Voles and weasels in the boreal Fennoscandian small mammal community : what happens if the least weasel disappears due to climate change?

Special Issue: Rodent Biology and ManagementClimate change, habitat loss and fragmentation are major threats for populations and a challenge for individual behavior, interactions and survival. Predator-prey interactions are modified by climate processes. In the northern latitudes, strong seasonality is changing and the main predicted feature is shortening and instability of winter. Vole populations in the boreal Fennoscandia exhibit multiannual cycles. High amplitude peak numbers of voles and dramatic population lows alternate in 3-5-year cycles shortening from North to South. One key factor, or driver, promoting the population crash and causing extreme extended lows, is suggested to be predation by the least weasel. We review the arms race between prey voles and weasels through the multiannual density fluctuation, affected by climate change, and especially the changes in the duration and stability of snow cover. For ground-dwelling small mammals, snow provides thermoregulation and shelter for nest sites, and helps them hide from predators. Predicted increases in the instability of winter forms a major challenge for species with coat color change between brown summer camouflage and white winter coat. One of these is the least weasel, Mustela nivalis nivalis. Increased vulnerability of wrong-colored weasels to predation affects vole populations and may have dramatic effects on vole dynamics. It may have cascading effects on other small rodent-predator interactions and even on plant-animal interactions and forest dynamics.Peer reviewe

Population cycles and outbreaks of small rodents : ten essential questions we still need to solve

Correction: 10.1007/s00442-021-04856-4, Oecologia (2021)Most small rodent populations in the world have fascinating population dynamics. In the northern hemisphere, voles and lemmings tend to show population cycles with regular fluctuations in numbers. In the southern hemisphere, small rodents tend to have large amplitude outbreaks with less regular intervals. In the light of vast research and debate over almost a century, we here discuss the driving forces of these different rodent population dynamics. We highlight ten questions directly related to the various characteristics of relevant populations and ecosystems that still need to be answered. This overview is not intended as a complete list of questions but rather focuses on the most important issues that are essential for understanding the generality of small rodent population dynamics.Peer reviewe

Pregnancy length and health in giant pandas: what can metabolic and urinary endocrine markers unveil?

Mature female giant pandas usually ovulate once a year. This is followed by an obligatory luteal phase, consisting of a long-lasting corpus luteum dormancy phase (CLD; primary increase in progestogens) and a much shorter active luteal phase (AL; secondary increase in progestogens). Varying duration of both the dormant (embryonic diapause) and AL (post-embryo reactivation) phases has hampered unambiguous pregnancy length determination in giant pandas until today. Additionally, progestogen profiles have been considered not to differ between pregnant and pseudopregnant cycles. Only ceruloplasmin, 13,14-dihydro-15-keto-PGF2α (PGFM) and – more recently – estrogens have been assigned diagnostic power so far. Our study investigated the competence of metabolic (fecal output) and Urinary Specific Gravity (USpG)-normalized urinary endocrine (progestogens, PGFM, glucocorticoids (GCM) and ceruloplasmin) markers for pregnancy monitoring including defining the duration of the AL phase length. Research on 24 (6 pregnant, 8 pseudopregnant and 10 non-birth) cycles of 6 giant pandas revealed a fixed AL phase length of 42 days in giant pandas, e.g. representing 6 weeks of post- diapause development in case of pregnancy. Progestogen concentrations were significantly higher in pregnant cycles throughout the majority of the AL phase, with significant higher values during the AL phase in healthy twin compared to singleton pregnancies. GCM concentrations were also markedly higher in giant pandas expecting offspring, with a clear increase towards birth in the final 2 weeks of pregnancy. This increase in GCM was running in parallel with elevating estrogen and PGFM concentrations, and decreasing progestogens. In addition, during the AL phase, a more pronounced decrease in fecal output was obvious for pregnant females. The combined profiles of non-invasive metabolic and endocrine markers, the latter normalized based on USpG, showed a true pregnancy signature during the AL phase. The findings of this study are applicable to retrospective evaluations of non-birth cycles facilitating categorizing those into pseudopregnant or lost pregnancies, with USpG-normalization of the urinary endocrine markers as a prerequisite

Habitat fragmentation, seasonality and predation affecting behaviour and survival of bank voles Myodes glareolus

Habitat loss and fragmentation are the main causes for innumerable population and species having become threatened and for many of them already having gone extinct. Declines in species richness or populations are primarily caused by habitat loss, but habitat fragmentation, which subdivides populations into smaller units, is also important factor. Habitat fragmentation inevitably affects behaviour, space use and social interactions of individuals. These are likely to form essential part of the mechanism behind observed population declines. In this thesis I have studied the role of behaviour and space use of animals in fragmented landscape in a series of enclosure experiments. Summer experiments (I-III) concentrate more on behavioural effects of fragmentation whilst the winter experiments (IV-V) focus on behaviour, survival and onset of breeding with food supplementation and predation risk. I found that increased fragmentation led to increased risk-taking in the case of male bank voles and the hunting weasel when resources were distributed into separate patches. Female bank voles tended to stay inside the habitat patch and closer to their nest in more fragmented landscape. During winter snow evened out differences between habitat and matrix, but during spring when the breeding season starts, males in the fragmented treatment needed to take more risks by crossing the open matrix. Food in winter is important factor for the condition, survival and onset of breeding in bank voles. Surprisingly, also mere predation risk during winter had significant effect on vole population density, condition, survival and onset of breeding in the spring. To conclude, habitat fragmentation have direct survival and fitness consequences for individuals and it changes individual interactions, but direction of these effects depend on fragmentation types and duration and scale of experiments

Do phase-dependent life history traits in cyclic voles persist in a common environment?

Phenotype and life history traits of an individual are a product of environmental conditions and the genome. Environment can be current or past, which complicates the distinction between environmental and heritable effects on the phenotype in wild animals. We studied genome-environment interactions on phenotype and life history traits by transplanting bank voles (Myodes glareolus) from northern and southern populations, originating from low or high population cycle phases, to common garden conditions in large outdoor enclosures. The first experiment focused on the persistence of body traits in autumn-captured overwintering populations. The second experiment focused on population growth and body traits in spring-captured founder voles and F1 generation. This experiment lasted the breeding season and subsequent winter. We verified phase-dependent differences in body size at capture. In the common environment, adult voles kept their original body size differences both over winter and during the breeding season. In addition, the first generation born in the common environment kept the size distribution of their parent population. The increase phase population maintained a more rapid growth potential, while populations from the decline phase of the cycle grew slower. After winter, the F1 generation of the increasing northern population matured later than the F1 of the southern declining ones. Our results suggest a strong role of heredity or early life conditions, greater than that of current juvenile and adult environmental conditions. Environmental conditions experienced by the parents in their early life can have inter-generational effects that manifest in offspring performance.Peer reviewe

Habitat fragmentation and predation: Experiments with bank voles (Myodes glareolus) and least weasel (Mustela nivalis nivalis)

Habitat loss and fragmentation are the main causes for innumerable population declines and species having become threatened or extinct. Habitat fragmentation inevitably affects behaviour and social interactions of individuals. These are likely to form an essential part of the mechanism behind observed population declines. Predator - prey interaction is strong factor shaping population viability and individual numbers and it is thought to change after habitat loss and fragmentation. The prediction is that specialized predators, dependent on a certain habitat type, should be more vulnerable to habitat loss compared to generalist predators, but habitat fragmentation effects are unknown. In this presentation, I summarize the results from our predator - prey experiments conducted in experimentally fragmented habitat, created in to 0.25 ha small mammal proof enclosures. Enclosures consisted of either non-fragmented (one patch) or fragmented (four patches) habitat of the same total area surrounded by low vegetation matrix. We have been measuring the fragmentation effects on behaviour and fitness of prey species the bank vole (Myodes glareolus) and predator species the least weasel (Mustela nivalis nivalis) in a series of experiments. We found that fragmentation led to increased matrix use in male voles and weasels, when resources were distributed into separate habitat patches. Small habitat fragments kept female bank voles closer to their nest where they were better able to protect pups against nest predators, infanticidal males. However, this did not affect the number of offspring recruited per female 1. Mammalian predator odor, a cue about increased predation risk in the habitat patches, decreased vole movements and voles directed movements towards matrix where the avian predation risk was higher 2. During high avian predation pressure, survival of male voles was poorer in fragmented habitat. Especially, males who moved most and spent time on open and risky matrix during radio -tracking were more likely to be depredated. Weasels killed more voles in the continuous habitat, which provided them safe hunting habitat from avian predators. However, this was only during autumn, when the kill rate was also higher due to cold weather 3. To conclude, habitat fragmentation has direct survival and fitness consequences for individuals and it changes species interactions, but direction of these effects depend on fragmentation types and duration and scale of experiments. 1 Haapakoski M. et al. Infanticide effects on behavior of the bank vole (Myodes glareolus) in the fragmented breeding habitat. Behav Ecol Sociobiol 2015; 69: 49–59. 2 Haapakoski M. et al. Conservation implications of change in antipredator behavior in fragmented habitat: Boreal rodent, the bank vole, as an experimental model. Biol Conserv 2015; 184: 11–17. 3 Haapakoski M. et al. Mammalian predator-prey interaction in a fragmented landscape: Weasels and voles. Oecologia 2013; 173: 1227–1235.peerReviewe

Olfactory cues and the value of information : Voles interpret cues differently based on recent predator encounters

Prey strategically respond to the risk of predation by varying their behavior while balancing the tradeoffs of food and safety. We present here an experiment that tests the way the same indirect cues of predation risk are interpreted by bank voles, Myodes glareolus, as the game changes through exposure to a caged weasel. Using optimal patch use, we asked wild-caught voles to rank the risk they perceived. We measured their response to olfactory cues in the form of weasel bedding, a sham control in the form of rabbit bedding, and an odor-free control. We repeated the interviews in a chronological order to test the change in response, i.e., the changes in the value of the information. We found that the voles did not differentiate strongly between treatments preexposure to the weasel. During the exposure, vole foraging activity was reduced in all treatments, but proportionally increased in the vicinity to the rabbit odor. Post-exposure, the voles focused their foraging in the control, while the value of exposure to the predator explained the majority of variation in response. Our data also suggested a sex bias in interpretation of the cues. Given how the foragers changed their interpretation of the same cues based on external information, we suggest that applying predator olfactory cues as a simulation of predation risk needs further testing. For instance, what are the possible effective compounds and how they change Bfear^ response over time. The major conclusion is that however effective olfactory cues may be, the presence of live predators overwhelmingly affects the information voles gained from these cues.peerReviewe

How Do Infanticidal Male Bank Voles (Myodes glareolus) Find the Nest with Pups?

Infanticide, the killing of conspecific young, occurs in most mammal species, like in our study species, the bank vole (Myodes glareolus). Infanticide by adult males is regarded as a strong factor affecting recruitment of young into population. It is considered as an adaptive behaviour, which may increase male fitness via resource gain or an increased access to mates. When an intruder is approaching the nest, the mother should not be present, as her nest guarding is very aggressive and successful. Pups use ultrasonic vocalisation to call their mother when mother leaves nest for foraging but it is not know which cues do infanticidal males use to find the nest with vulnerable pups to commit infanticide? We studied whether the pups' sounds or the olfactory cues of the nest guide the males of known infanticidal behavioural trait towards the nest with vulnerable pups. Four nest boxes in a large indoor arena offered different nesting cues: nest odour, pup vocalisation, both odour and sound or control with no cue. The result showed that infanticidal males were more active in their searching behaviour than non-infanticidal males and seemed to target the nest providing only acoustic cues. Four of the males, all infanticidal, intruded the nest box. Infanticidal males seem to actively search for nests with vulnerable pups by eavesdropping pup begging calls for absent mother. However, under natural conditions, mother presence and aggressive nest protection may be an effective counter strategy against strange male infanticide. When trapping study voles from the wild, we monitored occurrence of male infanticide across the breeding season from early to late summer. Proportion of infanticidal males was between 25 and 29% of all males tested along the breeding season. Our results suggest that male infanticide seems to cause a stable threat for pup mortality in increasing breeding season density.peerReviewe

Pre- and Postnatal Predator Cues Shape Offspring Anti-predatory Behavior Similarly in the Bank Vole

Prey animals can assess the risks predators present in different ways. For example, direct cues produced by predators can be used, but also signals produced by prey conspecifics that have engaged in non-lethal predator-prey interactions. These non-lethal interactions can thereby affect the physiology, behavior, and survival of prey individuals, and may affect offspring performance through maternal effects. We investigated how timing of exposure to predation-related cues during early development affects offspring behavior after weaning. Females in the laboratory were exposed during pregnancy or lactation to one of three odor treatments: (1) predator odor (PO) originating from their most common predator, the least weasel, (2) odor produced by predator-exposed conspecifics, which we call conspecific alarm cue (CAC), or (3) control odor (C). We monitored postnatal pup growth, and we quantified foraging and exploratory behaviors of 4-week-old pups following exposure of their mothers to each of the three odour treatments. Exposure to odors associated with predation risk during development affected the offspring behavior, but the timing of exposure, i.e., pre- vs. postnatally, had only a weak effect. The two non-control odors led to different behavioral changes: an attraction to CAC and an avoidance of PO. Additionally, pup growth was affected by an interaction between litter size and maternal treatment, again regardless of timing. Pups from the CAC maternal treatment grew faster in larger litters; pups from the PO maternal treatment tended to grow faster in smaller litters. Thus, in rodents, offspring growth and behavior are seemingly influenced differently by the type of predation risk perceived by their mothers.peerReviewe