Phenology of hibernation and reproduction in ground squirrels: integration of environmental cues with endogenous programming

Abstract

Mammalian hibernation is characterized by prolonged dormancy consisting of pronounced depression of metabolism and body temperature. Though hibernation occurs in at least seven mammalian orders and several families of the order Rodentia, the ecology and physiology of hibernation in rodents has been most extensively studied in the family Sciuridae, particularly in the so‐called ground squirrels, that is, the tribe Marmotini. Early studies of these rodents demonstrated the important role of an endogenous circannual clock in the persistence of annual timing and phasing of key seasonal events, including weight gain, hibernation and reproduction. Here, we review the causes and consequences of intraspecific variation in the timing of hibernation and reproduction in these sciurids and examine the physiological mechanisms that contribute to phenotypic plasticity in seasonal timing. Although the duration, annual phasing and predictability of seasonal change in environmental conditions likely promoted the evolution of endogeneity, precision and brevity of breeding seasons in the annual cycles of sciurids, substantial intraspecific variation in hibernation and reproductive phenology exists along latitudinal and altitudinal clines, as well as among locally varying environmental micro‐conditions. We suggest that much of this variation is a function of plasticity in the physiological mechanisms controlling annual cycles. While studies of captive animals have been instrumental in establishing the role of an endogenous rhythm, a greater emphasis on experimental field manipulations is needed to better understand the function, causes and consequences of phenological shifts in wild populations. Ultimately, the capacity of hibernators to adjust their timing in response to changing environmental conditions, either through phenotypic plasticity or microevolution, will be an important determinant of the resilience of sciurid species to changing climate.

Metabolic Flexibility: Hibernation, Torpor, and Estivation

“…The cycle is entrained and affected by environmental conditions (see ref. 305 for an excellent review), as illustrated by comparisons of three woodchuck (Marmota monax) populations spread over a large latitudinal gradient. Not surprisingly, in the wild the more polar (northerly) population starts hibernating earlier in the autumn, stops hibernating later in the spring and spends more total time torpid compared with more southern populations (314).…”

Modelling mammalian energetics: the heterothermy problem

“…For a species with readily predictable torpor bout lengths and hibernation seasons of a set length, such as the Holarctic ground squirrels (family Sciuridae, tribe Marmotini, [142]), this would often cover the winter months only (eg. [143]), although this may also change based on latitude or local climate conditions [144,145]. Such obligate hibernators, must undergo significant pre-hibernation fattening before entering into torpor [30,105,146,147].…”

When to initiate torpor use? Food availability times the transition to winter phenotype in a tropical heterotherm

“…To date, it remains controversial whether heterothermy is mainly expressed in anticipation of upcoming seasonal unfavourable conditions, and triggered by fixed seasonal cues, or mainly a flexible thermal strategy that fine-tunes energy expenditure according to short-term fluctuations in energy availability (Vuarin and Henry 2014;Williams et al 2014). Photoperiod is an ubiquitous, proximal environmental cue for seasonal acclimation (Helm et al 2013).…”