Limits to sustained energy intake. XXXIV. Can the heat dissipation limit (HDL) theory explain reproductive aging?

According to the heat dissipation limit (HDL) theory, reproductive performance is limited by the capacity to dissipate excess heat. We tested the novel hypotheses that (1) the age-related decline in reproductive performance is due to an age-related decrease of heat dissipation capacity and (2) the limiting mechanism is more severe in animals with high metabolic rates. We used bank voles (Myodes glareolus) from lines selected for high swim-induced aerobic metabolic rate, which have also increased basal metabolic rate, and unselected control lines. Adult females from three age classes - young (4 months), middle-aged (9 months) and old (16 months) - were maintained at room temperature (20°C), and half of the lactating females were shaved to increase heat dissipation capacity. Old females from both selection lines had a decreased litter size, mass and growth rate. The peak-lactation average daily metabolic rate was higher in shaved than in unshaved mothers, and this difference was more profound among old than young and middle-aged voles (P=0.02). In females with large litters, milk production tended to be higher in shaved (least squares mean, LSM±s.e.: 73.0±4.74 kJ day-1) than in unshaved voles (61.8±4.78 kJ day-1; P=0.05), but there was no significan"t effect of fur removal on the growth rate [4.47±2.29 g (4 days-1); P=0.45]. The results provide mixed support of the HDL theory and no support for the hypotheses linking the differences in reproductive aging with either a deterioration in thermoregulatory capability or genetically based differences in metabolic rate.

Artificial selection for predatory behaviour results in dietary niche differentiation in an omnivorous mammal.

The diet of an individual is a result of the availability of dietary items and the individual's foraging skills and preferences. Behavioural differences may thus influence diet variation, but the evolvability of diet choice through behavioural evolution has not been studied. We used experimental evolution combined with a field enclosure experiment to test whether behavioural selection leads to dietary divergence. We analysed the individual dietary niche via stable isotope ratios of nitrogen (δ15N) and carbon (δ13C) in the hair of an omnivorous mammal, the bank vole, from four lines selected for predatory behaviour and four unselected control lines. Predatory voles had higher hair δ15N values than control voles, supporting our hypothesis that predatory voles would consume a higher trophic level diet (more animal versus plant foods). This difference was significant in the early but not the late summer season. The δ13C values also indicated a seasonal change in the consumed plant matter and a difference in food sources among selection lines in the early summer. These results imply that environmental factors interact with evolved behavioural tendencies to determine dietary niche heterogeneity. Behavioural selection thus has potential to contribute to the evolution of diet choice and ultimately the species' ecological niche breadth.

Does selection for behavioral and physiological performance traits alter glucocorticoid responsiveness in bank voles?

One of the key elements of an animal's Darwinian fitness is its ability to adequately respond to and cope with challenging situations. Glucocorticoid hormones, such as corticosterone, affect an organism's ability to overcome such challenges. We hypothesized that changes in the glucocorticoid response curve contribute to the evolution of increased performance during challenging conditions, and tested it on bank voles (Myodes glareolus) from a multidirectional artificial selection experiment, which involves lines selected for high aerobic exercise metabolism achieved during swimming (A - Aerobic), predatory behavior towards a cricket (P - Predatory) and ability to maintain body mass on a low-quality herbivorous diet (H - Herbivorous), as well as unselected control lines (C - Control). We elicited a glucocorticoid response either by restraining the animal or by maximum pharmacological stimulation, and measured plasma corticosterone levels at baseline, during the response and during the recovery phase. Response-level corticosterone was higher in females, and recovery from maximal level was faster than that of males. Selection did not affect baseline or stress-induced corticosterone levels, but it decreased the maximum corticosterone level in Aerobic and Predatory lines, reducing the difference between stress-induced and maximum levels. Recovery from restraint-induced corticosterone level tended to be slower in the Herbivorous than in the other lines, an effect that was stronger in females than in males. In conclusion, successful selection for increased performance in challenging conditions was not associated with changes in absolute values of the glucocorticoid response to stress, but can affect other characteristics of the glucocorticoid response curve.

The metabolic performance predicts home range size of bank voles: a support for the behavioral-bioenergetics theory.

The pace-of-life syndrome describes covariation between life-history, behavioral and physiological traits; while, the emerging behavioral-bioenergetics theory proposes mechanistic links between those traits in a spatial-ecological context. However, little is known about the association between the limits to metabolic rate and spatial performance (i.e., mobility, home range size) in free-living individuals. Here we show, for the first time at the intra-specific level, that mobility traits increased with the aerobic exercise capacity ([Formula: see text]O2max) in a wild rodent, the bank vole (Myodes glareolus): [Formula: see text]O2max affected directly the movement intensity, which in turn affected home ranges. The results show that evolution of high [Formula: see text]O2max could be driven by selection for spatial performance traits, and corroborate one of the key assumptions of the behavioral-bioenergetics theory. However, the minimum maintenance metabolism, measured as the basal metabolic rate (BMR), was not correlated with movement intensity, and the direction of the BMR-home range correlation tended to change with age of the voles. The latter result indicates that testing the theory will be particularly challenging.

Stress coping and evolution of aerobic exercise performance: corticosterone levels in voles from a selection experiment.

The locomotor performance achieved in a challenging situation depends not only on physiological limitations, such as the aerobic exercise capacity, but also on behavioral characteristics, such as adequate coping with stress. The stress response is mediated largely by the hypothalamic-pituitary-adrenal (HPA) axis, through modulated release of glucocorticoids. We used a unique experimental evolution model system to test the hypothesis that the evolution of an increased aerobic exercise performance can be facilitated by modification of the glucocorticoid-related stress-coping mechanisms. Bank voles (Myodes glareolus) from 'aerobic' (A) lines, selected for 22 generations for high maximum swim-induced rate of oxygen consumption (V̇O2,swim), achieved a 64% higher V̇O2,swim than those from unselected, control lines. The temporal pattern of exercise during the swimming trial also evolved, and the A-line voles achieved V̇O2,swim later in the course of the trial, which indicates a modification of the stress response characteristics. Both V̇O2,swim and the average metabolic rate measured during the trial tended to increase with baseline corticosterone level, and decreased with the post-exercise corticosterone level. Thus, increased baseline corticosterone level promotes high metabolic performance, but a high corticosterone response to swimming acts as an inhibitor rather than stimulator of intense activity. However, neither of the corticosterone traits differed between the A-selected and control lines. Thus, the experiment did not provide evidence that evolution of increased aerobic performance is facilitated by the modification of glucocorticoid levels. The results, however, do not exclude the possibility that other aspects of the HPA axis function evolved in response to the selection.

Experimental evolution of aerobic exercise performance and hematological traits in bank voles.

The maximum rate of aerobic exercise metabolism (VO2max) is a trait informative from both medical and evolutionary perspective, and both the physiological mechanisms limiting its level and its evolution are subject to vivid debate. Both comparative analyses and studies on the effects of training or acclimation to aerobically-demanding conditions suggest a role of oxygen transport-related properties of blood in limiting VO2max. Here we used a unique experimental evolution model - lines of bank voles selected for high rate of swim-induced aerobic metabolism (VO2swim; A lines), which evolved a 60% higher VO2swim than that observed in unselected control lines (C) - and asked how the hematological parameters evolved in response to the selection. Voles from the A lines had a decreased hemoglobin concentration in cardiac blood samples (adjusted means ±â€¯SE, A: 14.7 ±â€¯1.1, C: 15.3 ±â€¯1.1 g/dl; p = .008), hematocrit (A: 51.7 ±â€¯4.5, C: 53.8 ±â€¯4.2%; p = .042) and tended to have less erythrocytes per microliter of blood (A: 11.5 ±â€¯1.4, C: 12.7 ±â€¯1.3 mln/µl; p = .083). The effect of selection was more pronounced in males than in females. Thus, selection for high aerobic-exercise performance resulted in a paradoxical decrease in traits positively associated with oxygen-carrying capacity per unit of blood volume, and the effect was sex-dependent. However, as a decreased blood viscosity associated with the lowered hematocrit reduces the costs of blood circulation, it can be hypothesized that the change can actually boost the oxygen supply to peripheral tissues.

Genomic Response to Selection for Predatory Behavior in a Mammalian Model of Adaptive Radiation.

If genetic architectures of various quantitative traits are similar, as studies on model organisms suggest, comparable selection pressures should produce similar molecular patterns for various traits. To test this prediction, we used a laboratory model of vertebrate adaptive radiation to investigate the genetic basis of the response to selection for predatory behavior and compare it with evolution of aerobic capacity reported in an earlier work. After 13 generations of selection, the proportion of bank voles (Myodes [=Clethrionomys] glareolus) showing predatory behavior was five times higher in selected lines than in controls. We analyzed the hippocampus and liver transcriptomes and found repeatable changes in allele frequencies and gene expression. Genes with the largest differences between predatory and control lines are associated with hunger, aggression, biological rhythms, and functioning of the nervous system. Evolution of predatory behavior could be meaningfully compared with evolution of high aerobic capacity, because the experiments and analyses were performed in the same methodological framework. The number of genes that changed expression was much smaller in predatory lines, and allele frequencies changed repeatably in predatory but not in aerobic lines. This suggests that more variants of smaller effects underlie variation in aerobic performance, whereas fewer variants of larger effects underlie variation in predatory behavior. Our results thus contradict the view that comparable selection pressures for different quantitative traits produce similar molecular patterns. Therefore, to gain knowledge about molecular-level response to selection for complex traits, we need to investigate not only multiple replicate populations but also multiple quantitative traits.

A highly divergent Puumala virus lineage in southern Poland.

Puumala virus (PUUV) represents one of the most important hantaviruses in Central Europe. Phylogenetic analyses of PUUV strains indicate a strong genetic structuring of this hantavirus. Recently, PUUV sequences were identified in the natural reservoir, the bank vole (Myodes glareolus), collected in the northern part of Poland. The objective of this study was to evaluate the presence of PUUV in bank voles from southern Poland. A total of 72 bank voles were trapped in 2009 at six sites in this part of Poland. RT-PCR and IgG-ELISA analyses detected three PUUV positive voles at one trapping site. The PUUV-infected animals were identified by cytochrome b gene analysis to belong to the Carpathian and Eastern evolutionary lineages of bank vole. The novel PUUV S, M and L segment nucleotide sequences showed the closest similarity to sequences of the Russian PUUV lineage from Latvia, but were highly divergent to those previously found in northern Poland, Slovakia and Austria. In conclusion, the detection of a highly divergent PUUV lineage in southern Poland indicates the necessity of further bank vole monitoring in this region allowing rational public health measures to prevent human infections.

Initial Molecular-Level Response to Artificial Selection for Increased Aerobic Metabolism Occurs Primarily through Changes in Gene Expression.

Experimental evolution combined with genome or transcriptome resequencing (Evolve and Resequence) represents a promising approach for advancing our understanding of the genetic basis of adaptation. Here, we applied this strategy to investigate the effect of selection on a complex trait in lines derived from a natural population of a small mammal. We analyzed the liver and heart transcriptomes of bank voles (Myodes [=Clethrionomys] glareolus) that had been selected for increased aerobic metabolism. The organs were sampled from 13th generation voles; at that point, the voles from four replicate selected lines had 48% higher maximum rates of oxygen consumption than those from four control lines. At the molecular level, the response to selection was primarily observed in gene expression: Over 300 genes were found to be differentially expressed between the selected and control lines and the transcriptome-wide pattern of expression distinguished selected lines from controls. No evidence for selection-driven changes of allele frequencies at coding sites was found: No single nucleotide polymorphism (SNP) changed frequency more than expected under drift alone and frequency changes aggregated over all SNPs did not separate selected and control lines. Nevertheless, among genes which showed highest differentiation in allele frequencies between selected and control lines we identified, using information about gene functions and the biology of the selected phenotype, plausible targets of selection; these genes, together with those identified in expression analysis, have been prioritized for further studies. Because our selection lines were derived from a natural population, the amount and the spectrum of variation available for selection probably closely approximated that typically found in populations of small mammals. Therefore, our results are relevant to the understanding of the molecular basis of complex adaptations occurring in natural vertebrate populations.

Hindlimb muscle fibre size and glycogen stores in bank voles with increased aerobic exercise metabolism.

To test hypotheses concerning physiological factors limiting the rate of aerobic exercise metabolism, we used a unique experimental evolution model: lines of bank voles selected for high swim-induced aerobic metabolism (A) and unselected, control lines (C). We investigated putative adaptations that result in the increased performance of the hindlimb muscle (gastrocnemius joined with plantaris). The body mass-adjusted muscle mass was higher in A-lines (0.093 g) than in C-lines (0.083 g; P=0.01). However, selection did not affect mean muscle fibre cross-sectional area (P=0.34) or glycogen content assessed with a histochemical periodic acid-Schiff reaction (PAS; P=0.82). The results suggest that the increased aerobic performance is achieved by an increase of total muscle mass, without major qualitative changes in the muscle fibre architecture. However, such a conclusion should be treated with caution, because other modifications, such as increased density of capillaries or mitochondria, could occur.

Limits to sustained energy intake. XXIII. Does heat dissipation capacity limit the energy budget of lactating bank voles?

Understanding factors limiting sustained metabolic rate (SusMR) is a central issue in ecological physiology. According to the heat dissipation limit (HDL) theory, the SusMR at peak lactation is constrained by the maternal capacity to dissipate body heat. To test that theory, we shaved lactating bank voles (Myodes glareolus) to experimentally elevate their capacity for heat dissipation. The voles were sampled from lines selected for high aerobic exercise metabolism (A; characterized also by increased basal metabolic rate) and unselected control lines (C). Fur removal significantly increased the peak-lactation food intake (mass-adjusted least square means ± s.e.; shaved: 16.3 ± 0.3 g day(-1), unshaved: 14.4 ± 0.2 g day(-1); P<0.0001), average daily metabolic rate (shaved: 109 ± 2 kJ day(-1), unshaved: 97 ± 2 kJ day(-1); P<0.0001) and metabolisable energy intake (shaved: 215 ± 4 kJ day(-1), unshaved: 185 ± 4 kJ day(-1); P<0.0001), as well as the milk energy output (shaved: 104 ± 4 kJ day(-1); unshaved: 93 ± 4 kJ day(-1); P=0.021) and litter growth rate (shaved: 9.4 ± 0.7 g 4 days(-1), unshaved: 7.7 ± 0.7 g 4 days(-1); P=0.028). Thus, fur removal increased both the total energy budget and reproductive output at the most demanding period of lactation, which supports the HDL theory. However, digestive efficiency was lower in shaved voles (76.0 ± 0.3%) than in unshaved ones (78.5 ± 0.2%; P<0.0001), which may indicate that a limit imposed by the capacity of the alimentary system was also approached. Shaving similarly affected the metabolic and reproductive traits in voles from the A and C lines. Thus, the experimental evolution model did not reveal a difference in the limiting mechanism between animals with inherently different metabolic rates.

Evolution of basal metabolic rate in bank voles from a multidirectional selection experiment.

A major theme in evolutionary and ecological physiology of terrestrial vertebrates encompasses the factors underlying the evolution of endothermy in birds and mammals and interspecific variation of basal metabolic rate (BMR). Here, we applied the experimental evolution approach and compared BMR in lines of a wild rodent, the bank vole (Myodes glareolus), selected for 11 generations for: high swim-induced aerobic metabolism (A), ability to maintain body mass on a low-quality herbivorous diet (H) and intensity of predatory behaviour towards crickets (P). Four replicate lines were maintained for each of the selection directions and an unselected control (C). In comparison to C lines, A lines achieved a 49% higher maximum rate of oxygen consumption during swimming, H lines lost 1.3 g less mass in the test with low-quality diet and P lines attacked crickets five times more frequently. BMR was significantly higher in A lines than in C or H lines (60.8, 56.6 and 54.4 ml O2 h(-1), respectively), and the values were intermediate in P lines (59.0 ml O2 h(-1)). Results of the selection experiment provide support for the hypothesis of a positive association between BMR and aerobic exercise performance, but not for the association of adaptation to herbivorous diet with either a high or low BMR.

Reproduction is not costly in terms of oxidative stress.

One of the core assumptions of life-history theory is the negative trade-off between current and future reproduction. Investment in current reproduction is expected to decrease future reproductive success or survival, but the physiological mechanisms underlying these costs are still obscure. To test for a role of oxidative stress, we measured oxidative damage to lipids and proteins in liver, heart, kidneys and muscles, as well as the level of antioxidants (total glutathione and catalase), in breeding and non-breeding bank voles. We used females from lines selected for high aerobic metabolism and non-selected control lines and manipulated their reproductive investment by decreasing or increasing litter size. Unlike in most previous studies, the females reared four consecutive litters (the maximum possible during a breeding season). Contrary to predictions, oxidative damage in reproducing females was decreased or not changed, and did not differ between the selected and control lines. Oxidative damage to lipids and proteins in the liver was lower in females that weaned enlarged litters than in non-breeding ones, and was intermediate in those with reduced litters. Oxidative damage to proteins in the heart also tended to be lower in breeding females than in non-breeding ones. A negative relationship between the level of oxidative damage and activity of catalase in kidneys indicated a protective action of antioxidants. In conclusion, our study falsified the hypothesis that oxidative stress is a part of the proximate physiological mechanism underlying the fundamental life-history trade-off between current and future reproduction.

Selection for high activity-related aerobic metabolism does not alter the capacity of non-shivering thermogenesis in bank voles.

An intriguing question is how the capacity of non-shivering thermogenesis (NST)-a special mechanism supporting endothermic thermoregulation in mammals-is affected by selection for high exercise metabolism. It has been proposed that high NST could be a mechanism to compensate for a low basal production of heat. On the other hand, high basal or activity metabolism is associated with physiological characteristics such as high performance of the circulatory system, which are also required for achieving a high NST. Here we tested whether selection for high aerobic exercise performance, which correlates with an increased basal metabolic rate, led to a correlated evolution of maximum and facultative NST. Therefore, we measured the NST of bank voles, Myodes (= Clethrionomys) glareolus, from lines selected for 13-14 generations (n=46) for high aerobic metabolism achieved during swimming and from unselected, control lines (n=46). Open-flow respirometry was used to measure the rate of oxygen consumption (V(·)O2) in anesthetized bank voles injected with noradrenaline (NA). After adjusting for body mass, maximum NST (maximum V(·)O2 recorded after injection of NA) did not differ between the selected (2.38±0.08 mLO2min(-1)) and control lines (2.36±0.08 mLO2min(-1); P=0.891). Facultative NST (= maximum NST minus resting metabolic rate of anesthetized animals) did not differ between the selected (1.49±0.07 mLO2min(-1)) and control lines (1.50±0.07 mLO2min(-1); P=0.985), either. Therefore, our results suggest that NST capacity is not strongly linked to maximum activity-related aerobic metabolic rate.

Genetic variation in bank vole populations in natural and metal-contaminated areas.

The effects of isolation and heavy-metal pollution on genetic diversity in Myodes (=Clethrionomys) glareolus populations were studied. Isolation and pollution are considered to have important effects on biodiversity. Animals were collected from ten populations in isolated (island), mainland, and metal-polluted areas. Three populations were in areas near zinc and lead smelters; four were on islands in the relatively unpolluted Mazurian Lake District and in the Bieszczady Mountains; and three were in clean-mainland areas in the Mazurian Lake District, the Niepolomice Forest, and the Bieszczady Mountains. Cadmium and lead concentrations in liver and kidney were measured to assess the animals' exposure to metals. The metal concentrations were greater in animals from areas classed as polluted than in animals from the clean-mainland areas and islands. The genetic diversity of each population was analyzed using eight microsatellite markers. The results confirmed that isolation adversely affects genetic diversity in M. glareolus populations (giving low heterozygosity and poor allelic richness), but the effect of metal exposure on genetic diversity was not strong. Of the samples from polluted areas, only the Katowice population, which is exposed to high levels of metal pollution and is also isolated because of human activity, showed genetic variation parameters that were similar to those for the island populations. Nei's genetic distances indicated that the island populations were genetically distant from each other and from the other populations, and there were noticeable inbreeding effects that would have been caused by the isolation of these populations.

Development of hyperglycemia and diabetes in captive Polish bank voles.

Diabetes has been detected in Danish and Swedish bank voles (Myodes glareolus). There are no data, however, concerning the prevalence of diabetes in populations from other geographic regions. We investigated the frequency and physiological effects of glucose metabolism disorders in captive bank voles from Poland. Single measurement of fasting blood glucose concentration performed in the 3-4month old captive-born bank Polish voles without any disease symptoms showed that 8% of individuals (22/284) displayed an impaired fasting glucose (IFG, blood glucose (BG) ≥100mg/dL) and 1% (4/284) showed hyperglycemia (BG ≥126mg/dL) which could suggest diabetes. Next, we analyzed blood glucose in samples taken once a month from an additional cohort of bank voles with (FHD), or without (H), a family history of diabetes. The prevalence of IFG at age six months was 26% (16/62) among bank voles from the H group. In the FHD group the prevalence increased to 49% (43/88), and additional 12% (11/88) became diabetic (DB, BG ≥126mg/dL at two time points). Postnatal stress (three maternal deprivations before weaning) did not affect the risk of developing IFG or DB in H voles, but significantly reduced the frequency of glucose metabolism disorders (IFG and DB combined) in FHD voles. IFG was associated with hyperinsulinemia, but not with other biochemical disturbances. Diabetic animals displayed a progressive malformation and vacuolization of ß-cells in the pancreas, without visible leukocytic infiltrations. In summary, our results indicate that Polish captive bank voles can develop diabetes, which shows features of both type 1 and type 2 diabetes in humans. Risk of diabetes is higher in animal with FHD.

Tropism of Puumala orthohantavirus and Endoparasite Coinfection in the Bank Vole Reservoir.

In Europe, most cases of human hantavirus disease are caused by Puumala orthohantavirus (PUUV) transmitted by bank voles (Clethrionomys glareolus, syn. Myodes glareolus), in which PUUV causes inconspicuous infection. Little is known about tropism and endoparasite coinfections in PUUV-infected reservoir and spillover-infected rodents. Here, we characterized PUUV tropism, pathological changes and endoparasite coinfections. The voles and some non-reservoir rodents were examined histologically, immunohistochemically, by in situ hybridization, indirect IgG enzyme-linked immunosorbent assay and reverse transcription-polymerase chain reaction. PUUV RNA and anti-PUUV antibodies were detected simultaneously in a large proportion of the bank voles, indicating persistent infection. Although PUUV RNA was not detected in non-reservoir rodents, the detection of PUUV-reactive antibodies suggests virus contact. No specific gross and histological findings were detected in the infected bank voles. A broad organ tropism of PUUV was observed: kidney and stomach were most frequently infected. Remarkably, PUUV was detected in cells lacking the typical secretory capacity, which may contribute to the maintenance of virus persistence. PUUV-infected wild bank voles were found to be frequently coinfected with Hepatozoon spp. and Sarcocystis (Frenkelia) spp., possibly causing immune modulation that may influence susceptibility to PUUV infection or vice versa. The results are a prerequisite for a deeper understanding of virus-host interactions in natural hantavirus reservoirs.

Is reproduction costly? No increase of oxidative damage in breeding bank voles.

According to life-history theory, investment in reproduction is associated with costs, which should appear as decreased survival to the next reproduction or lower future reproductive success. It has been suggested that oxidative stress may be the proximate mechanism of these trade-offs. Despite numerous studies of the defense against reactive oxygen species (ROS) during reproduction, very little is known about the damage caused by ROS to the tissues of wild breeding animals. We measured oxidative damage to lipids and proteins in breeding bank vole (Myodes glareolus) females after rearing one and two litters, and in non-breeding females. We used bank voles from lines selected for high maximum aerobic metabolic rates (which also had high resting metabolic rates and food intake) and non-selected control lines. The oxidative damage was determined in heart, kidneys and skeletal muscles by measuring the concentration of thiobarbituric acid-reactive substances, as markers of lipid peroxidation, and carbonyl groups in proteins, as markers of protein oxidation. Surprisingly, we found that the oxidative damage to lipids in kidneys and muscles was actually lower in breeding than in non-breeding voles, and it did not differ between animals from the selected and control lines. Thus, contrary to our predictions, females that bred suffered lower levels of oxidative stress than those that did not reproduce. Elevated production of antioxidant enzymes and the protective role of sex hormones may explain the results. The results of the present study do not support the hypothesis that oxidative damage to tissues is the proximate mechanism of reproduction costs.

Evolution of an increased performance under acute challenge does not exacerbate vulnerability to chronic stress.

An adequate stress response plays a vital role in coping with challenges. However, if selection for improved coping with an acute challenge affects the entire stress response system, susceptibility to adverse effects of chronic stressors can be deepened. Here, we used bank voles from lines selected for high swim-induced aerobic metabolism (A) and unselected control (C), and asked if the selection affected sensitivity to chronic mild stress (CMS). The voles were first habituated to daily weighing and feces collection for three weeks, and then for two weeks were exposed to CMS or remained undisturbed. The habituation itself resulted in an increased swim-induced oxygen consumption in both line types, and a decreased body mass. The CMS treatment caused reduction of food consumption in the second week of the experiment, and, in males, a decline in the metabolic rate. Paradoxically, fecal corticosterone metabolites decreased in the CMS-treated group. The response to CMS did not differ between the line types. Thus, the selection for increased performance was not traded off by increased vulnerability to chronic stress. The counter-intuitive results may even lead to a speculation that bank voles-and perhaps also other animals-prefer experiencing unpredictable, unpleasant stressors over the monotony of standard laboratory housing.

Fear effects on bank voles (Rodentia: Arvicolinae): testing for repellent candidates from predator volatiles.

BACKGROUND: Arvicolinae rodents are known pests causing damage to both agricultural and forest crops. Today, rodenticides for rodent control are widely discouraged owing to their negative effects on the environment. Rodents are the main prey for several predators, and their complex olfactory system allows them to identify risks of predation. Therefore, the potential use of predators' scents as repellents has gained interest as an ecologically based rodent control method. In a two-choice experiment, we investigated the potential repellent effects of five synthetic predator compounds: 2-phenylethylamine (2-PEA), 2-propylthietane (2-PT), indole, heptanal and 2,5-dihydro-2,4,5-trimethylthiazoline (TMT), at 1% and 5% doses, using the bank vole (Myodes glareolus) as a rodent model. RESULTS: The compound 2-PEA reduced both the food contacts and the time spent by voles in the treatment arm compared to the control arm. Likewise, 2-PT-treated arms reduced the food contacts, and the voles spent less time there, although this latter difference was not significant. Indole also showed a tendency to reduce the time spent at the treatment arm; however, this result was not significant. Unexpectedly, TMT had the reverse effect in showing attractive properties, possibly due to odor cues from differently sized predators and intraguild predation in nature. We found no dose-related effects for any compounds tested. CONCLUSION: Our results suggest that the 2-PEA and 2-PT are both effective odor stimuli for triggering reduced food contacts and area avoidance, and they may be good repellent candidates. We suggest further testing of 2-PEA and 2-PT in field experiments to further determine their dose-efficiency as repellents against rodents in more natural environments. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.