Paulina A. Szafrańska

Trade-offs between activity and thermoregulation in a small carnivore, the least weasel Mustela nivalis

We studied factors influencing daily energy expenditures (DEE) of male least weasels (Mustela nivalis) using the doubly labelled water technique. The relationship between ambient temperature and DEE formed a triangular pattern, characterized by invariance of the maximum DEE and an inverse relationship between minimum DEE and temperature. A simple energetic model relating the DEE of male weasels to activity time (AT) and ambient temperature predicted that, across seasons, less than 10 per cent of measurements approach the upper bound of observed DEE. Male weasels were able to maintain a relatively constant maximum energy output across varying temperatures by adjusting their AT to changes in temperature. They achieved maximum energy expenditures in winter due to high thermoregulatory costs, and in spring and summer due to high levels of physical activity. This pattern exemplifies a ‘metabolic niche’ of a small mammal having extremely high energy expenditures primarily driven by ambient temperature.

Phylogenetic analysis of mammalian maximal oxygen consumption during exercise

SUMMARY We compiled published values of mammalian maximum oxygen consumption during exercise () and supplemented these data with new measurements of for the largest rodent (capybara), 20 species of smaller-bodied rodents, two species of weasels and one small marsupial. Many of the new data were obtained with running-wheel respirometers instead of the treadmill systems used in most previous measurements of mammalian . We used both conventional and phylogenetically informed allometric regression models to analyze of 77 ‘species’ (including subspecies or separate populations within species) in relation to body size, phylogeny, diet and measurement method. Both body mass and allometrically mass-corrected showed highly significant phylogenetic signals (i.e. related species tended to resemble each other). The Akaike information criterion corrected for sample size was used to compare 27 candidate models predicting (all of which included body mass). In addition to mass, the two best-fitting models (cumulative Akaike weight=0.93) included dummy variables coding for three species previously shown to have high (pronghorn, horse and a bat), and incorporated a transformation of the phylogenetic branch lengths under an Ornstein–Uhlenbeck model of residual variation (thus indicating phylogenetic signal in the residuals). We found no statistical difference between wheel- and treadmill-elicited values, and diet had no predictive ability for . Averaged across all models, the allometric scaling exponent was 0.839, with 95% confidence limits of 0.795 and 0.883, which does not provide support for a scaling exponent of 0.67, 0.75 or unity.

Plant–herbivore interactions: silicon concentration in tussock sedges and population dynamics of root voles

Summary It has been hypothesized that the induction of silicon (Si)-based plant defence in response to herbivore damage may engender rodent population cycles. Many studies have also considered accumulation of Si as a process controlled by geo-hydrological factors. To test these ideas, we investigated the relationship between concentration of Si in fibrous tussock sedge (Carex appropinquata) and the population density of a major sedge consumer, the root vole (Microtus oeconomus), in field enclosures in natural habitat under a variety of natural water regimes and weather conditions. We found that a high density of voles at the end of summer resulted in the immediate accumulation of Si by rhizomes, followed by accumulation of Si in leaves with a 1-year lag time. The level of river flooding in the same year had an additional impact on Si concentration in rhizomes but did not affect silicification of leaves. Overwinter changes in concentration of Si in sedges were influenced by fluctuations in ambient temperature and the depth of snow cover (multiple freeze–thaw cycles), thus affecting the quality of winter food available for voles. Smaller voles had lower mortality during early winter than large voles, which seemed to be connected with changes in the quality of the autumn rather than the winter food base. Winter survival of voles was not associated with Si concentration in their faeces, however. Our results suggest that changes in Si concentration in fibrous tussock sedge can be induced by changes in vole population density and are also additionally affected by the amount of flooding and weather conditions.

Effect of energetic constraints on distribution and winter survival of weasel males.

1. The absolute energy needs of small animals are generally lower than those of larger animals. This should drive higher mortality of larger animals, when the environmental conditions deteriorate. However, demonstration of the effect of energy constraints on survivals proved difficult, because the range of body mass within species is generally too small to produce enough variation for studying such an effect. An opportunity for an intraspecific study comes from weasels inhabiting the Białowieża Forest (north-eastern Poland), which are characterized by a threefold variation in body mass. 2. We assumed that in summer larger weasel males are favoured by sexual selection, because they are more successful when competing for mates. We then tested whether they suffer higher mortality in winter, because they have difficulty finding sufficient food to satisfy their energy needs and/or because the additional foraging time would result in increased exposure to predation. 3. We measured daily energy expenditures (DEE) of overwintering weasel males using the doubly labelled water (DLW) technique. We constructed an energetic model predicting how individuals of different size are able to balance their energy budgets feeding on large and small prey while minimizing time spent hunting, thereby reducing their own exposure to predation. 4. The range of body mass in overwintering weasels predicted by our model corresponded very well with the distribution of prey body mass in three different habitats within our study area. Larger individuals were able to compensate for higher food requirements by using habitats with larger prey species than those available to smaller male weasels. This effectively offset the expected negative association between body mass and winter survival predicted from considerations of energy balance. 5. Our results show how energetic constraints affect body mass and spatial segregation of a species at the intra-specific level not only across large geographical ranges, but also within a relatively small area.

Silicon-based plant defences, tooth wear and voles

ABSTRACT Plant–herbivore interactions are hypothesized to drive vole population cycles through the grazing-induced production of phytoliths in leaves. Phytoliths act as mechanical defences because they deter herbivory and lower growth rates in mammals. However, how phytoliths impair herbivore performance is still unknown. Here, we tested whether the amount of phytoliths changes tooth wear patterns. If confirmed, abrasion from phytoliths could play a role in population crashes. We applied dental microwear texture analysis (DMTA) to laboratory and wild voles. Lab voles were fed two pelleted diets with differing amounts of silicon, which produced similar dental textures. This was most probably due to the loss of food mechanical properties through pelletization and/or the small difference in silicon concentration between diets. Wild voles were trapped in Poland during spring and summer, and every year across a population cycle. In spring, voles feed on silica-rich monocotyledons, while in the summer they also include silica-depleted dicotyledons. This was reflected in the results; the amount of silica therefore leaves a traceable record in the dental microwear texture of voles. Furthermore, voles from different phases of population cycles have different microwear textures. We tentatively propose that these differences result from grazing-induced phytolith concentrations. We hypothesize that the high amount of phytoliths in response to intense grazing in peak years may result in malocclusion and other dental abnormalities, which would explain how these silicon-based plant defences help provoke population crashes. DMTA could then be used to reconstruct vole population dynamics using teeth from pellets or palaeontological material. Highlighted Article: Increased abrasiveness in the diet of voles, assessed by DMTA, could be caused by high phytolith concentration of plants in response to intense grazing, and could in turn help provoke vole population crashes.

Individual variation in dispersal associated with phenotype influences fine-scale genetic structure in weasels

In general, landscape genetic studies have ignored the potential role that the phenotype of individuals plays in determining fine-scale genetic structure in species. This potential over-simplification ignores an important component that dispersal is both condition- and phenotype-dependent. In order to investigate the relationship between potential dispersal, habitat selection and phenotype, we examined the spatial ecology, body mass and fine-scale genetic structure of weasels (Mustela nivalis) in Białowieża Forest in Poland. Our study population is characterized by an almost three-fold phenotypic variation in adult body mass and weasels were segregated in certain habitats according to size. We detected significant genetic structuring associated with habitat within the studied area and analyses of radio-tracking and re-capture data showed that the maximum extent of movement was achieved by weasels of medium body size, whereas the smallest and largest individuals exhibited higher site fidelity. With the unrestricted movement of the medium-sized individuals across optimal habitat, genetic admixture does occur. However, the presence of a barrier leads to unidirectional gene flow, with larger individuals outcompeting smaller individuals and therefore maintaining the genetic break in the study area. This highlights the importance of considering both intrinsic (phenotype) and extrinsic (environmental) factors in understanding dispersal patterns and ultimately, gene flow in complex landscapes.

Effect of the abrasive properties of sedges on the intestinal absorptive surface and resting metabolic rate of root voles.

Recent studies on grasses and sedges suggest that the induction of a mechanism reducing digestibility of plant tissues in response to herbivore damage may drive rodent population cycles. This defence mechanism seems to rely on the abrasive properties of ingested plants. However, the underlying mechanism has not been demonstrated in small wild herbivores. Therefore, we carried out an experiment in which we determined the joint effect of abrasive sedge components on the histological structure of small intestine as well as resting metabolic rate (RMR) of the root vole (Microtus oeconomus). Histological examination revealed that voles fed with a sedge-dominated diet had shorter villi composed from narrower enterocytes in duodenum, jejunum and ileum. Reduction in the height of villi decreased along the small intestine. Activity of the mucus secretion increased along the small intestine and was significantly higher in the ileum. The intestinal abrasion exceeded the compensatory capabilities of voles, which responded to a sedge-dominated diet by a reduction of body mass and a concomitant decrease in whole body RMR. These results explain the inverse association between body mass and the probability of winter survival observed in voles inhabiting homogenous sedge wetlands.

The energy cost of voluntary running in the weasel Mustela nivalis

SUMMARY The small size and elongate shape of weasels (Mustela nivalis) probably evolved to facilitate movement within the burrow systems of prey species, but result in high energy costs of thermoregulation. In this study we measured metabolic rates of weasels during voluntary locomotion to determine whether energy costs of transport are also high in these unusually shaped mammals. In addition, we measured the lower and upper limits of aerobic metabolism [resting metabolic rate (RMR) and maximal oxygen consumption in forced exercise (V̇O2,max)], and used the wide size range of adult weasels to investigate the intraspecific scaling of energy metabolism. Finally, we combined measurements of energy use during running with radiotracking and doubly labeled water data from free-living weasels to estimate the importance of locomotor costs in daily energy budgets. We found that weasels have higher than predicted costs of running, largely because of an elevated intercept of the speed versus metabolic rate relationship. Running costs were strongly affected by the approximately fourfold range of body size in adults. As reported in other studies, the RMR of weasels was considerably higher than predicted from body mass. Maximal oxygen consumption was also higher than predicted, but factorial aerobic scope (V̇O2,max/RMR) was within the normal range for mammals. Intraspecific mass scaling of RMR and V̇O2,max did not differ from typical interspecific mammalian allometries. In wild weasels, locomotor costs comprised roughly 5% of daily energy expenditures; this low value was primarily a result of short travel times and distances.

Male Weasels Decrease Activity and Energy Expenditure in Response to High Ambient Temperatures

The heat dissipation limit (HDL) hypothesis suggests that the capacity of endotherms to dissipate body heat may impose constraints on their energy expenditure. Specifically, this hypothesis predicts that endotherms should avoid the detrimental consequences of hyperthermia by lowering their energy expenditure and reducing their activity in response to high ambient temperatures (Ta). We used an extensive data set on the daily energy expenditure (DEE, n = 27) and the daily activity time (AT, n = 48) of male weasels (Mustela nivalis) during the spring and summer breeding season to test these predictions. We found that Ta was related in a “hump-shaped” (i.e. convex) manner to AT, DEE, resting metabolic rate (RMR) and metabolic scope (the ratio of DEE to RMR). These results support the HDL hypothesis because in response to warm Tas male weasels reduced their AT, DEE, and RMR. Although the activity and energy expenditure of large endotherms are most likely to be constrained in response to warm Tas because they are less able to dissipate heat, our results suggest that small endotherms may also experience constraints consistent with the HDL hypothesis.

Seasonal Variation of Resting Metabolic Rate and Body Mass in Free-Living Weasels Mustela nivalis

Metabolic rates and body mass of mammals vary seasonally along with ambient temperatures and food availability. At the population level, seasonal changes in metabolic rate and mass can be due to selective mortality or emigration of individuals whose metabolic rate or mass differs from the average for the population. Alternatively, the metabolic rates of individuals can change seasonally, such that the population average increases or decreases due to shifts in the physiology of the overall population. The latter implies that individuals respond in a similar manner to changing seasonal conditions. We studied seasonal changes in body mass (BM) and resting metabolic rate (RMR) in free-ranging male weasels (Mustela nivalis) to test the consistency of these traits in individuals caught in different seasons of the year. At the population level, BM was remarkably stable across the seasons (, ). In contrast, BM- corrected RMR varied significantly between seasons and was the lowest in winter (, ). We demonstrated that individual weasels were consistent in how their BM and RMR deviated from the seasonal means for the population (intraclass correlation, and 0.33, respectively). This variation among individuals explained ∼76% and 27% of the total variation of BM and basal metabolic rate, respectively. Hence, the relatively constant BM at the population level across seasons is due to a relative constancy of BM in individuals. Our study is one of relatively few research projects that demonstrate that seasonal changes in RMR observed in the wild population are in part due to a consistency in individual responses to changing environmental conditions.