striped mouse (Rhabdomys pumilio),
are appropriate model organisms to study the regulation of seasonal changes of DEE. We quantified DEE using the ‘doubly
labelled water’ method, measured resting metabolic rate (RMR), and concomitantly determined activity levels using all-day
focal observations of 69 free-living striped mice in the cold moist season with high food availability and the hot dry season
with low food availability. Striped mice decreased their DEE in the food scarce dry season using multiple mechanisms,
especially reductions in RMR, and reduced overall physical activity. This was further facilitated passively by reduced ther-
moregulatory costs. Our study demonstrates that animals reduce DEE via active and passive mechanisms in food-restricted
environments, and highlights that several environmental factors should be considered simultaneously when aiming to under-
stand how animals cope with harsh environments.
Keywords Drought· Eco-physiology· Energetics· Field metabolic rate· Physical activity level· Phenotypic flexibility
Introduction
An individual’s fitness is affected by the balance between
acquisition and expenditure of energy, which is essential for
maintenance, growth, survival and reproduction (Krackow
1989; Boutin 1990). In nature, availability of food, the
primary source of energy for animals, varies both on a
spatial and a temporal scale. For many species, seasonal
changes in rainfall and temperature cause significant varia-
tion in food availability, often characterized by one season
with super-abundant food (often the breeding season), and
one season with low food availability, which has to be sur-
vived to reach the following breeding season. While climate
change might increase the likelihood of periods of food scar-
city, such as droughts and extreme weather events, so far we
do not know in how far animals are able to reduce their daily
energy expenditure (DEE) as an adaptive response to such
events. When energy expenditure exceeds energy acquisi-
tion, allostatic overload occurs, which leads to a decrease
in body condition, reduced fitness, pathologies and finally,
if it persists, death due to starvation occurs (McEwen and
Wingfield 2003; Romero etal. 2009). When energy acquisi-
tion is reduced and migration to other areas is not possible,
decreasing energy expenditure is the only adaptive solution
to avoid or reduce allostatic overload.
During food shortages, energy investment into repro-
duction is typically the first expenditure that is ceased
Communicated by H.V. Carey.
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s0036 0-018-1168-z) contains
supplementary material, which is available to authorized users.
* Rebecca Rimbach
rrimbach@gmail.com; Rebecca.Rimbach@wits.ac.za
1 School ofAnimal, Plant andEnvironmental Sciences,
University oftheWitwatersrand, Private Bag 3, Wits,
Johannesburg2050, SouthAfrica
2 IPHC, UNISTRA, CNRS, 23 rue du Loess,
67200Strasbourg, France
3 Institute ofEnvironmental Sciences, Leiden University, PO
Box9518, 2300RALeiden, TheNetherlands
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Both stressful and harsh environments challenge homeostasis and survival, impacting fitness. Stress and harshness are often considered synonymous [4][5][6][7][8][9], but we maintain that the factors leading to stress differ from factors leading to harshness and that the resulting adaptive physiological responses are mutually exclusive. ...
... Increasing harshness due to climate change, such as extended periods of heat and drought, has been identified as a major threat to biodiversity and ecosystem functioning [4,7]. However, there is no clear definition of harshness, which is often wrongly assumed to be the same as stress or long-term stress [4][5][6][7][8][9]. To predict long-term consequences of harshness, we must identify which mechanisms evolved to cope with it, what their limits are, and when they might fail [11]. ...
... One of the most common harsh conditions that animals experience is the seasonal reduction in food availability, due to cold, heat, and/or drought. To endure low food availability, animals save energy by terminating reproduction, reducing physical activity and metabolism, leading to a net decrease in daily energy expenditure [9]. For this, the harshness response leads to a decrease in the levels of metabolic hormones including those of the physiological stress response. ...
Harshness is not stress
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We must differentiate between stressful and harsh environments to understand animals’ resilience to global change. Harshness is not stress. Stressful environments activate the physiological stress response to increase energy avail- ability, while harsh environments inhibit the physiological stress response to save energy.
View
... Seasonal responses of species from less predictable environments unsurprisingly often deviate from the general trend mentioned above. Melano-bellied oriental voles (Eothenomys melanogaster) increase BMR and NST in winter relative to summer, but M b remains the same (Xu et al., 2011), whereas African striped mice (Rhabdomys pumilio) increase NST (Haim and Fourie, 1980a,b,c), resting metabolic rate and M b in winter relative to summer (Rimbach et al., 2018). Further, cold-acclimated rock elephant shrews (Elephantulus myurus) increased BMR relative to their warmacclimated counterparts even though M b was similar (Mzilikazi et al., 2007). ...
... The reason for such deviations is that seasonal responses also include physiological factors that are independent of, yet confounded by, T a , including reproductive status, locomotion, diet and food availability, all of which influence the animal's energy budget (McNab, 1986;Bozinovic, 1992;Hammond and Diamond, 1992;Cruz-Neto et al., 2001;Lovegrove, 2001;Mzilikazi et al., 2007;Withers et al., 2016). For instance, Rimbach et al. (2018) studied seasonal responses in African striped mice in a karoo habitat, where it is known that they typically become food stressed in summer and lose about 12% of their M b (Schradin and Pillay, 2004;Schradin, 2005). The summer-winter increase in metabolism thus accompanies an increase in M b as a result of an increase in resources during winter. ...
... The African striped mouse is an ideal study model to test for differences between subpopulations because the species is widely distributed throughout southern Africa, occupies starkly different habitats and much is already known about its behaviour, ecology and physiology (Haim and Fourie, 1980b;Korn, 1989;Haim et al., 1998;Schradin and Pillay, 2004;Schradin, 2005;Schradin and Pillay, 2005;Scantlebury et al., 2006;Schradin et al., 2007;Lovegrove, 2009;Scantlebury et al., 2010;Schradin et al., 2012;Rimbach et al., 2018Rimbach et al., , 2019Schradin et al., 2019;Zduniak et al., 2019). African striped mice residing in arid succulent karoo habitats favour group living (Schradin and Pillay, 2004), whereas mice residing in more mesic habitats favour a solitary existence (Schradin, 2005). ...
Obligatory homeothermy of mesic adapted African striped mice, Rhabdomys pumilio, is governed by seasonal basal metabolism and year-round "thermogenic readiness" of brown adipose tissue
Article
  • Jun 2022
  • J EXP BIOL
Small mammals undergo thermoregulatory adjustments in response to changing environmental conditions. Whereas small heterothermic mammals can employ torpor to save energy in the cold, homeothermic species must increase heat production to defend normothermia through the recruitment of brown adipose tissue (BAT). Here, we studied thermoregulatory adaptation in an obligate homeotherm, the African striped mouse (Rhabdomys pumilio), captured from a subpopulation living in a mesic, temperate climate with marked seasonal differences. Basal metabolic rate (BMR), non-shivering thermogenesis (NST) and summit metabolic rate (MSUM) increased from summer to winter, with NST and MSUM already reaching maximal rates in autumn, suggesting seasonal preparation to the cold. Typical of rodents, cold-induced metabolic rates positively correlate with BAT mass. Analysis of cytochrome c oxidase (COX) activity and UCP1 content, however, demonstrate that thermogenic capacity declines with BAT mass. This resulted in seasonal differences in NST being driven by changes in BMR. The increase in BMR is supported by a comprehensive anatomical analysis of metabolically active organs, revealing increased mass proportions in the cold season. The thermoregulatory response of R. pumilio is associated with the maintenance of body weight throughout the year (48.3±1.4 g), contrasting large summer-winter mass reductions often observed in Holarctic rodents. Collectively, bioenergetic adaptation of this Afrotropical rodent involves seasonal organ adjustments influencing BMR, combined with a constant thermogenic capacity dictated by trade-offs in thermogenic properties of BAT. Arguably, this high degree of plasticity was a response to unpredictable cold spells throughout the year. Consequently, the reliance on such a resource intensive thermoregulatory strategy may expose more energetic vulnerability in changing environments of food scarcity and extreme weather conditions due to climate change, with major ramifications for survival of the species.
View
... phenotypic flexibility, Maldonado et al., 2012). Recently, Rimbach et al. (2018) reported that during the food scarce dry season, the striped mice reduced their energy expenditure by decreasing RMR and overall physical activity. This was further facilitated passively by a reduction in thermoregulatory costs. ...
... This was further facilitated passively by a reduction in thermoregulatory costs. Furthermore, changes in body mass, water loss, and thermal conductance have been reported as responses to seasonal changes in food resources, relative humidity, and temperature in endotherms (Haim et al., 1991;Rimbach et al., 2018;Wan-long et al., 2013). ...
Seasonal acclimation of energy and water balance in desert‐dwelling rodents of South America
Article
Full-text available
Seasonal changes in environmental conditions may induce reversible physiological adjustments in organisms. We studied the acclimatization for multiple stressors in energy expenditure and water balance in Galea leucoblephara, a diurnal hystricognath rodent native to South America that experiences significant changes in temperature, precipitation, and food availability among seasons. We conducted a field study in the Monte Desert of Mendoza, Argentina, where we evaluated adult individuals' physiological status during two contrasting seasons in terms of climate and primary productivity. Reduced temperature, rainfall, and primary productivity during winter were associated with a decrease of 70% in basal metabolic rate (BMR), 30% in total evaporative water loss (TEWL), and 9% in body mass (Mb). In contrast, higher water availability, high temperature, and primary productivity during summer, induced significant increases in energy expenditure and evaporative water loss. As expected, the proportion of dietary items consumed by G. leucoblephara varied seasonally, resulting in a more diverse diet during summer. Our results illustrate how G. leucoblephara can cope with high seasonal contrasts in water availability, temperature, and food availability by modifying its physiological performance. Our data provide support for the hypothesis of physiological flexibility in energetic traits and water balance in response to the environmental challenges of the Monte Desert.
View
... The two species responded similarly to increased dryness while maintaining body condition, a proxy of fat reserves. Similarly, R.pumilio individuals tended to maintain their body condition stable while reducing their energy expenditure and physical activity during periods of limited food availability (Rimbach et al., 2018a;2018b). The semi-arid populations of R.bechuanae and R.d.dilectus could be displaying a similar behavioral strategy. ...
View
... TEE has been shown to correlate with daily movement distance in some free-ranging animals, such as llamas (Riek et al., 2019), cheetahs (Scantlebury et al., 2014) and polar bears (Pagano and Williams, 2019). However, many studies show that physical activity is unrelated to TEE in humans, non-human primates and rodents (Edwards et al., 2017;Perrigo, 1987 2015b, 2017; Pontzer et al., 2014;Rimbach et al., 2018), and these studies suggest that physical activity is a relatively poor predictor of TEE both within and between species (Pontzer, 2015b(Pontzer, , 2017. ...
Total energy expenditure of bottlenose dolphins ( Tursiops truncatus ) of different ages
Article
  • Jul 2021
Marine mammals are thought to have an energetically expensive lifestyle because endothermy is costly in marine environments. However, measurements of total energy expenditure (TEE; kcal/day) are available only for a limited number of marine mammals, because large body size and inaccessible habitats make TEE measurements expensive and difficult for many taxa. We measured TEE in 10 adult common bottlenose dolphins (Tursiops truncatus) living in natural seawater lagoons at two facilities (Dolphin Research Center and Dolphin Quest) using the doubly labeled water method. We assessed the relative effects of body mass, age, and physical activity on TEE. We also examined whether TEE of bottlenose dolphins, and more generally marine mammals, differs from that expected for their body mass compared to other eutherian mammals, using phylogenetic least squares (PGLS) regressions. There were no differences in body mass or TEE (unadjusted TEE and TEE adjusted for fat free mass (FFM)) between dolphins from both facilities. Our results show that Adjusted TEE decreased and fat mass (FM) increased with age. Different measures of activity were not related to age, body fat or Adjusted TEE. Both PGLS and the non-phylogenetic linear regression indicate that marine mammals have an elevated TEE compared to terrestrial mammals. However, bottlenose dolphins expended 17.1% less energy than other marine mammals of similar body mass. The two oldest dolphins (>40 years) showed a lower TEE, similar to the decline in TEE seen in older humans. To our knowledge, this is the first study to show an age-related metabolic decline in a large non-human mammal.
View
... When food resources decline and conditions become harsher, their health status deteriorates and nonsurvivors exhibit signs of permanent pathology (Schoepf et al. 2017). To reduce their daily energy expenditure, striped mice reduce their metabolism and activity during the dry season (Rimbach et al. 2017(Rimbach et al. , 2018a(Rimbach et al. , 2018b. Thus, since breeding season for striped mice is followed by a food restricted dry season, we expect them to have reduced growth rates but over a period of longer growth to reach a larger body size that enhances their competitive abilities in the following breeding season. ...
Prolonged growth during the food-restricted dry season in a small African mammal
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Studying how different environmental parameters, such as resource availability and ambient temperature, affect growth rates aids to understand the evolution of different growth strategies. Low levels of food availability restrict growth, and high ambient temperature can constrain growth via trade-offs between body temperature maintenance and heat produced during digestion. We studied growth of African striped mice (Rhabdomys pumilio), a small mammal living in a seasonally arid habitat. Striped mice are born during spring with high food availability and low ambient temperature, and typically enter the food-restricted dry season before reaching adulthood. We predicted low food availability and high ambient temperature would negatively affect growth. We therefore expected an extended period of slow growth during the long dry season. We repeatedly measured body length of 369 free-living individuals, examined how ambient temperature and food availability influenced growth rate, and seasonal changes in growth rate. In addition, we investigated whether mice (N = 27) born in summer (atypical breeding season) have slower growth rates than those born in spring. Growth rate increased with increasing food availability and decreased with increasing ambient temperature. Individuals born in summer grew slower than those born in spring. Sexes reached asymptotic body length at 258 days (females) and 285 days (males), which is an unusually long growth period compared with other small rodents. As most striped mice live for less than 1 year, this period encompasses the entire life for most individuals, but stops at old age, which could indicate senescence. Our results demonstrate a positive influence of food availability on growth, a relationship mediated by ambient temperature. We conclude that striped mice enter the food-restricted dry season before postnatal growth is terminated, and early exposure to harsh environmental conditions during the long dry season likely explains the prolonged growth period in striped mice.
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... Hyperactivity in response to restricted food availability, while extreme in ABA, mimics, in its initial stages, the adaptive response of rodents in the wild to periods of food scarcity [23]. Here, strategies to maintain homeostatic energy balance and survive have to consider both reducing activity levels to compensate for a reduced energy intake and increasing activity levels to effectively forage [23][24][25]. While increasing activity in . ...
Suppression of cortico-striatal circuit activity improves cognitive flexibility and prevents body weight loss in activity-based anorexia in rats
Preprint
Full-text available
  • Mar 2020
Background The ability to adapt behavior to changing environmental circumstances, or cognitive flexibility , is impaired in multiple psychiatric conditions, including anorexia nervosa (AN). Exaggerated prefrontal cortical activity likely underpins the inflexible thinking and rigid behaviors exhibited by patients with AN. A better understanding of the neural basis of cognitive flexibility is necessary to enable treatment approaches that may target impaired executive control. Methods Utilizing the activity-based anorexia (ABA) rat model and touchscreen operant learning paradigms, we investigated the neurobiological link between pathological weight loss and cognitive flexibility. We used pathway-specific chemogenetics to selectively modulate activity in neurons of the medial prefrontal cortex (mPFC) projecting to the nucleus accumbens shell (AcbSh) in female Sprague-Dawley rats. Results DREADD-based inhibition of the mPFC-AcbSh pathway prevented weight loss in ABA and improved flexibility during early reversal learning by reducing perseverative responding. Modulation of activity within the mPFC-AcbSh pathway had no effect on running, locomotor activity or feeding under ad libitum conditions, indicating the specific involvement of this circuit in conditions of dysregulated reward. Conclusions Both attenuation of weight loss in ABA and improved cognitive flexibility following suppression of mPFC-AcbSh activity aligns with the relationship between disrupted prefrontal function and cognitive rigidity in AN patients. The identification of a neurobiological correlate between cognitive flexibility and pathological weight loss provides a unique insight into the executive control of feeding behavior. It also highlights the utility of the ABA model for understanding the biological bases of cognitive deficits in AN and provides context for new treatment strategies.
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The seasonal variation of basal metabolic rate is related to the expression of torpor among small mammals
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A variety of responses to climate seasonality have evolved by small mammals, including adjustments of the basal rate of metabolism (BMR) and the use of daily or seasonal torpor (here referred to as short-bout and long-bout torpor). The seasonal variation of their BMR is known to depend mainly on the concurrent variation of body mass, but it should also be affected by structural and functional changes occurring within the body that could depend on the expression of torpor. Thus it was hypothesized that BMR seasonality is related to the expression of torpor at an interspecific level. Seasonal BMR and body mass data were gathered from the literature and phylogenetic comparative analyses were done to test this hypothesis among mammals of less than 1 kg. BMR seasonality (dBMR) was quantified as the log-transformed ratio of the mean whole-animal BMR reported for the period P2 (autumn-winter) over that for the period P1 (spring-summer). Predictors were the seasonal body mass adjustment (dm), mean body mass (m) and torpor expression (TO, a three-level factor: no torpor, short-bout torpor, long-bout torpor). The seasonal variation of BMR was significantly related to dm but also to. Accounting for dm, species expressing long-bout torpor, but not those entering short-bout torpor, collectively exhibited a lower dBMR than species not entering torpor. Fat storage and use by species entering long-bout torpor, alone, could not explain their lower dBMR, as the TO:dm interaction was not significant. The low dBMR of species entering long-bout torpor may result from their collective tendency to down-regulate more strongly costly visceral organs during P2. The dBMR of the different TO categories overlapped appreciably, which highlights our still limited knowledge of the BMR seasonality among small mammals.
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Seasonal changes in problem-solving in wild African striped mice
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Seasonal variation in telomere dynamics in African striped mice
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  • Dec 2020
  • OECOLOGIA
Telomere shortening has been used as an indicator of aging and is believed to accelerate under harsh environmental conditions. This can be attributed to the fact that telomere shortening has often been regarded as non-reversible and negatively impacting fitness. However, studies of laboratory mice indicate that they may be able to repair telomere loss to recover from environmental harshness, as indicated by recent studies in hibernating rodents. We studied seasonal variation in telomere dynamics in African striped mice (Rhabdomys pumilio) living in a highly seasonal environment. In our annual species, individuals born in the moist spring (high food availability) need to survive the harsh dry summer (low food availability) to be able to reproduce in the following spring. We studied the effect of the harsh dry vs. the benign moist season on telomere dynamics. We also tested if telomere length or the rate of change in telomere length over the dry season predicted the probablity of dissapearance from the population at the same time. Male, but not female, stripped mice showed age-related telomere erosion. Telomeres were longer at the beginning of the dry season compared to the rest of the year. Telomeres increased significantly in length during the moist season. Neither telomere length at the onset of the dry season nor telomere loss over the dry season predicted whether or not individuals disappeared. In conclusion, our data suggest that seasonal attrition and restoring of telomeres also occurs in non-hibernating wild rodents living in hot food restricted environments.
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Total energy expenditure in captive capuchins ( Sapajus apella )
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Full-text available
  • Jan 2017
  • AM J PRIMATOL
Primates have markedly lower total energy expenditure (TEE; kcal/day) than other placental mammals, expending approximately 50% less energy for their mass than non-primate eutherians. However, little is known regarding interspecific variation of energy expenditure within platyrrhine primates. We investigated TEE in captive tufted capuchins (Sapajus apella, n = 8, ages 7-36), a frugivorous platyrrhine, to compare TEE with other placental mammals and primates. We tested the hypothesis that large-brained capuchins would exhibit greater TEE than other platyrrhines that are less encephalized. We used the doubly labeled water (DLW) method to measure TEE over 7-11 days, during which physical activity data were recorded via focal observation. TEE was strongly correlated with fat free mass, but sex, age, and rates of walking and climbing were not correlated with variation in TEE in multivariate analyses controlling for fat free mass. We found evidence that daily physical activity was negatively correlated with body fat percentage. Capuchin TEE was similar (P = 0.67) to other, less encephalized platyrrhines (Callithrix and Alouatta) and 54% lower than other placental mammals, in analyses controlling for body mass. These results suggest that brain size and physical activity do not necessarily influence variation in daily energy expenditure across primate species.
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Food Availability Is the Main Driver of Seasonal Changes in Resting Metabolic Rate in African Striped Mice (Rhabdomys pumilio)
Article
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Resting metabolic rate (RMR) influences energy allocation to survival, growth, and reproduction, and significant seasonal changes in RMR have been reported. According to one hypothesis, seasonal changes in RMR are mainly attributable to seasonal changes in ambient temperature (Ta) and food availability. Studies on species from the temperate zone indicated that food availability is the main driver. However, whether this is generally true is unknown, because studies from the tropics and subtropics, where most species live, are rare. We studied the African striped mouse (Rhabdomys pumilio) inhabiting a seasonal environment with hot dry seasons with low food availability and cold moist seasons with high food availability. Using 603 RMR measurements of 277 individuals, we investigated the relative importance of food availability and Ta on RMR during selected periods, in which one extrinsic factor varied while the other factor was relatively constant. At similar Ta, residual RMR increased with increasing levels of food availability. In contrast, different Ta did not influence residual RMR at similar levels of food availability. Thus, our study on a subtropical species gives support to the hypothesis, derived from temperate zone species, that food availability mainly drives seasonal changes in RMR.
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Active and explorative individuals are often restless and excluded from studies measuring resting metabolic rate: Do alternative metabolic rate measures offer a solution?
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  • Feb 2017
  • PHYSIOL BEHAV
It has often been proposed that bolder, more explorative or more active individuals also have a higher resting metabolic rate (RMR), indicating metabolic costs of these personality types. However, such individuals might often be restless and thus excluded from RMR datasets, leading to a significant sampling bias. We tested (1) whether such a bias occurs when animals are measured for a relatively common but short time period of 3 hours, and if so, (2) whether alternative measures of metabolic rate, that allow the incorporation of non-resting individuals, would reveal associations between metabolism and personality. For this, we studied free-living individuals of the African striped mouse (Rhabdomys pumilio) both during the moist season (N=25 individuals) with high food availability and the dry season (N=48 individuals) with low food availability. We assessed variation in the latency to explore a novel object, and the time spent active and time spent in the centre of a neutral arena. We examined links between personality and (i) RMR and (ii) four alternative metabolic rate (MR) metrics: average MR, highest MR, lowest MR and span of MR. Twenty-nine percent of the measured individuals had to be excluded from our RMR study because they remained restless during respirometry trials. Striped mice showed a behavioural syndrome where fast explorers also spent more time in centre and more time active than slow explorers. Individuals that did not rest during respirometry trials were faster explorers and in the moist season, they were also more active and spent more time in the centre than individuals that rested. We found no relationship between RMR and the behavioural syndrome, which might be due to the exclusion of individuals with a certain behavioural type, leaving a subset of compliant individuals. In the moist season, we found positive relationships between the behavioural syndrome and span of MR and lowest MR. In the dry season, low food availability may mask links between the behavioural syndrome and alternative MR measures due to reduced overall activity in striped mice. Our study demonstrated the importance to consider personality when measuring RMR and suggests that some alternative MRs may be useful to examine relationships between metabolism and personality when it is impossible to measure individuals over extended time periods.
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Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases
Article
  • Dec 2016
  • J EXP BIOL
In response to variation in food availability and ambient temperature (Ta), many animals show seasonal adaptations in their physiology. Laboratory studies showed that thyroid hormones are involved in the regulation of metabolism, and their regulatory function is especially important when the energy balance of an individual is compromised. However, little is known about the relationship between thyroid hormones and metabolism in free-living animals and animals inhabiting seasonal environments. Here, we studied seasonal changes in triiodothyronine (T3) levels, resting metabolic rate (RMR) and two physiological markers of energy balance (blood glucose and ketone bodies) in 61 free-living African striped mice (Rhabdomys pumilio) that live in an semi-arid environment with food shortage during the dry season. We predicted a positive relationship between T3 levels and RMR. Further, we predicted higher T3 levels, blood glucose levels and RMR, but lower ketone body concentrations, during the moist season when food availability is high compared to summer with low food availability. RMR and T3 levels were negatively related in the moist season but not in the dry season. Both RMR and T3 levels were higher in the moist than in the dry season, and T3 levels increased with increasing food availability. In the dry season, blood glucose levels were lower but ketone body concentrations higher, indicating a change in substrate use. Seasonal adjustments in RMR and T3 levels permit a reduction of energy expenditure when food is scarce, and reflect an adaptive response to reduced food availability in the dry season.
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Young But Not Old Adult African Striped Mice Reduce Their Activity in the Dry Season When Food Availability is Low
Article
  • Aug 2016
An individual′s survival and fitness depend on its ability to effectively allocate its time between competing behaviors. Sex, social tactic, season and food availability are important factors influencing activity budgets. However, few field studies have tested their influences. The African striped mouse (Rhabdomys pumilio) lives in highly seasonal habitats in southern Africa, and individuals can adopt different social tactics. We investigated seasonal changes in activity budgets of different tactics and predicted that individuals will reduce their activity in the non-breeding season to save energy when food availability is low and that young non-breeding adults (‘philopatrics’) invest mainly in activities related to gaining body mass to increase survival probability. We predicted old adults (‘breeders’), which bred during the previous breeding season, to invest mainly in maintenance of their social status. We conducted 90 focal observations during the non-breeding season and 73 during the breeding season. Activity budgets of striped mice were season and tactic specific, with philopatrics, but not breeders, reducing activity when food availability was low, possibly to decrease energy expenditure. Philopatrics of both sexes foraged and basked more in the breeding season than during the non-breeding season. Male philopatrics gained body mass and female philopatrics maintained their body mass in both seasons. Sex-specific differences occurred during the breeding season, when female breeders foraged more than male breeders, while male breeders chased other individuals more than female breeders. These findings indicate that individuals adopting different social tactics display distinct behaviors to fulfill tactic-specific energetic needs.
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Resilience to Droughts in Mammals: A Conceptual Framework for Estimating Vulnerability of a Single Species
Article
  • Jun 2016
The frequency and severity of droughts in certain areas is increasing as a consequence of climatechange. The associated environmental challenges, including high temperatures, low food, and wateravailability, have affected, and will affect, many populations. Our aims are to review the behavioral,physiological, and morphological adaptations of mammals to arid environments, and to aid researchersand nature conservationists about which traits they should study to assess whether or not their studyspecies will be able to cope with droughts. We provide a suite of traits that should be considered whenmaking predictions about species resilience to drought. We define and differentiate between generaladaptations, specialized adaptations, and exaptations, and argue that specialized adaptations areof little interest in establishing how nondesert specialists will cope with droughts. Attention should beplaced on general adaptations of semidesert species and assess whether these exist as exaptations innondesert species. We conclude that phenotypic flexibility is the most important general adaptationthat may promote species resilience. Thus, to assess whether a species will be able to cope with increasingaridity, it is important to establish the degree of flexibility of traits identified in semidesert species thatconfer a fitness advantage under drying conditions.
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Using doubly-labelled water to measure free-living energy expenditure: Some old things to remember and some new things to consider
Article
  • Apr 2016
The doubly-labelled water (DLW) method provides the ability to measure the energy expenditure of free-living animals based only on the injection of two isotopes in water (one of oxygen and one of hydrogen) and traditionally the collection of 2 blood samples. We review here the fundamental basis of how the method works, and highlight how the choice of the appropriate calculation equation can have a large impact on the resultant estimates, particularly in species where the difference between the isotope elimination constants is small. This knowledge is not new, but is worth reiterating given the potential for error by making the wrong choice. In particular, it is important to remember that for mammals weighing less than 5kg, and birds weighing less than 2kg, the single pool models perform best in validation studies, while in mammals above 15kg the two-pool models perform best. Above 2kg in birds and between 5 and 15kg in mammals, however, the model superiority is uncertain. Even where the choice based on body mass would appear clear, the decision may need to be tempered by species specific information regarding potential additional sources for hydrogen turnover, such as de novo lipogenesis or methanogenesis. Recent advances in the technique have included attempts to make the method less invasive by using innovative methods for dosing and sample collection. In addition, the advent of laser spectroscopy, as a replacement technology for mass spectrometry, may open up many new opportunities in the field. These potentially include direct sampling of breath in the field and tracking background isotope drift using (17)oxygen levels.
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Endocrine Responses to Inclement Weather in Naturally Breeding Populations of White-Crowned Sparrows (Zonotrichia leucophrys pugetensis)
Article
  • Jan 1983
Plasma levels of luteinizing hormone (LH), testosterone, and corticosterone were measured in relation to periods of inclement versus fair weather during the reproductive season of the Puget Sound White-crowned Sparrow (Zonotrichia leucophrys pugetensis). In 1974, cool stormy weather in spring delayed the onset of breeding by one month and also prolonged the period of elevated circulating levels of LH and testosterone, compared with the fair spring of 1975. Inclement weather in 1974 did not appear to be stressful, as indicated by body weights and plasma levels of corticosterone. In late May 1980, however, a storm occurred after nesting activities had begun and all pairs sampled were feeding young. In this case, plasma levels of corticosterone were greatly elevated above those of birds sampled at the same time in the warm spring of 1979 and also above those of birds sampled in spring of both 1974 and 1975. In addition, fat depots were virtually exhausted in birds sampled during the storm of 1980, suggesting that these birds were stressed. Most pairs lost their brood in May 1980, presumably to starvation, and renested after amelioration of environmental conditions in June. These data suggest that although storms may modify the onset and temporal progression of the reproductive cycle, they are stressful to adults only when the nesting phase is in progress. Thus, the underlying mechanisms by which inclement weather delays the onset of breeding or disrupts the nesting once underway are likely to have different endocrine bases.
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