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The heat dissipation limit hypothesis suggests that the capacity for lactating mammals to transfer energy to their offspring through milk may be constrained by limits on heat dissipation, particularly in species that raise offspring in well-insulated nests. We tested a prediction of this hypothesis by evaluating whether lactating free-ranging red squirrels (Tamiasciurus hudsonicus) occupy less insulated nests when experiencing conditions that increase heat load. In support of the hypothesis, when climate normal ambient temperatures were warm, squirrels supporting large litter masses of furred offspring occupied nests of lower insulative value. These results support the heat dissipation limit hypothesis and suggest that free-ranging mammals may select nests based on their insulative value, not only to reduce heat loss in cold conditions but also to dissipate heat during periods of heat stress.
The parental care hypothesis for the evolution of endothermy proposes that endothermy evolved to facilitate the increased aerobic capacity and warm temperatures required for rapid juvenile provisioning and growth (Farmer 2000; Koteja 2000). Considerable research has focused on what limits energy export during lactation (Hammond & Diamond 1997; Bacigalupe & Bozinovic 2002), because higher energy export should allow females to raise more, faster-growing offspring and thereby increase reproductive success (Clutton-Brock 1991; Thompson 1992). The recently proposed heat dissipation limit hypothesis suggests that energy export during lactation is limited by the ability of mothers to dissipate heat associated with milk production (Król & Speakman 2003). Experimental manipulations of the conductance of laboratory animals demonstrates that heat stress reduces the quantity and quality of milk exported (Król & Speakman 2003; Król et al. 2007). These findings are intriguing because, although endothermy may have evolved to enhance parental care (Farmer 2000; Koteja 2000), heat stress may presently be limiting energy export during lactation in some mammals.
The implications of the heat dissipation limit hypothesis to free-ranging mammals have never been examined. Heat load experienced by lactating females is a function of heat production, determined by the combined mass and metabolic rate of mothers and offspring occupying the nest, and heat dissipation, determined by the thermal conductance of the mother, nest insulation and environmental conditions. Thus, negative consequences of heat production during lactation are likely to be experienced by mammals raising litters of large mass, in well-insulated nests, during periods of warm ambient temperature. To prevent excessive insulation from becoming a liability to parental care, free-ranging mammals may avoid heat stress by selecting nests with differing insulative values (Puchalski et al. 1988). Thus, a key prediction arising from the heat dissipation limit hypothesis is that the insulation of nests occupied by lactating females should be affected by the conditions that influence heat production and dissipation. We tested this prediction on a high latitude population of free-ranging red squirrels (Tamiasciurus hudsonicus) that nurse pups across a wide range of ambient conditions, by evaluating whether the insulation of nests occupied by lactating females is less under conditions when heat production within the nest is high and ambient conditions limit heat dissipation.
Adult and pre-weaned juveniles on five study areas in southwestern Yukon, Canada (61°N, 138°W) were enumerated using standardized methodology (McAdam et al. 2007). Females give birth to litter sizes averaging 3.1 naked offspring (1–7 pups) that are weaned at approximately 70 days (McAdam et al. 2007). Squirrels occupy multiple nests within their territories (S. Boutin 1987–2008, unpublished data). Nests are constructed of grass balls situated in the branches of white spruce (Picea glauca) trees, within witches' brooms (Chrysomyxa arctostaphyli) infecting spruce trees, spruce or aspen (Populus tremuloides) cavities or underground.
We entered 45 nests and recorded the number and mass of pups when they were furless (0–10 days old; furless nest entry) and when they had fur (18–28 days old; furred nest entry). We examined 17 furless and 28 furred nest entries (range of entries 27 May 2007 to 14 August 2007). Nest types included 22 grass, 11 witches' brooms, nine cavities and three underground nests.
Red squirrels routinely move their litters to different nests following entries (S. Boutin 1987–2008, unpublished data), allowing us to quantify the insulation of recently vacated nests. Nest insulation was measured in the evening (start times 18.45–23.45) on the same day of the nest entry (n=34 nests), the day after (n=9) or two days after (n=2). The insulation of vacated nests was determined by comparing the cooling rates of one water bottle that was placed inside the nest, and another that was hung above ground less than 1m away (Redman et al. 1999). Water bottles (HDPE plastic 125ml, Nalge Nunc International) were filled with hot water from a common thermos. Temperature data loggers (iButton; Maxim Integrated Products) were suspended in the water bottles using a nylon stocking to avoid contact with the bottle walls. Bottle water temperature (Tw; 0.5°C increments) was recorded every 5s while air filled white balls (ovoids 4.5×3.1cm), hung less than 5m from the nest and recorded ambient temperature (Ta). The start point of cooling rates was 10min after the bottle was placed in the nest, to ensure that the bottle inside the nest had warmed the interstitial air space (Lamprecht & Schmolz 2004). Tw readings taken over 2h were converted to levels of heat . Nest insulation was measured as the ratio of the cooling rate slopes (ln[Q] versus ln[time]) of the outside bottle (boutside) over the nest bottle (bnest; insulation=boutside/bnest; Redman et al. 1999); therefore, more insulated nests had higher insulation values. These measurements were conducted in the evening to reduce sunlight and wind on the nest, and outside bottle. Insulative values did not vary according to Ta at the start time (p=0.73) or wind speed (land adapted Beaufort scale; p=0.77), and there was no difference between the insulation of nests quantified on the day of the nest entry and those that were quantified ≥1 day(s) later (F1,43=0.40, p=0.53).
We evaluated how insulation varied according to nest type, heat production within the nest, nest stage (furless versus furred) and ambient temperature. The combined body mass (MB) of all offspring at the time of nest entry (litter mass: ML) was used as an index of heat production within the nest. Previous estimates of the field metabolic rate (FMR, kJd−1; Speakman 1997) of pre-weaned juveniles revealed a strong relationship between log10MB and FMR (b=1.21±0.12 s.e.; r2=0.50, F1,104=104.7, p<0.001; Q. E. Fletcher, J. R. Speakman & M. M. Humphries 2003–2006, unpublished data). Lactating female MB was not incorporated into our index of heat production within the nest because there is no overall relationship between log10MB and FMR of lactating females (b=0.21±0.39; r2=0.002, F1,141=0.29, p=0.59; Q. E. Fletcher, J. R. Speakman & M. M. Humphries 2003–2006, unpublished data). We compared the furless versus furred nest stages because furless pups were unlikely to be homeothermic (Knight 1987), and thus contributed less to heat load. To evaluate whether nest insulation varied according to prevailing ambient temperatures during the 24h prior to the nest entry or according to the expected seasonal temperatures, we obtained mean and maximum daily temperature (Tmean, Tmax; Environment Canada: Haines Junction, Yukon, 60°N, 136°W; approx. 30km from study areas), and climate normal mean temperature (Tcn; 1967–2006; Burwash, Yukon, 61°N, 139°W; approx. 70km from study areas; Tcn values were not available from Haines Junction).
We evaluated the predictors of insulation using linear (LM) and linear mixed models (LME; www.r-project.org; v. 2.5.1). Squirrel identification (ID) was included as a random factor because we determined the insulation of both the furless and furred nest entries for eight females. The inclusion of ID did not improve the fit of the full model (likelihood ratio test: p>0.43), so ID was excluded from subsequent models. Model simplification was used to test our hypotheses that factors increasing the heat production and reducing heat dissipation would be associated with lower insulation levels. To simplify our full factorial models, one effect was removed at each step (p>0.10), with higher order interactions considered first and main effects second. Main effects were retained if their interactions were retained.
There was no difference between the insulation of the four nest types (F3,41=1.36, p=0.27). From a full factorial model including nest stage (furless and furred), Tcn and ML (pooling the nest types), model simplification retained the significant or marginally significant two-way interactions of nest stage by Tcn (F1,39=5.01, p=0.03) and nest stage by ML (F1,39=3.66, p=0.06), in addition to the significant main effect of nest stage (F1,39=5.26, p=0.03). Nests were less insulated when pups were furred (3.35±0.13s.e.) than when pups were furless (3.89±0.21; figure 1a). Moreover, the insulation of nests at furred entries, but not furless entries, decreased with increasing ML and increasing Tcn (figure 1b). The main effects of Tcn (F1,39=0.98, p=0.33) and ML (F1,39=1.78, p=0.19) were not significant but were retained in the model. In two subsequent analyses that substituted Tmean and Tmax for Tcn, neither Tmean nor Tmax were significant (p>0.10) and the same qualitative conclusions for the other parameters remained (analyses not shown). Tcn values were left skewed; however, the qualitative conclusions remain with reduced significance (p<0.076) when Box–Cox [λ=8] transformed Tcn values are substituted into the final model.
Our results suggest that squirrels occupy less insulated nests in response to the conditions that increase heat load. Overall, more insulated nests were occupied when pups were furless and this was not affected by the variation in ML and Tcn. Moreover, females occupied less insulated nests when caring for furred offspring when ML was larger. Furless pups are unlikely to be homeothermic (Knight 1987); therefore, they are less likely to contribute to excessive heat load and they might also benefit from the warmth and thermal stability offered by well-insulated nests (Newkirk et al. 1998).
Weaker relationships suggested that females caring for furred offspring occupied less insulated nests in response to warmer Tcn, but were not influenced by Tmean or Tmax. Past research has shown that Djungarian hamsters (Phodopus sungorus) alter nest properties in response to both photoperiod and short-term Ta variation (Puchalski et al. 1988). Our findings suggest that squirrels may match nest insulation to prevailing climatic norms. Long-term climatic averages may provide a more reliable basis for thermoregulatory decisions than short-term weather patterns, since the latter are less predictable and more prone to rapid reversals (Bronson 1985).
The heat dissipation limit hypothesis proposes that energy export during lactation is limited by the ability of mothers to dissipate body heat (Król & Speakman 2003). Our results suggest that heat dissipation is an important issue for lactating squirrels, even in high latitude environments, but also show that free-ranging squirrels can mitigate potential negative impacts of heat stress by reducing nest insulation. Squirrels may match nest insulation to heat load conditions by altering the insulative properties of a given nest (e.g. by adding or removing grass) or by switching nests based on thermal properties. Resolving the energetic effectiveness and parental care importance of these insulative adjustments requires expanding our research beyond quantifying nest insulation to examine how factors affecting heat load (e.g. litter mass, ambient temperature) influence the temperature profiles of occupied nests, maternal nest attendance and ultimately reproductive performance.
The animal research described here was approved by the Macdonald Campus Facility Animal Care Committee at McGill University and the Biosciences Animal Policy and Welfare Committee at the University of Alberta.We thank all squirrelers for fieldwork and anonymous reviewers for their suggestions. Funding was provided by the following grants: NSERC USRA (C.U.G.), NSERC PGS (Q.E.F.), NSERC Discovery (M.M.H., S.B.), NSF (A.G.M.) and NSTP (Q.E.F.). This is contribution number 46 of the Kluane Red Squirrel Project.