Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels.
View 12 excerpts, references background. View 1 excerpt, references background. Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Highly Influential. View 5 excerpts, references background.
Endogenous annual rhythm of reproductive function in the non-hibernating desert ground squirrelAmmospermophihis leucurus.
View 4 excerpts, references background. Evolutionary Ecology of Mammalian Hibernation Phenology. View 2 excerpts, references background. View 3 excerpts, references background. Data logging of body temperatures provides precise information on phenology of reproductive events in a free-living arctic hibernator. Interrelation of endogenous annual rhythms of reproduction and hibernation in the golden-mantled ground squirrel.
Related Papers. By clicking accept or continuing to use the site, you agree to the terms outlined in our Privacy Policy , Terms of Service , and Dataset License. A key question in contemporary ecology is whether rare, range-restricted species can change their behavior in response to climate change i. The northern Idaho ground squirrel, Urocitellus brunneus A. Howell, , is a federally threatened species that hibernates for approximately 8 months per year within the bounds of its small range in central Idaho, USA.
Changes in temperature, snow accumulation, and summer precipitation, all brought about as a result of climate change, may reduce survival or fecundity of northern Idaho ground squirrels if they cannot adapt to these climate changes. Hibernating species can respond to climate-change-induced thermal challenges in two ways: change their hibernation physiology and behavior i.
We explored a suite of intrinsic and extrinsic factors to document the extent to which they influenced hibernation behavior of northern Idaho ground squirrels. Emergence date was positively associated with snowpack and negatively associated with mean winter temperature. Duration of the heterothermal period, number of euthermic bouts, and total time spent euthermic were positively associated with body mass.
Immergence date and duration of the longest torpor bout were negatively associated with body mass. Warmer temperatures and less snow accumulation in the winter—caused by climate change—likely will cause altered emergence dates.
Our results suggest that any future climate-induced changes in snowfall, ambient temperature, food availability, or habitat likely will impact survival of this rare ground squirrel, because such changes will cause changes in hibernation behavior, percent mass loss during hibernation, and duration of the active season when small mammals are more susceptible to predation. Climate change is likely to impact plants and animals at many scales: individuals, populations, communities, and ecosystems.
Species not capable of responding appropriately to changes in climate to meet their bioenergetic or thermal needs may ultimately face extinction McCain and King Animals can potentially mitigate the impacts of climate change via one of two behavioral responses: 1 spatially e. We need to better understand the ability of imperiled animals to adjust to climate change via either or both of these mechanisms, because the frequency and magnitude of extreme climatic conditions are projected to increase Mote et al.
Many mammals use one of four strategies to survive challenging winter climate conditions: 1 migration to areas with more favorable conditions Telfer and Kelsall ; Avgar et al. Western North America is expected to have warmer summers, earlier spring snowmelt, and less snow accumulations i. Mammals that hibernate must select or create a hibernaculum within the desired temperature range or change their physiology to accommodate climate change effects.
Some hibernators enter into hibernation for a large part of a year, which may include both warmer temperatures and below-freezing temperatures. Hibernation may begin during the warmest part of the year and squirrels remain in hibernation throughout the winter to avoid cold and food stress Wang ; Wilz and Heldmaier ; Staples Animals that select a hibernaculum for long term across multiple seasons may be especially sensitive to changes in habitat suitability related to climate conditions e.
We know relatively little about the plasticity of behaviors related to hibernation and the capacity of hibernators to respond to climate change. However, there have been few studies on this topic and they have reported both positive Ozgul et al. Notwithstanding, it does appear that these species are changing their behavior in response to a changing climate—although the overall effect of these changes differs.
For instance, Inouye et al. Columbian ground squirrels Urocitellus columbianus emerged later in years with late season snow fall but this led to a shortened active season and reduced survival Lane et al. In addition, the optimal hibernaculum under one set of climatic conditions may not be the optimal hibernaculum under a different set of conditions such as animals that undergo multiseason hibernation. For example, northern Idaho ground squirrels, Urocitellus brunneus , are a federally threatened species and all individuals hibernate approximately 8 months per year, some beginning as early as July and emerging the following March Yensen and Sherman ; Sherman and Runge Thus, individuals begin torpor bouts during the warm summer months when body temperature will remain higher and total energy savings should be less than in the winter, i.
Northern Idaho ground squirrels are solo hibernators, hence do not share body heat with other conspecifics, as is the case in most marmot species Patil et al. Juvenile survival and yearling female breeding propensity of northern Idaho ground squirrels were lower than those of congeners, based on data from a year study Sherman and Runge Sherman and Runge hypothesized that the population they studied declined because animals were unable to enter hibernation with sufficient body reserves, which reduced the ability for squirrels to survive hibernation.
However, squirrels could potentially mitigate the effects of changes in nutrient availability by altering their hibernation behavior in ways that allow them to save energy and thereby survive the long hibernation period.
Climate-induced changes in environmental conditions over the past few decades may have changed the likelihood of one or more of these three requirements for survival. This rare ground squirrel also faces new challenges because the landscape that supports northern Idaho ground squirrels has changed over the past few decades Burak et al.
Fire suppression has allowed coniferous trees to encroach into some of the forest openings that support northern Idaho ground squirrels. Canopy cover of overstory trees reduces snow depth but increases the seasonal duration of snowpack Davis et al. Snow cover has an insulative effect and likely helps maintain a constant burrow temperature within hibernacula Svendsen ; Young a ; Tafani et al. Thus, snow cover likely influences optimal hibernacula depth.
As snow depth increases, the depth of frost in the soil column decreases Hardy et al. Hence, temperature of the hibernaculum, mediated by snowpack and hibernaculum depth, may influence overwinter survival of northern Idaho ground squirrels. Furthermore, canopy cover provides shade, reducing direct effects of the sun on soil temperatures, resulting in cooler soil temperatures with less temperature fluctuation prior to snow cover Breshears et al.
Snow depth and duration of winter snowpack therefore may affect northern Idaho ground squirrel survival by several mechanisms: 1 snow's insulating quality during hibernation; 2 deep snow may afford protection from terrestrial predators; and 3 the effect of snow on the date of vegetation green-up.
The latter may affect reproduction and survival during the subsequent year. To explore these relationships, we measured daily snow depth, ambient air temperature, and light intensity, at hibernacula locations of northern Idaho ground squirrels from through and examined the relationships among hibernation behavior, weather, and hibernacula habitat.
Many climate change effects are gradual, so examining their consequences on ground squirrels is difficult in field studies. We therefore used space-for-time substitution Blois et al.
And 2 what is the relationship between hibernaculum depth and weather, body condition, and other habitat features? We carried out field work at seven sites in Adams County, Idaho, from to The seven sites were on both public and private land and ranged in elevation from 1, to 1, m.
During the spring and summer active season, northern Idaho ground squirrels are associated with south-facing aspects U. Fish and Wildlife Service and open-canopy habitat meadows and rocky scabs patchily distributed within a forest mosaic Burak Active-season habitat contains a wide variety of grasses and forbs with a few patches of shrubs and trees Goldberg et al.
The surrounding forests where northern Idaho ground squirrels often hibernate— Goldberg et al. We trapped and collared northern Idaho ground squirrels between 2 June and 19 July each year. We attached ear tags to both ears on each squirrel for individual identification and recorded body mass, sex, and reproductive condition of each squirrel. We considered all females to be reproductively active if they had visual nipples which are only visible above the fur when they are nursing young Kenagy et al.
We attached collars to 56 females seven in , 16 in , 19 in , and 14 in and 43 males three in , 12 in , 14 in , and 14 in We deployed two models of light loggers: five Intigeo C65 in older model and 94 Intigeo F We used telemetry receivers and handheld antennas to locate hibernacula and retrieve dropped collars. Light loggers recorded both the light level which allowed us to document when a northern Idaho ground squirrel immerged and emerged from hibernation and the skin temperature T sk at min intervals 4-h intervals on the older C65 models.
Skin temperature measurements during hibernation should be similar to body temperature because light loggers produced temperature readings during hibernation that were similar to those from implanted thermochrons in Arctic ground squirrels Urocitellus parryii — Williams et al.
We used VHF collars to track squirrels to their hibernacula. The Biotrack collars were designed to emit a signal on a preselected schedule we programmed the collars to emit a signal 2 or 3 days per week to maximize the battery life. We collected four habitat measurements at each hibernaculum location to document the habitat conditions used by hibernating northern Idaho ground squirrels.
We placed a graduated staff gauge and a trail camera Bushnell Trophy Cam C, Bushnell Corporation, Overland Park, Kansas at hibernacula each fall we did not place snow gauges at two hibernacula due to a limited number of snow gauges from to to document depth of winter snowpack.
We preprogrammed cameras to photograph the gauge two times per day throughout the winter. We estimated the snow depth daily and the duration of snow cover throughout the winter at those six study sites based on the photographs of the staff gauges. Cameras occasionally died or failed due to disturbance human or wildlife , battery failure, or other malfunction Furthermore, snow occasionally was deeper than the height of the snow gauge; maximum depth of snow was capped at 1.
We placed two soil temperature probes in the ground at study sites: 1 one within an open-canopy area meadow where squirrels are active during the summer near a previously used summer burrow location ; and 2 one in the adjacent forest near a hibernaculum location from a previous year.
Each soil probe consisted of one 1. Temperature probes were inserted into the ground by digging a 1-inch-wide hole with a hand-auger. Due to the high density of rocks and tree roots, we were unable to dig a 1. We cut the PVC pipe to fit the depth to which we were able to dig at each location.
As a result, soil temperature probes varied in maximum depth and number of thermochrons from 0. We deployed the soil temperature probes in June and downloaded the temperature data from the soil probes after we retrieved the thermochrons the following spring.
We redeployed the temperature probes in the same locations each spring. We deployed Hobo temperature loggers Onset Computer Corporation, Bourne, Massachusetts to measure light intensity and air temperature during the active season: one in the open-canopy area and one in the forest under tree canopy. All the Hobo loggers were placed 1—1. Loggers in the forest were placed on a ponderosa pine branch close to the trunk to reduce impact of light on air temperature.
Over the winter, we deployed the Hobo temperature loggers at the hibernacula locations after the squirrel had entered into hibernation and at a snow gauge in the open-canopy areas. We weighed all squirrels that we captured from to we had body mass measurements from an ongoing companion study at the same study sites in years prior to collaring squirrels.
Body mass increases across the summer active season, so we sought to standardize our body mass measurements given that we caught animals throughout the 3-month summer active season May—July. The rate of seasonal increase in body mass should differ between males and females due to changes in mass brought on by pregnancy and lactation.
We therefore regressed adult body mass against capture date for each sex separately and also for each of the two trapping sessions spring and summer. We also expected body mass to differ among our seven study sites because they differed in elevation , so we included site in our regression models. These body mass regressions were calculated using a generalized linear model in program R v3. We recorded the residual body mass from those regressions as a seasonally adjusted metric of relative body mass for each adult squirrel.
We combined data from all years for these regressions because we had too few data for any 1 year at most of the seven study sites. We used generalized linear models to evaluate the relationships between our 15 explanatory variables and each of seven hibernation behaviors: 1 immergence date; 2 emergence date; 3 total length of the heterothermal period; 4 number of euthermic bouts during the heterothermal period; 5 total sum of the time spent euthermic; 6 longest torpor bout duration; and 7 mean minimum skin temperature T sk.
We did not evaluate all combinations of variables but rather used a common approach for model comparison and selection Burnham and Anderson ; Grueber et al. The number of squirrels for which we had missing values varied from zero to eight of 36 total for the 15 explanatory variables and varied from zero to 10 for the seven response variables.
So that we could use all 36 squirrels in our analyses, we used multiple imputation procedures to account for missing values. The mice package uses conditional multiple imputation, which is an iterative procedure that models the conditional distribution of a certain variable given the other variables. Multiple imputation, including for both response and explanatory variables, produces values that generally reflect the true patterns in the data Lang and Little One of the main advantages to PMM is that it is considered robust and able to preserve the distribution of the original data well Kleinke We assumed our data were missing at random MAR.
As a result, we created 47 imputed data sets that we ran separately for each of the seven response variables. We used methods described in Rubin to pool all point and variance estimates for each response variable based on our final model. MAMI carries out model selection and model averaging on multiple imputed data sets and combines the resulting estimates.
We used a Gaussian distribution and MA. Predicted relationship between each of 15 explanatory variables and seven response variables describing northern Idaho ground squirrel hibernation behavior. If a cell is blank, we did not believe there is a relationship. T sk refers to skin temperature and T a refers to air temperature. In addition, we evaluated all the univariate relationships between the 15 explanatory variables and the seven response variables for a total of 77 univariate tests.
We also used univariate analyses to evaluate the effects of pregnancy on the response variables; only females were included in this analysis, reducing our data set to 18 individuals. We assumed that a squirrel had entered its hibernaculum when all aboveground activity light readings ceased for more than 1 day based on data from the light loggers. We assumed that a squirrel had entered the heterothermal period when the first torpor bout was greater than 24 h. We assumed that the heterothermal period had ended when all subsequent torpor bouts were less than 24 h long.
Total torpor length, euthermic bout length, and number of euthermic bouts were only those that occurred during the heterothermal period. We assumed a squirrel had emerged when the light logger read lux or greater. We used the lux threshold to account for the fact that squirrels may poke their head up and resume hibernation in the early spring and we did not want to dismiss any final torpor bouts. Example of the skin temperature of a hibernating northern Idaho ground squirrel. We knew the exact age of 14 squirrels because we had trapped them in a prior year as juveniles.
However, if a squirrel was initially trapped as an adult and subsequently trapped again the following year, we knew it was at least 2 years old and we used 2. Similarly, if we trapped a squirrel as an adult and collared it 2 years later, we knew it was at least 3 years old and we used 3.
This approach allowed us to assign an age to as many squirrels as possible and to include age as a continuous variable in our models. Hibernation behavior can differ between yearlings and adults in other species Bailey and Davis ; Buck and Barnes a ; Bieber et al.
For the 36 squirrels for which we had hibernation behavior data, we were able to classify seven squirrels as yearlings, five as 2 years, one as 3 years, and one as 4 years. In addition, we assigned 11 as 1. Hibernacula habitat characteristics varied among squirrels, but we did not detect any significant differences between the sexes Table 2.
We obtained light logger data from 36 northern Idaho ground squirrels, three of which were collared during two winters, thus a total of 33 individuals for 36 hibernation events. No other individual squirrel exhibited this behavior i. Four other northern Idaho ground squirrels three males and one female emerged briefly and did not come aboveground again for 1.
Explanatory variables and two summary metrics means of raw data used to explain variation in hibernation behavior of northern Idaho ground squirrels Urocitellus brunneus. Sample sizes in parentheses. We included t -test statistics to test differences between males and females. T a is air temperature, T sk is skin temperature, and T s is soil temperature. Downed wood had a minimum diameter of 2 cm to be considered a log. We did not detect a difference in the number of days spent in their hibernacula between immergence and the start of the heterothermal period between females and males Table 2.
Females emerged later than males after the snow melted from the area above the hibernaculum Table 2. Females spent fewer days in their hibernacula after the heterothermal period ended compared to males Table 2 ; Fig. The lowest recorded T sk temperature during hibernation 0. Differences in hibernation phenology between male and female northern Idaho ground squirrels Urocitellus brunneus based on data from seven study sites in Adams County, Idaho from to Error bars represent standard errors.
Relationship between skin temperature and torpor bout duration for 33 northern Idaho ground squirrels Urocitellus brunneus in Adams County, Idaho. There was a nonlinear negative relationship between torpor bout duration and skin temperature for bouts prior to the longest torpor bout of the heterothermal period A , but no such relationship for torpor bouts following the longest torpor bout B.
Gray shading in panel A represents the standard error. Mean hibernacula depth was 0. The closest sensors we had to that depth were 0. However, we only had four probes at three sites that reached a depth of at least 0. Soil temperatures were higher in the meadow than in the forest for sensors at both 0.
T s also were higher at 0. The difference in mean T s between meadow and forest was greatest during the summer and early fall and lowest during the winter Fig. Overall soil temperature increased by 0. Soil temperature 30 cm belowground during the hibernation season 15 July to 1 April differed between hibernacula site in the forest and those in the meadow open canopy for northern Idaho ground squirrel Urocitellus brunneus hibernacula locations.
The four panels represent data from four study sites that differed in elevation: 1, m A , 1, m B , 1, m C , and 1, m D. The greatest difference in soil temperature between meadow and forest hibernacula were recorded in the first few months of hibernation. Standard errors are too small to be visually noticeable. The majority of the univariate relationships between hibernation behavior and our explanatory variables were similar to those from the full generalized linear models using the imputed data.
Model selection of the imputed data set suggested that eight of the 10 explanatory variables be included, but only residual body mass and canopy closure had a confidence interval that did not include zero Supplementary Data SD2. Univariate generalized linear model coefficients Est. Mean number of euthermic bouts was similar between sexes: Both heavier and older individuals had more euthermic bouts but only according to the univariate analysis; Table 3.
Model selection of the imputed data set suggested that eight of the 10 explanatory variables be included, but only residual body mass had a confidence interval that did not include zero Supplementary Data SD3. Similarly, heavier individuals and also males spent more total time euthermic Table 3 ; Supplementary Data SD4. Model selection of the imputed data set suggested that nine of the 10 explanatory variables be included, but only residual body mass and sex had a confidence interval that did not include zero Supplementary Data SD5.
Females Squirrels at higher elevation sites had longer heterothermal periods Table 3. Model selection of the imputed data set suggested that all 12 explanatory variables be included, but only residual body mass, sex, canopy closure, and minimum T b had confidence intervals that did not include zero Supplementary Data SD7.
The maximum torpor bout length was longest for those that had the lowest residual body mass Table 3. Model selection of the imputed data set suggested that nine of the 11 explanatory variables be included, but only residual body mass had a confidence interval that did not include zero Supplementary Data SD8. Squirrel age, snowmelt date, minimum T sk , slope, and soil temperature also may influence emergence date Table 3.
Model selection of the imputed data set suggested that all 13 explanatory variables be included in the top model, but only sex had a confidence interval that did not include zero Supplementary Data SD Mean minimum T sk during hibernation was 9. Eight of the 11 explanatory variables were included in the top model and none had confidence intervals that did not include zero Supplementary Data SD We retrieved 14 collars seven from females and seven from males from inside a hibernaculum and determined from them hibernaculum depth for 14 squirrels.
Depth of the hibernacula was similar between sexes 0. We did not find any correlations between hibernacula depth and the eight explanatory variables that we evaluated. Fifty-six percent of the female squirrels that we caught showed evidence of reproduction the summer prior to immergence into hibernation.
However, we did not find any correlations between reproductive condition and the seven response variables.
A changing climate may impact the effectiveness of behavioral choices that hibernators make to survive periods of extreme temperature.
Our results suggest that snow cover affects emergence date: squirrels emerged later at hibernacula in areas with deeper snow and later snowmelt. Snowfall totals and duration of snowpack are predicted to decline Mote et al. If an individual emerges too early, they may find suboptimal forage conditions. In contrast, emerging too late reduces the time an individual has available to consume food while it is most nutritious and easily digested compared to later in the summer when plants dry out and senesce.
It would be worthwhile to determine whether these behaviors are phenotypically plastic or fixed but vary among populations. Northern Idaho ground squirrel populations have moderate genetic differences that may reflect local selection regimes Gavin et al.
Females emerged later than males, similar to other ground squirrels Kenagy et al. Males exit hibernacula prior to female emergence to establish and defend territories and gain access to females Michener Female northern Idaho ground squirrels are sexually receptive for just a few hours on the first or second afternoon after they emerge Yensen and Sherman Emerging prior to females ensures that a male does not miss this short time window.
Heavier ground squirrels immerged earlier. Small-bodied hibernators should enter into torpor as soon as they are heavy enough to survive hibernation to reduce their risk of predation by spending additional days foraging aboveground Turbill et al.
In contrast to several studies on other ground squirrels Fagerstone ; Young b ; Millesi et al. Male ground squirrels immerge prior to females in many but not all species and the variation may reflect interspecific differences in the need to protect food caches for spring Millesi et al ; Williams et al.
If immergence date does not shift along with emergence date, earlier snow melt dates may lead to a prolonged active season shorter hibernation period and longer period of time exposed to higher predation rates Turbill et al.
Future climate scenarios predict that summers in central Idaho will be warmer with less rainfall Mote and Salathe , resulting in changes in plant phenology and diversity Bertin ; Khanduri et al. Climate-induced changes in hibernation behavior may result in phenological mismatches with preferred food items or changes in competitive interactions with other herbivores.
Furthermore, warmer temperatures during the peak active season lactation and peak mass gain may reduce the number of hours a squirrel can forage aboveground because many squirrels are subject to heat stress Vispo and Bakken ; Sharpe and Van Horne and may not be able to forage during the night.
Reduced forage time may lead to delays in immergence date due to difficulties in gaining the mass needed to survive the hibernation season. Examination is required to evaluate the effects of climate on timing, diversity, and quality of northern Idaho ground squirrel forage.
Body condition also affected northern Idaho ground squirrel euthermic bouts; body mass was positively correlated with the time spent euthermic and number of euthermic bouts. Similarly, heavier woodchucks Marmota monax had warmer body temperatures and spent less time in torpor Zervanos et al. However, we did not find relationships between T sk and maximum torpor length. Animals with extra energy may prefer to stay in torpor for less time because prolonged torpor can have negative consequences Humphries et al.
Furthermore, males had longer euthermic bouts than females. Males are heavier and have shorter heterothermal periods. Extra energy may be needed prior to female emergence while males defend their territory at a time when forage is suboptimal.
Potential functions of these euthermic bouts include: 1 reduce immune system suppression Prendergast et al. Hibernacula location may impact hibernation behavior. Higher canopy closure was positively related to immergence date, and slope was positively related to emergence date.
Further work is needed to understand the mechanisms underlying these relationships. Northern Idaho ground squirrel T sk while in torpor tracks soil temperature and likely does so until a fatal lower threshold Geiser et al.
Shallower hibernacula likely experience more fluctuation in soil temperature before snowfall Kay and Whitford ; Baker and Baker and likely have lower soil temperatures after snow has fallen Hardy et al. Soil temperatures during the hibernation season 15 July to 1 March in our system were warmer in the meadows open canopy compared to the forest Fig.
If cooler T s is preferred during the start of hibernation summer and early fall , squirrels either should select deeper hibernacula or areas with greater canopy closure.
Northern Idaho ground squirrels may select hibernacula in forests rather than in open areas, especially at higher elevations Goldberg et al. Further research is needed to better understand how snow depth and duration impact soil temperature and how both interact with canopy closure to influence optimal thermal conditions for hibernation of this rare ground squirrel.
Furthermore, we also need more information regarding the consequences of variation in hibernaculum depth. Hibernacula depths varied between 0. Depth of hibernacula may be regulated by: 1 predator avoidance; 2 ideal thermal conditions Young b ; Michener ; Buck and Barnes b ; 3 energetics the amount of energy necessary to dig a deeper burrow ; or 4 some combination of the three mechanisms. Our results are in line with those from previous studies and suggest that increased parasympathetic activation plays a key role in the reduction in HR at den entry in bears as well, but does not rule out potential decreases in sympathetic nervous system activity.
Although den exit was not correlated with either T A or photoperiod, the bears exited the dens at T A of 3. A bear den is not an adiabatic shell, however, the inside air temperature could easily rise, depending on the type of den ant hill, under rocks or nests [ 41 ]. The fairly narrow range of T b between bears on the day of exit That T A does not drive T b during the phase before exit period 5, Table 1 might be due to the adaptive thermoregulation that occurred over several months, making the T A immediately around the day of exit less important.
It could also be that the den temperature was more relevant, as the bears exited when T A reached approximately 3. T b started rising 2 months prior to exit, whereas HR rose a month later, and was followed by SDANN 20 days prior to exit and activity 10 days prior to exit.
The gradually decreasing difference between T b and T A during the first period Additional file 1 : Figure S5 , suggests that bears were thermoregulating at a lower thermoregulatory set point during hibernation.
This is consistent with recent findings from captive bears showing a negative relationship between den temperatures and hibernating metabolic rates [ 42 ]. Then, SDANN started rising and may have caused T b and HR to rise, likely via an increase in sympathetic nervous system activity, a decrease in parasympathetic nervous system activity, or a combination.
At this stage T b lost its causal association with T A although T b -T A remained stable during the second period, suggesting that euthermic metabolism was reestablished later by active thermogenesis, likely involving the sympathetic nervous system. The exact roles of the sympathetic and parasympathetic nervous systems in this process can only be assessed by direct measurements of sympathetic and parasympathetic nervous system activity in free-ranging conditions, which would be difficult to conduct.
This could indicate transitioning out of hibernation i. Den exit occurred when T b was almost at euthermia mean T b and SDANN stabilized quickly within two weeks after den exit , but HR and activity took longer, indicating that the bears took longer to return to their original activity levels.
Although shivering may play a role in active thermogenesis, it occurs at the end of arousal in the species studied to date, excluding tropical hibernators [ 44 ]. Increased T b allows restoration of enzyme functioning through a Q 10 effect and contributes to restoration of muscle function. Early on, the processes start with SNS activation of the vascular system to increase body temperature and heart rate [ 44 ]. The role of SNS in thermogenesis in addition to vascular control has also been the topic of numerous investigations starting from the early studies of Lyman.
Studies on American black bear in the laboratory show a role for shivering at the end of arousal [ 34 ], although our results show that it was less important in free-living conditions. A recent study on captive American black bears found that metabolic rate was related to den temperature and showed that larger bears showed more variation in length of T b cycles [ 42 ].
During experimental manipulations of den temperature, they found no direct relationship between den temperature and T b , although the time between peaks in T b became longer at higher den temperatures. The authors suggested, based on a single bear that increased its T b to It is not clear whether this was merely an effect of being inside an isolated den or was a physiological phenomenon.
Interestingly, they found no relationship between T A and den temperatures. Although it was not possible to measure the den temperatures in our study, we would expect a correlation with T A , because the bears in our study were not in adiabatic shells; they were under rocks or tree roots or in anthills, with oxygen exchange varying from a small ventilation hole to large openings under rocks.
Although [ 42 ] found a negative relationship between T A and metabolic rate, we conclude that this is more likely an adaptive thermoregulation allowing maintenance and slowly rising T b at a minimal cost, simultaneously with the increasing T A. In a previous study, the HR in captive black bears was reported to decline gradually over five weeks from the date that food and water were removed [ 45 ].
Our results would have been enhanced considerably had we succeeded at measuring den temperature. Bears in this population are very susceptible to disturbance in winter [ 46 ], repeatedly changing dens after captures or capture attempts, so putting temperature loggers inside the den was not realistic.
Our novel results and the methods adapted for this analysis could impact our general understanding of how climate change influences other ecophysiological and behavioral adaptations.
In this study, we demonstrate mechanisms for the entry and exit into hibernation by the brown bear in Sweden that have implications for both bear population monitoring and management. These results highlight some of the differences between the bear and small hibernators, reinforcing the importance of not generalizing results from small hibernators to bears. This work is an example of how different types of datasets can be combined to provide coherent ecophysiological timeseries with potential applications for other ecophysiological and adaptation studies beyond hibernation.
The results from such analyses would provide management strategies and production optimization, while minimizing ecosystem-level impacts. Besides conservation practices, our study demonstrates the importance of several physiological and behavioral characteristics that are important for studies of adaptation, in this case to winter conditions and to climate change, in the context of selection pressures for matching the start and end of hibernation with resource availability.
We demonstrate that changes in brown bear T b during den entry were driven by environmental factors, particularly T A. This indicates that a warming climate could result in later den entry. Thus, although many studies have shown that den entry and exit are related to food availability, climate change also appears to be an important factor affecting the timing of the life events of the brown bear and could pose a threat through the mismatch of important physiological cues.
This should be anticipated by wildlife management agencies in areas where there is a large overlap between humans and bears. Further, this study suggests that Scandinavian brown bears terminated their hibernation due to physiological cues.
Although body temperature started to rise slowly very early in the hibernation period, it was only few weeks before exit that we observed activation of the sympathetic nervous system to restore euthermic metabolism. Hibernation in brown bears seems to be initiated based on environmental cues and terminated due to physiological cues. Andrew Allen Swedish Agricultural University prepared temperature and snow depth maps. The insertable cardiac monitors were donated by Medtronic Inc.
This is scientific paper no. Additional file 1: 10M, docx Supplemental Figures and Tables. DOCX kb. Co-first author is N. Competing interests. Data analysis and preparation of fig. Evans, Email: on. Singh, Email: es. Friebe, Email: ofni. Arnemo, Email: on. Laske, Email: moc. Swenson, Email: on. Blanc, Email: rf. National Center for Biotechnology Information , U.
Journal List Front Zool v. Front Zool. Published online Feb Evans , N. Singh , A. Friebe , J. Arnemo , T. Laske , O. Swenson , and S. Author information Article notes Copyright and License information Disclaimer. Corresponding author. Received Jan 29; Accepted Feb 4. This article has been cited by other articles in PMC. Abstract Background Hibernation has been a key area of research for several decades, essentially in small mammals in the laboratory, yet we know very little about what triggers or ends it in the wild.
Results To our knowledge, we have built the first chronology of both ecological and physiological events from before the start to the end of hibernation in the field.
Conclusions We conclude that brown bear hibernation was initiated primarily by environmental cues, but terminated by physiological cues. Electronic supplementary material The online version of this article doi Keywords: Body temperature, Denning ecology, Metabolic inhibition, Physiological ecology, Thermoregulation.
Background Hibernating mammals are good models for investigating the relationship between physiology, behavior, and environment, as hibernation patterns are important determinants of survival [ 1 ]. Data collection Fourteen bears 8 males, 6 females, 2—8 years old, 30— kg were captured by darting from a helicopter from April to June , , and [ 14 , 15 ].
Open in a separate window. Casual relationships To identify the causal relationships between the monitored environmental and physiological variables, we used a convergent cross-mapping approach devised to detect causal relationships between pairs of processes represented by time series [ 11 ].
Table 1 Cross Convergent Mapping 11 analyses of the causation between different ecophysiological variables. Results The longitudinal design of the study resulted in a combined total of 38 years of bear data data summary, Fig. Discussion During the den entry period, T b and activity level appeared to be influenced by environmental factors, such as T A and snow depth. Drivers of den exit Although den exit was not correlated with either T A or photoperiod, the bears exited the dens at T A of 3.
Conclusions We demonstrate that changes in brown bear T b during den entry were driven by environmental factors, particularly T A. Footnotes Co-first author is N. Competing interests Timothy Laske is an employee of Medtronic Inc. Contributor Information A. References 1. Hibernation is associated with increased survival and the evolution of slow life histories among mammals.
Climate change is affecting altitudinal migrants and hibernating species. Climate-mediated energetic constraints on the distribution of hibernating mammals. Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Light, time, and the physiology of biotic response to rapid climate change in animals. Annu Rev Physiol. Coupled dynamics of body mass and population growth in response to environmental change.
Kearney M, Porter W. Ecol Lett. Wikelski M, Cooke SJ. Conservation physiology. Trends Ecol Evol. Geiser F.
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