0000000000142387
AUTHOR
Marko Haapakoski
Population cycles and outbreaks of small rodents: ten essential questions we still need to solve
AbstractMost 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…
Voles and weasels in the boreal Fennoscandian small mammal community : What happens if the least weasel disappears due to climate change?
Climate 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 ar…
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…
Conservation implications of change in antipredator behavior in fragmented habitat: Boreal rodent, the bank vole, as an experimental model
Abstract Habitat fragmentation is known to cause population declines but the mechanisms leading to the decline are not fully understood. Fragmentation is likely to lead to changes in predation risk, which may cause behavioral responses with possible population level consequences. It has recently been shown that the awareness of predator presence, resulting in a fear response, strongly affects behavior and physiology of the prey individuals. Costs arising from fear may be as important for the prey population size as the direct killing of prey. We tested how predation risk in the form of scent of a specialist predator, the least weasel (Mustela nivalis nivalis), affects bank vole (Myodes glar…
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 i…
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 …
Population sex-ratio affecting behavior and physiology of overwintering bank voles (Myodes glareolus)
Many boreal rodents are territorial during the breeding season but during winter become social and aggregate for more energy efficient thermoregulation. Communal winter nesting and social interactions are considered to play an important role for the winter survival of these species, yet the topic is relatively little explored. Females are suggested to be the initiators of winter aggregations and sometimes reported to survive better than males. This could be due to the higher social tolerance observed in overwintering females than males. Hormonal status could also affect winter behavior and survival. For instance, chronic stress can have a negative effect on survival, whereas high gonadal ho…
Balancing food, activity and the dangers of sunlit nights
Living in northern latitudes poses challenges to the animals that live in those habitats. The harsh environment provides a short breeding season where the sunlit summer nights provide little reprieve from visibility to predators and increased risk. In this paper, we tested the activity and food choice patterns of bank voles Myodes glareolus in early spring season, categorized by 18 h of daylight and 6 h of dusk in every day cycle. We found that territorial females showed a less predictable pattern of activity than males that were most active during the hours of dusk. The voles also showed preference to forage on high carbohydrate foods at sunset, while switching over to a more protein and f…
State-dependent foraging: lactating voles adjust their foraging behavior according to the presence of a potential nest predator and season
Parental care often produces a trade-off between meeting nutritional demands of offspring and the duties of offspring protection, especially in altricial species. Parents have to leave their young unattended for foraging trips, during which nestlings are exposed to predators. We investigated how rodent mothers of altricial young respond to risk of nest predation in their foraging decisions. We studied foraging behavior of lactating bank voles (Myodes glareolus) exposed to a nest predator, the common shrew (Sorex araneus). We conducted the experiment in summer (high resource provisioning for both species) and autumn (less food available) in 12 replicates with fully crossed factors “shrew pre…
Effects of fragmented breeding habitat and resource distribution on behavior and survival of the bank vole ( Myodes glareolus )
Habitat fragmentation causes negative population trends or even local extinction in many species. Understanding the role of fragmentation on behavior and space use of animals is an essential part of revealing the mechanism behind observed population declines. We studied experimentally the effects of small-scale habitat fragmentation on the distribution and movement of bank voles (Myodes glareolus) in seminatural enclosures. We predicted that besides habitat structure, availability of two resources, food for both sexes, and receptive females for males, determine individual distribution. We manipulated female density (either 0, 4, or 12 per enclosure) and followed movements of radio-collared …
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 comm…
Secondhand horror: effects of direct and indirect predator cues on behavior and reproduction of the bank vole
Risk recognition by prey is of paramount importance within the evolutionary arms race between predator and prey. Prey species are able to detect direct predator cues like odors and adjust their behavior appropriately. The question arises whether an indirect predation cue, such as the odor of scared individuals, can be detected by conspecifics and subsequently affects recipient behavior. Parents may also transfer their experience with predators to their offspring. In two experiments, we assessed how direct and indirect predation cues affect bank vole (Myodes glareolus) foraging behavior, reproduction, and pup fitness. Weasel (Mustela nivalis) odor served as the direct cue, whereas the odor o…
Risk of inbreeding : problem of mate choice and fitness effects?
Mating with close kin may cause inbreeding depression with negative consequences to offspring and local populations. There exist mechanisms like kin-recognition or sex-specific dispersal to avoid mating with kin. In fluctuating population densities, like in many small mammals, both very low and very high densities provide conditions for inbreeding, if kin males are prone to stay in their natal area. Females are choosy and male dominance is thought to be the key feature when selecting mating partners. The aim of this study was to test the possible discrepancy in mate choice and negative fitness effects of inbreeding in two experiments, one in the laboratory and one in field enclosures. We as…
Sex-specific variation in the onset of reproduction and reproductive trade-offs in a boreal small mammal
In seasonal environments, the optimal onset of reproduction plays a major role in defining the reproductive success of an individual. Environmental cues, like day length, weather conditions, and food, regulate the initiation and termination of the breeding season. Besides the interspecific variation in response to environmental cues, it has been suggested that due to different selection pressures, females and males can have different responses to environmental stimuli. However, this phenomenon has gained relatively little consideration, and the physiological mechanism behind these differences is not well known. Here, we report how two different environmental cues, variability of temperature…
Bank vole alarm pheromone chemistry and effects in the field
Chemical communication plays an important role in mammalian life history decisions. Animals send and receive information based on body odour secretions. Odour cues provide important social information on identity, kinship, sex, group membership or genetic quality. Recent findings show, that rodents alarm their conspecifics with danger-dependent body odours after encountering a predator. In this study, we aim to identify the chemistry of alarm pheromones (AP) in the bank vole, a common boreal rodent. Furthermore, the vole foraging efficiency under perceived fear was measured in a set of field experiments in large outdoor enclosures. During the analysis of bank vole odour by gas chromatograph…
Predation on two vole species by a shared predator: antipredatory response and prey preference
In prey communities with shared predators, variation in prey vulnerability is a key factor in shaping community dynamics. Conversely, the hunting efficiency of a predator depends on the prey community structure, preferences of the predator and antipredatory behavioural traits of the prey. We studied experimentally, under seminatural field conditions, the preferences of a predator and the antipredatory responses of prey in a system consisting of two Myodes species of voles, the grey-sided vole (M. rufocanus Sund.) and the bank vole (M. glareolus Schreb.), and their specialist predator, the least weasel (Mustela nivalis nivalis L.). To quantify the preference of the weasels, we developed a ne…
Changing winter conditions in the boreal forest : the effects of fluctuating temperature and predation risk on activity and physiological stress level in bank voles
Due to global climate change, the winter conditions in the North are predicted to change, as the time with an intact insulating snow cover gets shorter or disappears altogether. For small mammals, this could cause exposure to strong temperature fluctuations and increased predation risk, inducing severe stress and leading to alterations in the physical condition and behavior. To test this, we exposed bank voles (Myodes glareolus) to different temperature regimes and cues of predator threat under laboratory conditions. The test animals experienced either a stable but cool temperature regime resembling the stable conditions under snow cover, or an unstable temperature regime with cold nights a…
Predation risk and food: opposite effects on overwintering survival and onset of breeding in a boreal rodent
1. In seasonal environments, optimal onset of breeding and survival plays major roles in individual fitness. Many physiological and behavioural factors related to breeding increase the risk of predation; thus, breeding decisions should be based on current risks and benefits. According to life-history theory, if current predation risk is high and breeding itself increases the risk, it may be beneficial to postpone breeding. 2. During winter in northern hemispheres, food availability is limited and is at its lowest just prior to the onset of breeding in spring. Food constraint may lead to poor condition and reduced ability to start breeding. 3. We studied the effects of food and predation ris…
Olfactory cues and the value of information: voles interpret cues based on recent predator encounters
Abstract 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.…
In utero behavioral imprinting to predation risk in pups of the bank vole
Abstract In the predator–prey arms race, survival-enhancing adaptive behaviors are essential. Prey can perceive predator presence directly from visual, auditory, or chemical cues. Non-lethal encounters with a predator may trigger prey to produce special body odors, alarm pheromones, informing conspecifics about predation risks. Recent studies suggest that parental exposure to predation risk during reproduction affects offspring behavior cross-generationally. We compared behaviors of bank vole (Myodes glareolus) pups produced by parents exposed to one of three treatments: predator scent from the least weasel (Mustela nivalis nivalis); scent from weasel-exposed voles, i.e., alarm pheromones;…
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 thi…