Free-ranging eastern chipmunks (Tamias striatus) infected with bot fly (Cuterebra emasculator) larvae have higher resting but lower maximum metabolism

Given the ubiquity and evolutionary importance of parasites, their effect on the energy budget of mammals remains surprisingly unclear. The eastern chipmunk (Tamias striatus (L., 1758)) is a burrowing rodent that is commonly infected by cuterebrid bot fly (Cuterebra emasculator Fitch, 1856) larvae. We measured resting metabolic rate (RMR) and cold-induced [Vo.sub.2]-max (under heliox atmosphere) in 20 free-ranging individuals, of which 4 individuals were infected by one or two larva. We found that RMR was significantly higher in chipmunks infected by bot fly larvae (mean [+ or -] SE = 0.88 [+ or -] 0.05 W) than in uninfected individuals (0.74 [+ or -] 0.02 W). In contrast, V[O.sub.2]-max was significantly lower in chipmunks infected by bot fly larvae (4.96 [+ or -] 0.70 W) than in uninfected individuals (6.37 [+ or -] 0.16 W). Consequently, the aerobic scope (ratio of [Vo.sub.2]-max to RMR) was negatively correlated with the number of bot fly larvae (infected individuals = 5.74 [+ or -] 1.03 W; noninfected individuals = 8.67 [+ or -] 0.26 W). Finally, after accounting for the effects of body mass and bot fly parasitism on RMR and [Vo.sub.2]-max, there was no correlation between the two variables among individuals within our population. In addition to providing the first estimate of [Vo.sub.2]-max in T. striatus, these results offer additional evidence that bot fly parasitism has significant impacts on the metabolic ecology of this host species.

Stress-induced rise in body temperature is repeatable in free-ranging Eastern chipmunks (Tamias striatus)

In response to handling or other acute stressors, most mammals, including humans, experience a temporary rise in body temperature (T b). Although this stress-induced rise in T b has been extensively studied on model organisms under controlled environments, individual variation in this interesting phenomenon has not been examined in the field. We investigated the stress-induced rise in T b in free-ranging eastern chipmunks (Tamias striatus) to determine first if it is repeatable. We predicted that the stress-induced rise in T b should be positively correlated to factors affecting heat production and heat dissipation, including ambient temperature (T a), body mass (M b), and field metabolic rate (FMR). Over two summers, we recorded both T b within the first minute of handling time (T b1) and after 5 min of handling time (T b5) 294 times on 140 individuals. The mean ∆T b (T b5 – T b1) during this short interval was 0.30 ± 0.02°C, confirming that the stress-induced rise in T b occurs in chipmunks. Consistent differences among individuals accounted for 40% of the total variation in ∆T b (i.e. the stress-induced rise in T b is significantly repeatable). We also found that the stress-induced rise in T b was positively correlated to T a, M b, and mass-adjusted FMR. These results confirm that individuals consistently differ in their expression of the stress-induced rise in T b and that the extent of its expression is affected by factors related to heat production and dissipation. We highlight some research constraints and opportunities related to the integration of this laboratory paradigm into physiological and evolutionary ecology.

Context-dependent correlation between resting metabolic rate and daily energy expenditure in wild chipmunks

Several empirical studies have shown that variation in daily energy expenditure (DEE) and resting metabolic rate (RMR) is influenced by environmental and individual factors, but whether these shared influences are responsible for, or independent of, relationships between DEE and RMR remains unknown. The objectives of this study were to (i) simultaneously evaluate the effects of environmental and individual variables on DEE and RMR in free-ranging eastern chipmunks (Tamias striatus) and (ii) quantify the correlation between DEE and RMR before and after controlling for common sources of variation. We found that the influence of individual factors on DEE and RMR is most often shared, whereas the influence of environmental factors tends to be distinct. Both raw and mass-adjusted DEE and RMR were significantly correlated, but this correlation vanished after accounting for the shared effect of reproduction on both traits. However, within reproductive individuals, DEE and RMR remained positively correlated after accounting for all other significant covariates. The ratio of DEE to RMR was significantly higher during reproduction than at other times of the year and was negatively correlated with ambient temperature. DEE and RMR appear to be inherently correlated during reproduction, but this correlation does not persist during other, less energy-demanding periods of the annual cycle.

The energetic and survival costs of growth in free-ranging chipmunks

The growth/survival trade-off is a fundamental aspect of life-history evolution that is often explained by the direct energetic requirement for growth that cannot be allocated into maintenance. However, there is currently no empirical consensus on whether fast-growing individuals have higher resting metabolic rates at thermoneutrality (RMRt) than slow growers. Moreover, the link between growth rate and daily energy expenditure (DEE) has never been tested in a wild endotherm. We assessed the energetic and survival costs of growth in juvenile eastern chipmunks (Tamias striatus) during a year of low food abundance by quantifying post-emergent growth rate (n = 88), RMRt (n = 66), DEE (n = 20), and overwinter survival. Both RMRt and DEE were significantly and positively related to growth rate. The effect size was stronger for DEE than RMRt, suggesting that the energy cost of growth in wild animals is more likely to be related to the maintenance of a higher foraging rate (included in DEE) than to tissue accretion (included in RMRt). Fast growers were significantly less likely to survive the following winter compared to slow growers. Juveniles with high or low RMRt were less likely to survive winter than juveniles with intermediate RMRt. In contrast, DEE was unrelated to survival. In addition, botfly parasitism simultaneously decreased growth rate and survival, suggesting that the energetic budget of juveniles was restricted by the simultaneous costs of growth and parasitism. Although the biology of the species (seed-storing hibernator) and the context of our study (constraining environmental conditions) were ideally combined to reveal a direct relationship between current use of energy and future availability, it remains unclear whether the energetic cost of growth was directly responsible for reduced survival.

The energetic and oxidative costs of reproduction in a free-ranging rodent

1. As understanding of the energetic costs of reproduction in birds and mammals continues to improve, oxidative stress is an increasingly cited example of a non-energetic cost of reproduction that may serve as a proximal physiological link underlying life-history trade-offs.

2. Here, we provide the first study to measure daily energy expenditure (DEE) and oxidative damage in a wild population. We measured both traits on eastern chipmunks (Tamias striatus) and assessed their relationships with age, reproductive status, litter size and environmental conditions.

3. We found that both physiological traits were correlated with environmental characteristics (e.g. temperature, seasons). DEE tended to increase with decreasing temperature, while oxidative damage was lower in spring, after a winter of torpor expression, than in autumn. We also found that DEE decreased with age, while oxidative damage was elevated in young individuals, reduced in animals of intermediate age and tended to increase at older age.

4. After controlling for age and environmental variables, we found that both female DEE and oxidative damage increased with litter size, although the latter increased weakly.

5. Our results corroborate findings from laboratory studies but highlight the importance of considering environmental conditions, age and reproductive status in broader analyses of the causes and consequences of physiological costs of reproduction in wild animals.

Energetic cost of bot fly parasitism in free-ranging eastern chipmunks

The energy and nutrient demands of parasites on their hosts are frequently invoked as an explanation for negative impacts of parasitism on host survival and reproductive success. Although cuterebrid bot flies are among the physically largest and most-studied insect parasites of mammals, the only study conducted on metabolic consequences of bot fly parasitism revealed a surprisingly small effect of bot flies on host metabolism. Here we test the prediction that bot fly parasitism increases the resting metabolic rate (RMR) of free-ranging eastern chipmunks (Tamias striatus), particularly in juveniles who have not previously encountered parasites and have to allocate energy to growth. We found no effect of bot fly parasitism on adults. In juveniles, however, we found that RMR strongly increased with the number of bot fly larvae hosted. For a subset of 12 juveniles during a year where parasite prevalence was particularly high, we also compared the RMR before versus during the peak of bot fly prevalence, allowing each individual to act as its own control. Each bot fly larva resulted in a ~7.6% increase in the RMR of its host while reducing juvenile growth rates. Finally, bot fly parasitism at the juvenile stage was positively correlated with adult stage RMR, suggesting persistent effects of bot flies on RMR. This study is the first to show an important effect of bot fly parasitism on the metabolism and growth of a wild mammal. Our work highlights the importance of studying cost of parasitism over multiple years in natural settings, as negative effects on hosts are more likely to emerge in periods of high energetic demand (e.g. growing juveniles) and/or in harsh environmental conditions (e.g. low food availability).

Individual (co)variation in standard metabolic rate, feeding rate, and exploratory behavior in wild-caught semiaquatic salamanders

Repeatability is an important concept in evolutionary analyses because it provides information regarding the benefit of repeated measurements and, in most cases, a putative upper limit to heritability estimates. Repeatability (R) of different aspects of energy metabolism and behavior has been demonstrated in a variety of organisms over short and long time intervals. Recent research suggests that consistent individual differences in behavior and energy metabolism might covary. Here we present new data on the repeatability of body mass, standard metabolic rate (SMR), voluntary exploratory behavior, and feeding rate in a semiaquatic salamander and ask whether individual variation in behavioral traits is correlated with individual variation in metabolism on a whole-animal basis and after conditioning on body mass. All measured traits were repeatable, but the repeatability estimates ranged from very high for body mass (R = 0.98), to intermediate for SMR (R = 0.39) and food intake (R = 0.58), to low for exploratory behavior (R = 0.25). Moreover, repeatability estimates for all traits except body mass declined over time (i.e., from 3 to 9 wk), although this pattern could be a consequence of the relatively low sample size used in this study. Despite significant repeatability in all traits, we find little evidence that behaviors are correlated with SMR at the phenotypic and among-individual levels when conditioned on body mass. Specifically, the phenotypic correlations between SMR and exploratory behavior were negative in all trials but significantly so in one trial only. Salamanders in this study showed individual variation in how their exploratory behavior changed across trials (but not body mass, SMR, and feed intake), which might have contributed to observed changing correlations across trials.

Energy expenditure and personality in wild chipmunks

© 2015, Springer-Verlag Berlin Heidelberg. According to the “pace-of-life syndrome” concept, slow-fast life-history strategies favored under different ecological conditions should lead to co-adaptations between metabolic rate and personality traits such as activity, exploration, and boldness. Although the relationships between resting metabolic rate (RMR) and personality traits have been recently tested several times, we still do not know whether personality is related to the daily energy expenditure (DEE) of free-living individuals in their natural habitat. The objectives of this study were to assess the links between RMR, DEE, and two personality traits (exploration in an open-field and docility during handling) in wild eastern chipmunks (Tamias striatus). Using a multivariate mixed model, we found that exploration and docility were significantly correlated at the among-individual level, confirming the presence of a behavioral syndrome within our population. We also found that exploration, but not docility, was negatively correlated with DEE. Hence, fast explorers show lower DEE levels than slow explorers, independently of RMR and docility. This result adds to an increasingly large (and complex) literature reporting the impacts of personality traits on the biology, ecology, and physiology of animals in their natural environment.