Fasting-induced daily torpor in desert hamsters ( Phodopus roborovskii )

Chi, Qing-Sheng; Wan, Xiaofeng; Geiser, Fritz; Wang, Dehua

doi:10.1016/j.cbpa.2016.05.019

Cited by 17 publications

(16 citation statements)

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“…Hibernating mammals exhibit an annual temperature rhythm [ 78 , 79 ] and alter the diversity and composition of gut microbiota over the circannual hibernation cycle [ 20 , 80 ]. Most mammals such as mice, desert hamsters ( Phodopus roborovskii ), and even humans show daily body temperature rhythm [ 81 , 82 ] and the diurnal variation of gut microbiota has been reported in mice [ 83 , 84 ]. A recent study showed that a 2–3 °C increase in ambient temperature can cause a 34% loss in gut bacterial diversity in a vertebrate ectotherm, the common lizard ( Zootoca vivipara ) [ 85 ].…”

Section: Discussionmentioning

confidence: 99%

Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure

et al. 2018

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BackgroundHuddling is highly evolved as a cooperative behavioral strategy for social mammals to maximize their fitness in harsh environments. Huddling behavior can change psychological and physiological responses. The coevolution of mammals with their microbial communities confers fitness benefits to both partners. The gut microbiome is a key regulator of host immune and metabolic functions. We hypothesized that huddling behavior altered energetics and thermoregulation by shaping caecal microbiota in small herbivores. Brandt’s voles (Lasiopodomys brandtii) were maintained in a group (huddling) or as individuals (separated) and were exposed to warm (23 ± 1 °C) and cold (4 ± 1 °C) air temperatures (Ta).ResultsVoles exposed to cold Ta had higher energy intake, resting metabolic rate (RMR) and nonshivering thermogenesis (NST) than voles exposed to warm Ta. Huddling voles had lower RMR and NST than separated voles in cold. In addition, huddling voles had a higher surface body temperature (Tsurface), but lower core body temperature (Tcore) than separated voles, suggesting a lower set-point of Tcore in huddling voles. Both cold and huddling induced a marked variation in caecal bacterial composition, which was associated with the lower Tcore. Huddling voles had a higher α and β-diversity, abundance of Lachnospiraceae and Veillonellaceae, but lower abundance of Cyanobacteria, Tenericutes, TM7, Comamonadaceae, and Sinobacteraceae than separated voles. Huddling or cold resulted in higher concentrations of short-chain fatty acids (SCFAs), particularly acetic acid and butyric acid when compared to their counterparts. Transplantation of caecal microbiota from cold-separated voles but not from cold-huddling voles induced significant increases in energy intake and RMR compared to that from warm-separated voles.ConclusionsThese findings demonstrate that the remodeling of gut microbiota, which is associated with a reduction in host Tcore, mediates cold- and huddling-induced energy intake and thermoregulation and therefore orchestrates host metabolic and thermal homeostasis. It highlights the coevolutionary mechanism of host huddling and gut microbiota in thermoregulation and energy saving for winter survival in endotherms.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0473-9) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure

et al. 2018

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“…The existence of more than two strategies or even a continuum from homeothermy through to poikilothermy has been suggested van Breukelen and Martin, 2015). Some endothermic species are only able to increase variation of T b minimally (Chaplin et al, 1984;Yoda et al, 2000;Nieminen et al, 2013), whereas the classical heterotherms include some that can enter shallower or deeper torpor during comparable fooddeprivation experiments (Walton and Andrews, 1981;Lovegrove et al, 2001;Nespolo et al, 2010;Chi et al, 2016;Boratynśki et al, 2018). Adaptive heterothermy is thus variable, but is probably a universal phenomenon among endotherms, including those considered classical homeotherms, or animals in general (Angilletta et al, 2006(Angilletta et al, , 2010.…”

Section: Introductionmentioning

confidence: 99%

An intra-population heterothermy continuum: notable repeatability of body temperature variation in food-deprived yellow-necked mice

Boratyński

Iwińska

Bogdanowicz

2019

Journal of Experimental Biology

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Theoretical modelling predicts that the thermoregulatory strategies of endothermic animals range from those represented by thermal generalists to those characteristic for thermal specialists. While the generalists tolerate wide variations in body temperature (T b ), the specialists maintain T b at a more constant level. The model has gained support from inter-specific comparisons relating to species and population levels. However, little is known about consistent among-individual variation within populations that could be shaped by natural selection. We studied the consistency of individual heterothermic responses to environmental challenges in a single population of yellow-necked mice (Apodemus flavicollis), by verifying the hypothesis that T b variation is a repeatable trait. To induce the heterothermic response, the same individuals were repeatedly food deprived for 24 h. We measured T b with implanted miniaturised data loggers. Before each fasting experiment, we measured basal metabolic rate (BMR). Thus, we also tested whether individual variation of heterothermy correlates with individual self-maintenance costs, and the potential benefits arising from heterothermic responses that should correlate with body size/mass. We found that some individuals clearly entered torpor while others kept T b stable, and that there were also individuals that showed intermediate thermoregulatory patterns. Heterothermy was found to correlate negatively with body mass and slightly positively with the BMR achieved 1-2 days before fasting. Nonetheless, heterothermy was shown to be highly repeatable, irrespective of whether we controlled for self-maintenance costs and body size. Our results indicate that specialist and generalist thermoregulatory phenotypes can co-exist in a single population, creating a heterothermy continuum.

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“…Similarly, when held under short photoperiod P. sungorus expressed spontaneous torpor, but not under long photoperiod (Geiser et al, 2013). However, torpor could be induced in a summer-acclimated congener, the desert hamster, P. roborovskii (Chi et al, 2016). Although it has been suggested that induced torpor and spontaneous torpor in P. sungorus differ functionally (Diedrich et al, 2012), some Phodopus species obviously have the ability to enter and arouse from torpor even when summer acclimated.…”

Section: Mammals Rodentsmentioning

confidence: 99%

“…Andean Hillstar, Oreotrochilus estella, spring and autumn unknown (Carpenter, 1974) Rufous hummingbird, Selasphorus rufus, migratory, winter unknown (Hiebert, 1993) Sunbird, Nectarina famosa, summer (Downs and Brown, 2002) Black-capped chickadee, Poecile atricapilla, spring and autumn unknown (Sharbaugh, 2001) Fat-tailed dunnart, Sminthopsis crassicaudata (Geiser and Baudinette, 1987;Warnecke et al, 2008) Stripe-faced dunnart, Sminthopsis macroura (Geiser and Baudinette, 1987;Körtner and Geiser, 2009) Kowari, Dasyuroides byrnei (Geiser and Baudinette, 1987) Blossom-bat, Syconycteris australis (Geiser et al, 1996;Coburn and Geiser, 1998) Elephant shrew, Elephantulus myurus (Mzilikazi and Lovegrove, 2004) White-footed mouse, Peromyscus leucopus (Lynch et al, 1978) Deer mouse, Peromyscus maniculatus (Tannenbaum and Pivorun, 1989) Desert hamster, Phodopus roborovskii (Chi et al, 2016;Geiser et al, 2019) Spiny mouse, Acomys russatus (Levy et al, 2011) Autumn to spring Tawny frogmouth, Podargus strigoides (Körtner et al, 2001) Owlet-nightjar, Aegotheles cristatus (Brigham et al, 2000) Whip-poorwill, Caprimulgus vociferous, migratory, winter unknown (Lane et al, 2004) Noisy miner, Manorina melanocephala (Geiser, 2019) Brown antechinus, Antechinus stuartii (Geiser, 1988;Hume et al, 2020) Yellow-footed antechinus, Antechinus flavipes (Geiser, 1988;Parker et al, 2019) Sugar glider, Petaurus breviceps (Körtner and Geiser, 2000a;Nowack et al, 2015) Djungarian hamster, Phodopus sungorus (Heldmaier and Steinlechner, 1981) other aspect of seasonal torpor use, the control of its expression differs among species and revealing the responsible cues will require further work.…”

Section: All Yearmentioning

confidence: 99%

Seasonal Expression of Avian and Mammalian Daily Torpor and Hibernation: Not a Simple Summer-Winter Affair†

Geiser

2020

Front. Physiol.

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Daily torpor and hibernation (multiday torpor) are the most efficient means for energy conservation in endothermic birds and mammals and are used by many small species to deal with a number of challenges. These include seasonal adverse environmental conditions and low food/water availability, periods of high energetic demands, but also reduced foraging options because of high predation pressure. Because such challenges differ among regions, habitats and food consumed by animals, the seasonal expression of torpor also varies, but the seasonality of torpor is often not as clear-cut as is commonly assumed and differs between hibernators and daily heterotherms expressing daily torpor exclusively. Hibernation is found in mammals from all three subclasses from the arctic to the tropics, but is known for only one bird. Several hibernators can hibernate for an entire year or express torpor throughout the year (8% of species) and more hibernate from late summer to spring (14%). The most typical hibernation season is the cold season from fall to spring (48%), whereas hibernation is rarely restricted to winter (6%). In hibernators, torpor expression changes significantly with season, with strong seasonality mainly found in the sciurid and cricetid rodents, but seasonality is less pronounced in the marsupials, bats and dormice. Daily torpor is diverse in both mammals and birds, typically is not as seasonal as hibernation and torpor expression does not change significantly with season. Torpor in spring/summer has several selective advantages including: energy and water conservation, facilitation of reproduction or growth during development with limited resources, or minimisation of foraging and thus exposure to predators. When torpor is expressed in spring/summer it is usually not as deep and long as in winter, because of higher ambient temperatures, but also due to seasonal functional plasticity. Unlike many other species, subtropical nectarivorous blossom-bats and desert spiny mice use more frequent and pronounced torpor in summer than in winter, which is related to seasonal availability of nectar or water. Thus, seasonal use of torpor is complex and differs among species and habitats.

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Fasting-induced daily torpor in desert hamsters ( Phodopus roborovskii )

Cited by 17 publications

References 34 publications

Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure

Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure

An intra-population heterothermy continuum: notable repeatability of body temperature variation in food-deprived yellow-necked mice

Seasonal Expression of Avian and Mammalian Daily Torpor and Hibernation: Not a Simple Summer-Winter Affair†

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