Photoperiod, temperature and melatonin effects on thermoregulatory behavior in Djungarian hamsters

doi:10.1016/0031-9384(88)90294-6

Physiology & Behavior

Volume 42, Issue 2, 1988, Pages 173-177

https://doi.org/10.1016/0031-9384(88)90294-6 Get rights and content

Abstract

Nesting and burrowing activity were measured in hamsters acclimated to either long or short day photoperiod in thermoneutrality and at 10°C. Hamsters build larger nests under short day photoperiod or at 10°C as compared to long day photoperiod or thermoneutrality. Both environmental cues contributed about 50% to a total increase in nest size from 1.8 g cotton/day to 7.7 g cotton/day (long day thermoneutral versus short day at 10°C). Burrowing activity was suppressed by both cold or short day exposure. Daily melatonin injections, effective in inducing physiological short day adjustment under a long day photoperiod, also increased nesting scores. Hamsters which did not respond to short day conditions or to melatonin treatment physiologically lacked behavioral adjustments as well. Collectively, these results demonstrate analogies in the environmental control of physiological thermoregulatory adjustment and nesting behavior. Burrowing activity seems to be more related to reproductive needs than to thermoregulatory requirements in this hamster.

References (31)

T.G. Hartung et al.
Nest building behavior in seven species of muroid rodents
Behav Neural Biol
(1979)
J.L. Wolfe
Experiments on nest-building behaviour in Peromyscus (Rodentia: Cricetinae)
Anim Behav
(1970)
P. Batchelder et al.
Effects of temperature and social interactions on huddling behavior in Mus musculus
Physiol Behav
(1982)
A. Buchberger et al.
Photoperiod and temperature effects on adrenal tyrosine hydroxylase and its relation to nonshivering thermogenesis
Pflugers Arch
(1983)
D.S. Carter et al.
Antigonadal effect of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): Duration is the critical parameter
Endocrinology
(1983)
J.M. Darrow et al.
Circadian regulation of pineal melatonin and reproduction in the Djungarian hamster
J Biol Rhythm
(1985)
M.J. Duncan et al.
Testicular function and pelage color have different critical photoperiods in the Djungarian hamster Phodopus sungorus
Endocrinology
(1985)
J. Figala et al.
Zur Jahresperiodik beim Dsungarischen Zwerghamster Phodopus sungorus sungorus Pallas
Oecologia
(1973)
W.E. Flint
Die Zwerghamster der Palaearktischen Fauna
(1966)
H. Glaser et al.
Energetics and nesting behavior of the northern white footed mouse Peromyscus leucopus noveboracensis
Physiol Zool
(1975)

G. Heldmaier et al.

Seasonal pattern and energetics of short daily torpor in the Djungarian hamster Phodopus sungorus

Oecologia

(1981)

G. Heldmaier et al.

Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus) living in natural photoperiod

J Comp Physiol [B]

(1981)

G. Heldmaier et al.

Pineal involvement in thermoregulation and acclimation

Pineal Res Rev

(1986)

G. Heldmaier et al.

Photoperiodic control and effect of melatonin on nonshivering thermogenesis and brown adipose tissue

Science

(1981)

G. Heldmaier et al.

Nonshivering thermogenesis and cold resistance during seasonal acclimation in the Djungarian hamster

J Comp Physiol [B]

(1982)

Cited by (25)

Glucose and insulin modulate sickness responses in male Siberian hamsters
2017, General and Comparative Endocrinology
Citation Excerpt :
When provided a nestlet, hamsters quickly start shredding the cotton to build a nest. Nest building is an adaptive behavior to enhance energy conservation in low temperatures, however, hamsters readily build nests in room temperature (20–23 °C) (Puchalski et al., 1988). Presentation of nestlets continued daily through day 3 post-injection.
Mounting a sickness response is an energetically expensive task and requires precise balancing of energy allocation to ensure pathogen clearance while avoiding compromising energy reserves. Sickness intensity has previously been shown to be modulated by food restriction, body mass, and hormonal signals of energy. In the current study, we tested the hypothesis that sickness intensity is modulated by glucose availability and an endocrine signal of glucose availability, insulin. We utilized male Siberian hamsters (Phodopus sungorus) and predicted that pharmacological induction of glucoprivation with 2-deoxy-d-glucose (2-DG), a non-metabolizable glucose analog that disrupts glycolysis, would attenuate energetically expensive sickness symptoms. Alternatively, we predicted that treatment of animals with insulin would enhance energetically expensive sickness symptoms, as insulin would act as a signal of increased glucose availability. Upon experimental treatment with lipopolysaccharide (LPS), we found that glucose deprivation resulted in increased sickness-induced hypothermia as compared to control- and insulin-treated animals; however, it did not have any effects on sickness-induced anorexia or body mass loss. Insulin treatment resulted in an unexpectedly exaggerated sickness response in animals of lesser body masses; however, in animals of greater body masses, insulin actually attenuated sickness-induced body mass loss and had no effects on hypothermia or anorexia. The effects of insulin on sickness severity may be modulated by sensitivity to sickness-induced hypoglycemia. Collectively, these results demonstrate that both glucose availability and signals of glucose availability can modulate the intensity of energetically expensive sickness symptoms, but their effects differ among different sickness symptoms and are sensitive to energetic context.
Leptin mediates seasonal variation in some but not all symptoms of sickness in Siberian hamsters
2014, Hormones and Behavior
Citation Excerpt :
When provided a nestlet, hamsters quickly start shredding the cotton to build a nest. Nest-building is an adaptive behavior to enhance energy conservation in low temperatures, however, hamsters readily build nests in room temperature (20–23 °C) (Puchalski et al., 1988). Presentation of nestlets continued daily through day 3 post-injection.
Many seasonally breeding species, including Siberian hamsters (Phodopus sungorus), exhibit seasonal variation in sickness responses. One hypothesis regarding the mechanism of this variation is that sickness intensity tracks an animal's energetic state, such that sickness is attenuated in the season that an animal has the lowest fat stores. Energetic state may be signaled via leptin, an adipose hormone that provides a signal of fat stores. Siberian hamsters respond to extended housing in short, winter-like days by reducing fat stores and leptin levels, relative to those housed in long, summer-like days. Sickness responses are also attenuated in short-day hamsters as compared to long-day hamsters. We hypothesized that leptin provides a physiological signal by which seasonally breeding animals modulate sickness responses, such that animals with higher leptin levels show increased sickness intensity. To test this, we provided short-day hamsters with a long-day-like leptin signal and assessed their responses to lipopolysaccharide (LPS), a sickness-inducing antigen. We compared these responses to short-day vehicle-, long-day vehicle-, and long-day leptin-treated hamsters. Unexpectedly, LPS induced a hypothermic response (rather than fever) in all groups. Short-day vehicle-treated hamsters exhibited the greatest LPS-induced hypothermia, and leptin treatment attenuated this response, making hypothermia more long-day-like. Contrary to our hypothesis, short-day leptin-treated hamsters showed the least pronounced LPS-induced anorexia among all groups. These results suggest that leptin may mediate some but not all aspects of seasonal sickness variation in this species. Future studies should be targeted at determining roles of other energetic hormones in regulating seasonal sickness response variation.
Huddling facilitates expression of daily torpor in the large Japanese field mouse Apodemus speciosus
2014, Physiology and Behavior
Citation Excerpt :
The practice is energetically expensive and endothermic animals are therefore obliged to employ a variety of behavioral and physiological adaptations to maintain energy balance, especially when faced with harsh winter conditions such as cold and food scarcity. These adaptations include torpor [2–4], huddling [5,6], intensive nesting behavior [7], molt into a better insulating pelage [8], increased thermogenic capacity [9], fat storage [10], and food hoarding [11]. The energy requirements per body mass of small endotherms are greater than in larger species because of their relatively large surface-area-to-volume ratio.
Small endotherms employ multiple adaptations to maintain energy balance in winter, including spontaneous daily torpor and simultaneous huddling. The relationships between these adaptations have been discussed in several previous studies, but it has not been well-established if huddling actually affects the expression of torpor in small endotherms. We examine whether and how huddling affects the expression of torpor in the large Japanese field mouse Apodemus speciosus, which is known to become torpid under artificial winter conditions. The mice were found to adjust expression of torpor in response to the number of cage mates. Torpor frequency and minimum torpid body temperature were both significantly elevated when the number of cage mates was increased, but there was no significant change in torpor bout length. Rewarming rate on arousal was lower when the number of cage mates was increased, suggesting reduction in endogenous rewarming due to exogenous passive rewarming. Food consumption per mouse decreased significantly with increasing number of cage mates. Thus, our study demonstrates that social thermoregulatory behaviors such as huddling can facilitate expression of spontaneous daily torpor in small rodents. These findings suggest that energy constraints, such as ambient temperature and food availability may not be the only modulating factors on the expression of daily torpor.
Behavioral tolerance to endotoxin is enhanced by adaptation to winter photoperiods
2008, Psychoneuroendocrinology
Citation Excerpt :
On the night following injection, coincident with lights-off, each hamster was also provided with access to a small piece of cotton batting (∼3 g) which was weighed before, and again 3 h after, presentation. This provided a measure of thermoregulatory behavior: energetic challenges increase the use of nesting material (Puchalski et al., 1988; Kauffman et al., 2003), and the availability of a nest reduces food intake in this species (Kauffman et al., 2003; Wen et al., 2007). Ten days later (week 13.5), behavioral tolerance was assessed by injecting all hamsters with LPS (625 μg/kg, i.p.) and measuring food intake and nesting material use over the next 72 h using procedures identical to those described for week 12.
Seasonal changes in day length enhance or suppress aspects of immune function in mammals. Following adaptation to short, winter-like short photoperiods, cytokine and behavioral responses to lipopolysaccharide (LPS)-induced simulated infections are attenuated in LPS-naive Siberian hamsters. This experiment examined whether diminished initial responses to LPS in short days (SDs) are accompanied by decrements in the development of innate immunological memory that leads to endotoxin tolerance. Male hamsters exposed to SDs (9 h-light/day) or kept in their natal long-day (LD) photoperiod (15 h-light/day) for 12–13 weeks were injected with bacterial LPS (625 μg/kg, i.p.) or sterile saline. Ten days later all hamsters were challenged with LPS (625 μg/kg, i.p.), and behavioral sickness responses (anorexia and reductions in nest building) were assessed. In LD hamsters, behavioral responses to the second LPS injection were markedly attenuated but still evident, indicative of partial tolerance. SD hamsters, in contrast, failed to exhibit anorexic or thermoregulatory responses to the second LPS injection, indicative of complete behavioral tolerance to LPS. Thus despite engaging greater naive responses to LPS, LD hamsters exhibited incomplete LPS tolerance relative to SD hamsters. The expression of behavioral tolerance to endotoxin is relatively diminished during the breeding season, a time of year when naive responses to endotoxin are at their greatest. During winter, enhancements in behavioral endotoxin tolerance may conserve energy and facilitate survival in the face of energetically challenging conditions.
The energetics of huddling in two species of mole-rat (Rodentia: Bathyergidae)
2008, Physiology and Behavior
Small rodents with a large surface-area-to-volume ratio and a high thermal conductance are likely to experience conditions where they have to expend large amounts of energy in order to maintain a constant body temperature at low ambient temperatures. The survival of small rodents is thus dependent on their ability to reduce heat loss and increase heat production at low ambient temperatures. Two such animals are the social subterranean rodents Cryptomys damarensis (the Damaraland mole-rat) and Cryptomys hottentotus natalensis (the Natal mole-rat). This study examined the energy savings associated with huddling as a behavioural thermoregulatory mechanism to conserve energy in both these species. Individual oxygen consumption (VO₂) was measured in groups ranging in size from one to 15 huddling animals for both species at ambient temperatures of 14, 18, 22, 26 and 30 °C. Savings in energy (VO₂) were then compared between the two species. Significant differences in VO₂ (p < 0.05) were found within each species, indicating that both Damaraland mole-rats and Natal mole-rats saved more energy in larger as opposed to smaller groups. VO₂ was also different between the two species, with Damaraland mole-rats showing a higher decrease in VO₂ with increasing group size compared to Natal mole-rats. These findings suggest that huddling confers significant energy savings in both species and that the amount of energy saved is related to each species' ecology. More generally, these findings suggest that group living desert-adapted species are likely to be more prone to heat loss at low ambient temperatures than temperate-adapted species, especially at low group sizes. This is presumably offset against the advantages obtained by having a low metabolic rate and avoiding hyperthermia when temperatures are hot.
Huddling, locomotor, and nest-building behaviors of furred and furless Siberian hamsters
2003, Physiology and Behavior
Rodents living in the cold employ both behavioral and physiological mechanisms to achieve thermoregulation. We examined the impact of fur loss on behavioral thermoregulation in cold-challenged Siberian hamsters (Phodopus sungorus). Intact female hamsters exposed to an ambient temperature (T_a) of 5 °C increased their general locomotor activity by 50% relative to animals maintained at 23 °C. At both T_a's, fur removal resulted in substantial increases in daily food intake (37% and 22% at 5 and 23 °C, respectively) but did not affect the amount of locomotor activity; increased food intake after fur loss evidently is not caused by increases in locomotor activity. Furred hamsters housed in groups of three at 5 °C consumed 16% less food per day than did singly housed individuals. Fur removal resulted in identical 39% increases in food intake in group- or singly housed animals. Energy savings that accrued from huddling were identical in furred and furless animals; this behavior conserves energy even in the absence of an insulative pelage. The availability of nesting material resulted in an 18% reduction in food consumption in intact animals kept at 5 °C. The increase in food intake produced by fur removal was attenuated by ∼80% when furless animals had access to nesting material. Huddling and nest-building behaviors each ameliorate energetic challenges posed by absence of fur; animals that concurrently employ several modes of thermoregulation realize substantial energy savings in the cold.

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Physiology & Behavior

Abstract

References (31)

Nest building behavior in seven species of muroid rodents

Behav Neural Biol

Experiments on nest-building behaviour in Peromyscus (Rodentia: Cricetinae)

Anim Behav

Effects of temperature and social interactions on huddling behavior in Mus musculus

Physiol Behav

Photoperiod and temperature effects on adrenal tyrosine hydroxylase and its relation to nonshivering thermogenesis

Pflugers Arch

Antigonadal effect of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): Duration is the critical parameter

Endocrinology

Circadian regulation of pineal melatonin and reproduction in the Djungarian hamster

J Biol Rhythm

Testicular function and pelage color have different critical photoperiods in the Djungarian hamster Phodopus sungorus

Endocrinology

Zur Jahresperiodik beim Dsungarischen Zwerghamster Phodopus sungorus sungorus Pallas

Oecologia

Die Zwerghamster der Palaearktischen Fauna

Energetics and nesting behavior of the northern white footed mouse Peromyscus leucopus noveboracensis

Physiol Zool

Seasonal pattern and energetics of short daily torpor in the Djungarian hamster Phodopus sungorus

Oecologia

Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus) living in natural photoperiod

J Comp Physiol [B]

Pineal involvement in thermoregulation and acclimation

Pineal Res Rev

Photoperiodic control and effect of melatonin on nonshivering thermogenesis and brown adipose tissue

Science

Nonshivering thermogenesis and cold resistance during seasonal acclimation in the Djungarian hamster

J Comp Physiol [B]

Cited by (25)

Glucose and insulin modulate sickness responses in male Siberian hamsters

Leptin mediates seasonal variation in some but not all symptoms of sickness in Siberian hamsters

Huddling facilitates expression of daily torpor in the large Japanese field mouse Apodemus speciosus

Behavioral tolerance to endotoxin is enhanced by adaptation to winter photoperiods

The energetics of huddling in two species of mole-rat (Rodentia: Bathyergidae)

Huddling, locomotor, and nest-building behaviors of furred and furless Siberian hamsters

ArticlePhotoperiod, temperature and melatonin effects on thermoregulatory behavior in Djungarian hamsters

Abstract

Behav Neural Biol

Anim Behav

Effects of temperature and social interactions on huddling behavior in Mus musculus

Physiol Behav

Photoperiod and temperature effects on adrenal tyrosine hydroxylase and its relation to nonshivering thermogenesis

Pflugers Arch

Antigonadal effect of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): Duration is the critical parameter

Endocrinology

Circadian regulation of pineal melatonin and reproduction in the Djungarian hamster

J Biol Rhythm

Testicular function and pelage color have different critical photoperiods in the Djungarian hamster Phodopus sungorus

Endocrinology

Zur Jahresperiodik beim Dsungarischen Zwerghamster Phodopus sungorus sungorus Pallas

Oecologia

Die Zwerghamster der Palaearktischen Fauna

Energetics and nesting behavior of the northern white footed mouse Peromyscus leucopus noveboracensis

Physiol Zool

Seasonal pattern and energetics of short daily torpor in the Djungarian hamster Phodopus sungorus

Oecologia

Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus) living in natural photoperiod

J Comp Physiol [B]

Pineal involvement in thermoregulation and acclimation

Pineal Res Rev

Photoperiodic control and effect of melatonin on nonshivering thermogenesis and brown adipose tissue

Science

Nonshivering thermogenesis and cold resistance during seasonal acclimation in the Djungarian hamster

J Comp Physiol [B]

Article
Photoperiod, temperature and melatonin effects on thermoregulatory behavior in Djungarian hamsters