Surveillance for diseases, pathogens, and toxicants of muskrat (Ondatra zibethicus) in Pennsylvania and surrounding regions.

Using diagnostic data and contemporary sampling efforts, we conducted surveillance for a diversity of pathogens, toxicants, and diseases of muskrats (Ondatra zibethicus). Between 1977 and 2019, 26 diagnostic cases were examined from Kansas and throughout the Southeast and Mid-Atlantic, USA. We identified multiple causes of mortality in muskrats, but trauma (8/26), Tyzzer's disease (5/6), and cysticercosis (5/26) were the most common. We also conducted necropsies, during November 2018-January 2019 Pennsylvania muskrat trapping season, on 380 trapper-harvested muskrat carcasses after the pelt was removed. Tissue samples and exudate were tested for presence of or exposure to a suite of pathogens and contaminants. Gastrointestinal tracts were examined for helminths. Intestinal helminths were present in 39.2% of necropsied muskrats, with Hymenolepis spp. (62%) and echinostome spp. (44%) being the most common Molecular testing identified a low prevalence of infection with Clostridium piliforme in the feces and Sarcocystis spp. in the heart. We detected a low seroprevalence to Toxoplasma gondii (1/380). No muskrats were positive for Francisella tularensis or Babesia spp. Cysticercosis was detected in 20% (5/26) of diagnostic cases and 15% (57/380) of our trapper-harvested muskrats. Toxic concentrations of arsenic, cadmium, lead, or mercury were not detected in tested liver samples. Copper, molybdenum, and zinc concentrations were detected at acceptable levels comparative to previous studies. Parasite intensity and abundance were typical of historic reports; however, younger muskrats had higher intensity of infection than older muskrats which is contradictory to what has been previously reported. A diversity of pathogens and contaminants have been reported from muskrats, but the associated disease impacts are poorly understood. Our data are consistent with historic reports and highlight the wide range of parasites, pathogens and contaminants harbored by muskrats in Pennsylvania. The data collected are a critical component in assessing overall muskrat health and serve as a basis for understanding the impacts of disease on recent muskrat population declines.

Timing outweighs magnitude of rainfall in shaping population dynamics of a small mammal species in steppe grassland.

Climate change-induced shifts in species phenology differ widely across trophic levels, which may lead to consumer-resource mismatches with cascading population and ecosystem consequences. Here, we examined the effects of different rainfall patterns (i.e., timing and amount) on the phenological asynchrony of population of a generalist herbivore and their food sources in semiarid steppe grassland in Inner Mongolia. We conducted a 10-y (2010 to 2019) rainfall manipulation experiment in 12 0.48-ha field enclosures and found that moderate rainfall increases during the early rather than late growing season advanced the timing of peak reproduction and drove marked increases in population size through increasing the biomass of preferred plant species. By contrast, greatly increased rainfall produced no further increases in vole population growth due to the potential negative effect of the flooding of burrows. The increases in vole population size were more coupled with increased reproduction of overwintered voles and increased body mass of young-of-year than with better survival. Our results provide experimental evidence for the fitness consequences of phenological mismatches at the population level and highlight the importance of rainfall timing on the population dynamics of small herbivores in the steppe grassland environment.

Rapid development of mature vocal patterns of ultrasonic calls in a fast-growing rodent, the yellow steppe lemming (Eolagurus luteus).

Ultrasonic vocalizations (USV) of laboratory rodents may serve as age-dependent indicators of emotional arousal and anxiety. Fast-growing Arvicolinae rodent species might be advantageous wild-type animal models for behavioural and medical research related to USV ontogeny. For the yellow steppe lemming Eolagurus luteus, only audible calls of adults were previously described. This study provides categorization and spectrographic analyses of 1176 USV calls emitted by 120 individual yellow steppe lemmings at 12 age classes, from birth to breeding adults over 90 days (d) of age, 10 individuals per age class, up to 10 USV calls per individual. The USV calls emerged since 1st day of pup life and occurred at all 12 age classes and in both sexes. The unified 2-min isolation procedure on an unfamiliar territory was equally applicable for inducing USV calls at all age classes. Rapid physical growth (1 g body weight gain per day from birth to 40 d of age) and the early (9-12 d) eyes opening correlated with the early (9-12 d) emergence of mature vocal patterns of USV calls. The mature vocal patterns included a prominent shift in percentages of chevron and upward contours of fundamental frequency (f0) and the changes in the acoustic variables of USV calls. Call duration was the longest at 1-4 d, significantly shorter at 9-12 d and did not between 9-12-d and older age classes. The maximum fundamental frequency (f0max) decreased with increase of age class, from about 50 kHz in neonates to about 40 kHz in adults. These ontogenetic pathways of USV duration and f0max (towards shorter and lower-frequency USV calls) were reminiscent of those in laboratory mice Mus musculus.

Subpopulation augmentation among habitat patches as a tool to manage an endangered Mojave Desert wetlands-dependent rodent during anthropogenic restricted water climate regimes.

Intensive management may be necessary to protect some highly vulnerable endangered species, particularly those dependent on water availability regimes that might be disrupted by ongoing climate change. The Amargosa vole (Microtus californicus scirpensis) is an increasingly imperiled rodent constrained to rare wetland habitat in the Mojave Desert. In 2014 and 2016, we trapped and radio-collared 30 voles, 24 were translocated and six remained at donor and recipient marshes as resident control voles. Soft-release was performed followed by remote camera and radio-telemetry monitoring. Although comparative metrics were not statistically significant, the mean maximum known distance moved (MDM) was longer for translocated (82.3 ± 14.6 m) vs. resident-control voles (74.9 ± 17.5 m) and for female (98.4 ± 19.9 m) vs. male (57.8 ± 9.1 m) voles. The mean area occupied (AO) tended to be greater in female (0.15 ± 0.04 ha) vs. male (0.12 ± 0.03 ha) voles, and control voles (0.15 ± 0.05 ha) compared with translocated voles (0.13 ± 0.03 ha). The mean minimum known time alive (MTA) was 38.2 ± 19.4 days for resident-control voles and 47.0 ± 10.6 days for translocated voles. Female survival (55.7 ± 14.3 days) exceeded that of males (31.5 ± 9.4 days) regardless of study group. Activity in bulrush/rushes mix and bulrush vegetation types was strongly and significantly overrepresented compared with salt grass and rushes alone, and habitat selection did not differ between resident and translocated voles. Our results provide ecological and methodological insights for future translocations as part of a strategy of promoting long-term survival of an extremely endangered small mammal in a wild desert environment.

An assessment of vegetation management practices and burrow fumigation with aluminum phosphide as tools for managing voles within perennial crop fields in California, USA.

Voles (Cricetidae) cause extensive damage to a variety of crops throughout much of the Northern Hemisphere. The removal of vegetation from crop fields at the end of the growing season, combined with a subsequent burrow fumigant application of aluminum phosphide, has the potential to substantially curtail vole activity but has not been thoroughly examined. We set up a study to test the impact of these management tools in perennial globe artichoke (Cynara cardunculus var. scolymus) fields in Monterey County, CA, during 2010 and 2011, to determine their potential utility as part of an integrated pest management (IPM) program for managing California voles (Microtus californicus). We used both chewing indices and mortality estimates derived via radiotelemetry to assess the efficacy of aboveground vegetation removal and aluminum phosphide applications on vole abundance. We determined the impact of plowing artichoke fields on vole activity as well. Both removal of vegetation and applications of aluminum phosphide substantially reduced vole presence within treated fields. Plowing also reduced vole abundance to the point of little residual activity following treatment. These management practices appear to be effective at eliminating voles from crop fields. Combining these tools with management practices designed to slow down reinvasion by neighboring vole populations (e.g., barriers, repellents, traps) has the potential to substantially reduce farmer reliance on rodenticides for vole management, although rodenticides will still be needed to curtail populations that reestablish within crop fields. Such an IPM approach should substantially benefit both farmers and agro-ecosystems.

Seasonal difference in temporal transferability of an ecological model: near-term predictions of lemming outbreak abundances.

Ecological models have been criticized for a lack of validation of their temporal transferability. Here we answer this call by investigating the temporal transferability of a dynamic state-space model developed to estimate season-dependent biotic and climatic predictors of spatial variability in outbreak abundance of the Norwegian lemming. Modelled summer and winter dynamics parametrized by spatial trapping data from one cyclic outbreak were validated with data from a subsequent outbreak. There was a distinct difference in model transferability between seasons. Summer dynamics had good temporal transferability, displaying ecological models' potential to be temporally transferable. However, the winter dynamics transferred poorly. This discrepancy is likely due to a temporal inconsistency in the ability of the climate predictor (i.e. elevation) to reflect the winter conditions affecting lemmings both directly and indirectly. We conclude that there is an urgent need for data and models that yield better predictions of winter processes, in particular in face of the expected rapid climate change in the Arctic.

Postnatal maturation of the intestinal epithelial barrier in prairie voles.

Intestinal epithelium develops during gestation and continues to mature post-natally into a selective barrier that will protect the individual while still allowing passage of nutrients. Until fully mature, the risk of translocation of microorganisms, toxins or antigens into the sub-epithelial tissue is high and could result in pathologies with life-altering consequences, or even premature death. Because of their monogamous mating system, prairie voles are an emerging model for studying the role of the intestinal microbiota in modulating social behavior via the microbiota-gut-brain-behavior axis. However, knowledge about the voles' intestinal barrier maturation is lacking. Understanding the maturation of the intestine epithelial barrier can complement the extensive behavioral literature for future studies involving the vole gut-brain axis. In this study, we characterized intestinal barrier function by demonstrating that two-week-old prairie voles have high paracellular absorption of FITC-dextran molecules prior to markedly decreased permeability at three weeks of age. In light of the fundamental role of tight junctions in maintaining epithelial integrity regulating intestinal permeability, we examined tight junction gene expression profiles. Transmission electron microscopy was used to visualize tight junction structure. Our results provide a timeline for intestinal barrier maturation and point to tight junction proteins involved in this process in prairie voles.

Age-specific and context-specific responses of the medial extended amygdala in the developing prairie vole.

The social needs of organisms change as they mature. Yet, little is known about the mechanisms that subserve processing social interactions or how these systems develop. The medial extended amygdala (meEA) is comprised of the medial bed nucleus of the stria terminalis (BSTm) and the medial amygdala (MeA). This neural complex holds great promise for understanding how the social brain processes information. We assessed expression of the immediate early gene cFos and the enzyme tyrosine hydroxylase (TH) at three developmental time-points (postnatal day [PND] 2, 9, and 21) to determine how developing prairie voles process familial social contact, separation, and reunion. We demonstrate that (1) BSTm cFos responses were sensitive to separation from family units at PND 9 and PND 21, but not at PND 2; (2) MeA cFos responses were sensitive to reunion with the family, but only in PND 21 pups; (3) BSTm TH neurons did not exhibit differential responses to social condition at any age; and (4) MeA TH neurons responded strongly to social contact (remaining with family or following reunion), but only at PND 21. Our results suggest that the sub-units of the meEA become functionally responsive at different developmental time points, and are differentially activated in response to distinct social contexts. Overall, our results support the notion that interconnected regions of the meEA follow divergent developmental timelines and are sensitive to distinct properties of social contexts.

Interactions of sex and early life social experiences at two developmental stages shape nonapeptide receptor profiles.

Early life social experiences are critical to behavioral and cognitive development, and can have a tremendous influence on developing social phenotypes. Most work has focused on outcomes of experiences at a single stage of development (e.g. perinatal or post-weaning). Few studies have assessed the impact of social experience at multiple developmental stages and across sex. Oxytocin and vasopressin are profoundly important for modulating social behavior and these nonapeptide systems are highly sensitive to developmental social experience, particularly in brain areas important for social behavior. We investigated whether oxytocin receptor (OTR) and vasopressin receptor (V1aR) distributions of prairie voles (Microtus ochrogaster) change as a function of parental composition within the natal nest or social composition after weaning. We raised pups either in the presence or absence of their fathers. At weaning, offspring were housed either individually or with a same-sex sibling. We also examined whether changes in receptor distributions are sexually dimorphic because the impact of the developmental environment on the nonapeptide system could be sex-dependent. We found that differences in nonapeptide receptor expression were region-specific, sex-specific and rearing condition-specific, indicating a high level of complexity in the ways that early life experiences shape the social brain. We found many more differences in V1aR density compared to OTR density, indicating that nonapeptide receptors demonstrate differential levels of neural plasticity and sensitivity to environmental and biological variables. Our data highlight that critical factors including biological sex and multiple experiences across the developmental continuum interact in complex ways to shape the social brain.

Circulation and diagnostics of Puumala virus in Norway: nephropatia epidemica incidence and rodent population dynamics.

Hantaviruses pose a public health concern worldwide causing haemorrhagic fever with renal syndrome (HFRS) and hantavirus pulmonary syndrome (HPS). Puumala virus (PUUV) is the most prevalent hantavirus in Central and Northern Europe, and causes a mild form of HFRS, also known as nephropathia epidemica (NE). In nature, the main host of PUUV is the bank vole (Myodes glareolus), and transmission to humans occurs through inhalation of aerosols from rodent excreta. Nephropathia epidemica is particularly prevalent in Nordic countries, however, few studies of PUUV have been performed in Norway. The aim of this study was to analyse the dynamics of PUUV in Norway and compare with bank vole population dynamics, and also to complement the current diagnostic methodology of NE in Norway. Our results showed a significant seasonal and geographical variation of NE, and a general parallel peak trend between bank vole population densities and human NE incidence. A real-time and a nested PCR were successfully established as an invaluable diagnostic tool, with detection and sequencing of PUUV in a human serum sample for the first time in Norway. Phylogenetic analysis showed clustering of the obtained human sample with previous Norwegian bank vole isolates.

Molecular cloning and characterization of kiss1 in Brandt's voles (Lasiopodomys brandtii).

Kisspeptin, encoded by kiss1, has been regarded as a major modulator of mammalian puberty and fertility due to its stimulation on GnRH. Brandt's vole is one of the main pest species on the Inner Mongolian steppes for its striking reproductive capacity and kiss1 is a key candidate gene related to reproductive regulatory cascades. In this study, kiss1 cDNA was cloned from the hypothalamus of Brandt's voles and kiss1 mRNA levels were investigated in different tissues, and at different developmental stages, using high-throughput real-time PCR. The full-length kiss1 cDNA was 682bp, containing an ORF of 405bp, encoding 134 amino acids with a conserved kisspeptin-10 region. Kiss1 mRNA was specifically expressed in ovary, testicle, small intestine, kidney, liver and hypothalamus tissues, and was undetectable in other tissues, including pituitary, heart, adrenal gland, bladder and uterus. Sexual organs of both male and female voles enter a period of rapid development in the postnatal 4weeks and reach or approach sexual maturity by 8weeks after birth. Kiss1 mRNA levels in the hypothalamus did not show a significant difference between week 2 and week 4, indicating kiss1 mRNA levels may not be related to the rapid growth of the sexual organs in early developmental stages. Kiss1 transcripts significantly increased in both sexes 8weeks after birth, and then were maintained at high levels in adults, indicating its possible role in the onset of puberty and maintaining of reproductive activity. These results are helpful to further the study of kiss1 function in reproductive regulation of Brandt's voles.

Thyroid pathology in deer mice (Peromyscus maniculata) from a reclaimed mine site on the athabasca oil sands.

Information on naturally occurring thyroid disease in wild animals in general and in small mammals specifically is extremely limited. In the present field-based work, we investigated the structure and function of thyroid glands of deer mice (Peromyscus maniculata) studied as sentinels of ecosystem sustainability on reclaimed areas post-mining on the oil sands of northeastern Alberta, because of their greater sensitivity to contaminants relative to meadow voles (Microtus pennsylvanicus) on the same sites. Extraction of bitumen in the oil sands of northeastern Alberta, results in the release of contaminants including polycyclic aromatic compounds (PACs), metals, and metalloids to the environment that have a measurable biological cost to wildlife living in the affected areas. In previous investigations, deer mice exposed to pollution at reclaimed areas showed compromised ability to regenerate glutathione indicating oxidative stress, together with decreased testicular mass and body condition during the breeding season. In the present study, thyroid glands from those deer mice from the reclaimed site had markedly increased follicular cell proliferation and decreased colloid compared to animals from the reference site. This pathology was positively associated with the greater oxidative stress in the deer mice. Thyroid hormones, both thyroxine and triiodothyronine, were also higher in animals with greater oxidative stress indicating increased metabolic demands from contaminant related subclinical toxicity. This work emphasizes the value of using a combination of endocrinological, histological and oxidative stress biomarkers to provide sensitive measures of contaminant exposure in small mammals on the oil sands.

Effects of dietary tannic acid on the growth, hepatic gene expression, and antioxidant enzyme activity in Brandt's voles (Microtus brandti).

This study was designed to investigate the physiological and biochemical responses of Brandt's voles to the persistent presence of dietary tannic acid. The diet for animals in the experimental group was supplemented with 3% dietary tannic acid for 5weeks. The control group received a commercial lab chow. No significant differences were detected in body weight, organ (heart, kidney, and liver) weights, and organ parameters between animals from two groups. However, voles in the experimental group had significantly higher daily food intake, increased contents of proline and histidine in saliva and feces after protein hydrolysis, and elevated hepatic expression of transferrin than the control. Our results suggested the existence of adaptive strategies developed in Brandt's voles to overcome the adverse effects of dietary tannic acid. (1) Food consumption was increased to satisfy their nutritional demands. (2) The secretion of tannic-acid-binding salivary proteins was promoted. (3) The absorption of iron was enhanced. These alterations contributed to neutralize the negative effects of tannic acid and maintain body mass in animals supplemented with tannic acid. As the result of the consumption of tannic acid, hepatic expression of 3-hydroxy-3-methylglutaryl coenzyme A reductase was significantly decreased, while the overall potential of the antioxidant system, characterized by increased hepatic enzymatic activities of catalase and glutathione peroxidase, was enhanced. Our results also implied the involvement of tannic acid in the regulation of lipid metabolism and oxidative stress in voles.

Intraspecific variation in the energetics of the Cabrera vole.

Basal metabolic rate (BMR) is an intensively topic studied in ecophysiology for the purpose of understanding energy budgets of the species, variations of energy expenditure during their diary activities and physiological acclimatization to the environment. Establishing how the metabolism is assembled to the environment can provide valuable data to improve conservation strategies of endangered species. In this sense, metabolic differences associated to habitats have been widely reported in the interspecific level, however little is known about the intraspecific view of BMR under an environmental gradient. In this study, we researched the effect of the habitat on metabolic rate of an Iberian endemic species: Iberomys cabrerae. Animals were captured in different subpopulations of its altitudinal range and their MR was studied over a thermal gradient. MR was analyzed through a Linear Mixed Model (LMM) in which, in addition to thermal effects, the bioclimatic zone and sex also influenced the metabolism of the species. The beginning of thermoneutrality zone was set on 26.5°C and RMR was 2.3ml O2g(-1)h(-1), intermediate between both bioclimatic zones. Supramediterranean subpopulations started the Tlc earlier (24.9°C) and had higher RMR than the mesomediterranean ones (26.9°C). The thermal environment together with primary productivity conditions could explain this difference in the metabolic behaviour of the Cabrera voles.

Developmental integration in a functional unit: deciphering processes from adult dental morphology.

The evolution of mammalian dentition is constrained by functional necessity and by the non-independence of morphological structures. Efficient chewing implies coherent tooth coordination from development to motion, involving covariation patterns (integration) within dental parts. Using geometric morphometrics, we investigate the modular organization of the highly derived vole dentition. Integration patterns between and within the upper and lower molar rows are analyzed to identify potential modules and their origins (functional and developmental). Results support an integrated adult dentition pattern for both developmental and functional aspects. The integration patterns between opposing molar pairs suggest a transient role for the second upper and lower molars during the chewing motion. Upper and lower molar rows form coherent units but the relative integration of molar pairs is in contradiction with existing developmental models. Emphasis on the first three cusps to grow leads to a very different integration pattern, which would be congruent with developmental models. The early developmental architecture of traits is masked by later stages of growth, but may still be deciphered from the adult phenotype, if careful attention is paid to relevant features.

Diet quality limits summer growth of field vole populations.

Marked variation occurs in both seasonal and multiannual population density peaks of northern European small mammal species, including voles. The availability of dietary proteins is a key factor limiting the population growth of herbivore species. The objective of this study is to investigate the degree to which protein availability influences the growth of increasing vole populations. We hypothesise that the summer growth of folivorous vole populations is positively associated with dietary protein availability. A field experiment was conducted over a summer reproductive period in 18 vegetated enclosures. Populations of field voles (Microtus agrestis) were randomised amongst three treatment groups: 1) food supplementation with ad libitum high protein (30% dry weight) pellets, 2) food supplementation with ad libitum low protein (1% dry weight; both supplemented foods had equivalent energy content) pellets, and 3) control (no food supplementation), n = 6 per treatment. Vole density, survival, demographic attributes and condition indicators were monitored with live-trapping and blood sampling. Highest final vole densities were attained in populations that received high protein supplementation and lowest in low protein populations. Control populations displayed intermediate densities. The survival rate of voles was similar in all treatment groups. The proportion of females, and of those that were pregnant or lactating, was highest in the high protein supplemented populations. This suggests that variation in reproductive, rather than survival rates of voles, accounted for density differences between the treatment groups. We found no clear association between population demography and individual physiological condition. Our results demonstrate that dietary protein availability limits vole population growth during the summer growing season. This suggests that the nutritional quality of forage may be an underestimated source of interannual variation in the density and growth rates of widely fluctuating populations of herbivorous small mammals.

[Experimental hybridization of voies of the genus Microtus s.l. M. socialis with species of the group arvalis (Mammalia, Rodentia)].

The results of interspecific crosses of the social vole Microtus socialis with the Altai vole M. obscurus, the East European vole M. rossiaemeridionalis, and the Transcaspian vole M. transcaspicus are presented. The role of the sperm head structure in the reproductive isolation of this species was studied. Hybrids were obtained in five of the six crossing combinations. It is established that significant differences in the sperm head shape in the social vole and in arvalis group species do not prevent fertilization. The sterility of hybrids indicates the existence of postcopulative mechanisms of reproductive isolation.

Influence of global atmospheric change on the feeding behavior and growth performance of a mammalian herbivore, Microtus ochrogaster.

Global atmospheric change is influencing the quality of plants as a resource for herbivores. We investigated the impacts of elevated carbon dioxide (CO2) and ozone (O3) on the phytochemistry of two forbs, Solidago canadensis and Taraxacum officinale, and the subsequent feeding behavior and growth performance of weanling prairie voles (Microtus ochrogaster) feeding on those plants. Plants for the chemical analyses and feeding trials were harvested from the understory of control (ambient air), elevated CO2 (560 µl CO2 l(-1)), and elevated O3 (ambient × 1.5) rings at the Aspen FACE (Free Air CO2 Enrichment) site near Rhinelander, Wisconsin. We assigned individual voles to receive plants from only one FACE ring and recorded plant consumption and weanling body mass for seven days. Elevated CO2 and O3 altered the foliar chemistry of both forbs, but only female weanling voles on the O3 diet showed negative responses to these changes. Elevated CO2 increased the fiber fractions of both plant species, whereas O3 fumigation elicited strong responses among many phytochemical components, most notably increasing the carbon-to-nitrogen ratio by 40% and decreasing N by 26%. Consumption did not differ between plant species or among fumigation treatments. Male voles were unaffected by the fumigation treatments, whereas female voles grew 36% less than controls when fed O3-grown plants. These results demonstrate that global atmospheric change has the potential to affect the performance of a mammalian herbivore through changes in plant chemistry.

Nonlinear effects of climate on boreal rodent dynamics: mild winters do not negate high-amplitude cycles.

Small rodents are key species in many ecosystems. In boreal and subarctic environments, their importance is heightened by pronounced multiannual population cycles. Alarmingly, the previously regular rodent cycles appear to be collapsing simultaneously in many areas. Climate change, particularly decreasing snow quality or quantity in winter, is hypothesized as a causal factor, but the evidence is contradictory. Reliable analysis of population dynamics and the influence of climate thereon necessitate spatially and temporally extensive data. We combined data on vole abundances and climate, collected at 33 locations throughout Finland from 1970 to 2011, to test the hypothesis that warming winters are causing a disappearance of multiannual vole cycles. We predicted that vole population dynamics exhibit geographic and temporal variation associated with variation in climate; reduced cyclicity should be observed when and where winter weather has become milder. We found that the temporal patterns in cyclicity varied between climatically different regions: a transient reduction in cycle amplitude in the coldest region, low-amplitude cycles or irregular dynamics in the climatically intermediate regions, and strengthening cyclicity in the warmest region. Our results did not support the hypothesis that mild winters are uniformly leading to irregular dynamics in boreal vole populations. Long and cold winters were neither a prerequisite for high-amplitude multiannual cycles, nor were mild winters with reduced snow cover associated with reduced winter growth rates. Population dynamics correlated more strongly with growing season than with winter conditions. Cyclicity was weakened by increasing growing season temperatures in the cold, but strengthened in the warm regions. High-amplitude multiannual vole cycles emerge in two climatic regimes: a winter-driven cycle in cold, and a summer-driven cycle in warm climates. Finally, we show that geographic climatic gradients alone may not reliably predict biological responses to climate change.