Cold exposure and food restriction facilitate physiological responses to short photoperiod in Djungarian hamsters (Phodopus sungorus)

Abstract

We investigated the influence of ambient temperature (Ta) and food availability on seasonal timing and extent of physiological responses to short photoperiod (SP), in particular daily torpor, in Djungarian hamsters (Phodopus sungorus). Exposure of hamsters to cold temperature (Ta = 5 degrees C), relative to warm Ta (23 degrees C), resulted in: 1) a significant advance (P < 0.05) of the first occurrence of torpor among cold-exposed hamsters (days 52-97 vs. days 83-99 in SP); 2) a higher (P < 0.01) incidence of torpor (48% vs. 20% torpid animals/day); 3) a higher (P < 0.05) degree of molt into the winter pelt; and 4) an accelerated reduction of body weights (P < 0.001). However, within SP/cold-Ta exposed groups, individual hamsters clearly showed different tendencies for torpor (torpor on 0-95% of days observed). Therefore, we evaluated the effects of small changes in Ta on torpor frequency and extension by subjecting the same SP-adapted individuals to varying temperatures. Lowering of Ta from 15 degrees C to 10 degrees C and 5 degrees C caused significant (P < 0.05) increases in the incidence of torpor (20%, 33%, and 40%, respectively) and lower minimal body temperatures during hypothermia (P < 0.05). When the same animals were subjected to 24-48 h lasting periods of food restriction (60% of the ad libitum intake), torpor frequency further increased 1.8- to 2.6-fold at all Tas. These results show that Ta and food availability are effective in modifying both seasonal timing and extent of photoperiodically controlled adaptations. This integration of multiple environmental cues, combined with a pronounced within-species variability of winter adjustments, indicates that Djungarian hamsters are capable of flexible physiological responses towards unpredictable climatic changes in the environment.

Specialist-generalist model of body temperature regulation can be applied on the intraspecific level

“…This was supported by the present results; we used male mice and we did not find torpor bouts described for females of the species elsewhere (Dikic et al, 2008;Hudson and Scott, 1979;Schubert et al, 2010;Swoap and Gutilla, 2009). However, contrary to animals that use torpor spontaneously and lower their T b only during rest phase (Ruf et al, 1993), fasted animals enter torpor regardless of the time of day (Dikic et al, 2008;Swoap and Gutilla, 2009), which is in line with the present results. T b of mice started to decrease on the first day of the experiment, and both diurnal and nocturnal T b,min decreased as food deprivation prolonged (Figs 1 and 2).…”

“…Based on the above, Boyles and Warne (2013) further predicted that in the face of energy limitation, specialists should be more prone to using facultative heterothermy than generalists. Food limitation and cold increase the costs of maintaining high T b and increase the frequency and lengthen duration of torpor bouts (Bozinovic et al, 2007; for rodent examples, see Ruf et al, 1993;Tomlinson et al, 2007). Hence, thermal generalists, or specialists that use facultative heterothermy, should be favored in environments with low or unpredictable energy supply (Lovegrove, 2000).…”

Basking hamsters reduce resting metabolism, body temperature and energy costs during rewarming from torpor

“…The resting T b of 34.7°C at T a 15°C was similar to that previously reported under similar thermal conditions (Ruf et al, 1993) and so was the decrease of RMR with T a (Heldmaier and Steinlechner, 1981), although our values were slightly lower. The torpor patterns of hamsters observed here were somewhat unusual because hamsters often expressed more than one torpor bout per day, but it is known that multiple bouts per day may be used by the species, especially when food is withheld (Steinlechner et al, 1986;Diedrich et al, 2015), as in our measurements.…”

“…A well-known example is the Djungarian hamster, Phodopus sungorus (body mass ∼30 g), which changes its fur from brown in summer (or when long photoperiod acclimated) to almost entirely white in winter (or when short photoperiod acclimated) (Steinlechner et al, 1986;Ruf et al, 1993;Hiebert et al, 2000;Geiser et al, 2013;Cubuk et al, 2015). White winter-acclimated individuals enter spontaneous daily torpor (food ad libitum), whereas brown summer-acclimated animals do not (Heldmaier and Steinlechner, 1981;Ruf et al, 1993;Geiser et al, 2013).…”

“…White winter-acclimated individuals enter spontaneous daily torpor (food ad libitum), whereas brown summer-acclimated animals do not (Heldmaier and Steinlechner, 1981;Ruf et al, 1993;Geiser et al, 2013). Little is known about the ecology and biology of the species in the wild, but they live in steppes of central Asia that receive substantial amounts of sun in winter and they do not restrict activity to the night (Flint, 1966), as is also the case in captivity, especially when exposed to low T a (Heldmaier et al, 1989;Ruf et al, 1991;Müller et al, 2015).…”