Marko Haapakoski

From interference to predation: type and effects of direct interspecific interactions of small mammals

Indirect exploitative competition, direct interference and predation are important interactions affecting species coexistence. These interaction types may overlap and vary with the season and life-history state of individuals. We studied effects of competition and potential nest predation by common shrews (Sorex araneus) on lactating bank voles (Myodes glareolus) in two seasons. The species coexist and may interact aggressively. Additionally, shrews can prey on nestling voles. We studied bank vole mothers’ spatial and temporal adaptations to shrew presence during summer and autumn. Further, we focused on fitness costs, e.g. decreased offspring survival, which bank voles may experience in the presence of shrews. In summer, interference with shrews decreased the voles’ home ranges and they spent more time outside the nest, but there were no effects on offspring survival. In autumn, we found decreased offspring survival in enclosures with shrews, potentially due to nest predation by shrews or by increased competition between species. Our results indicate a shift between interaction types depending on seasonal constraints. In summer, voles and shrews seem to interact mainly by interference, whereas resource competition and/or nest predation by shrews gain importance in autumn. Different food availability, changing environmental conditions and the energetic constraints in voles and shrews later in the year may be the reasons for the varying combinations of interaction types and their increasing effects on the inclusive fitness of bank voles. Our study provides evidence for the need of studies combining life history with behavioural measurements and seasonal constraints.

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 males. We also studied the effect of unequal food distribution between the fragments on vole distribution. The habitat of 0.25-ha enclosures was manipulated by forming either one large, two medium-sized, or four small habitat patches surrounded by an inhospitable matrix. Female density and distribution clearly affected male spacing behavior. Males had larger home ranges in the medium female density enclosures. Furthermore, the use of the inhospitable and risky matrix area increased with habitat fragmentation. Food supplementation improved individual condition measured as body mass but did not affect breeding success. Our experiments demonstrated that both small-scale habitat fragmentation and resource distribution affect the behavior and condition of individuals. Increased fragmentation led to increased risk taking in both mating and foraging behavior. This should have direct survival and fitness consequences, and therefore our results may be extrapolated to population-level consequences of habitat fragmentation.

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 risk on winter survival and onset of breeding in a common boreal rodent, the bank vole (Myodes glareolus). In a 2 × 2 factorial experiment, we manipulated food availability (food supplemented or not) and predation risk (presence/absence of predator odour) in 20 large outdoor enclosures in central Finland. 4. Survival probabilities were highest in no predation risk treatments, whereas they were lowest in the predator risk treatment. The same trend was observed in vole densities and the weight change in individuals. Voles with food addition bred earlier than in the other treatments. 5. We conclude that during energy constrained harsh conditions in winter, predation risk causes behavioural changes throughout the winter and has significant negative survival and fitness effects for small mammals, reflected as delay in the start of breeding.

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 new modelling framework that can be used for unbalanced data. The two vole species were hypothesised to have different habitat-dependent vulnerabilities. We created two habitats, open and forest, to provide different escape possibilities for the voles. We found a weak general preference of the weasels for the grey-sided voles over the bank voles, and a somewhat stronger preference specifically in open habitats. The weasels clearly preferred male grey-sided voles over females, whereas in bank voles, there was no difference. The activity of voles changed over time, so that voles increased their movements immediately after weasel introduction, but later adjusted their movements to times of lowered predation risk. Females that were more active had an elevated mortality risk, whereas in the case of males, the result was the opposite. We conclude that, in vulnerability to predation, the species- or habitat-specific characteristics of these prey species are playing a minor role compared to sex-specific characteristics.

Snow evens fragmentation effects and food determines overwintering success in ground-dwelling voles

Climate instability strongly affects overwintering conditions in organisms living in a strongly seasonal environment and consequently their survival and population dynamics. Food, predation and density effects are also strong during winter, but the effect of fragmentation of ground vegetation on ground-dwelling small mammals is unknown. Here, we report the results of a winter experiment on the effects of habitat fragmentation and food on experimental overwintering populations of bank voles Myodes glareolus. The study was conducted in large outdoor enclosures containing one large, two medium-sized or four small habitat patches or the total enclosure area covered with protective tall-grass habitat. During the stable snow cover of midwinter, only food affected the overwintering success, body condition, trappability and earlier onset of breeding in bank voles. However, after the snow thaw in spring, habitat fragmentation gained importance again, and breeding activities increased the movements of voles in the most fragmented habitat. The use of an open, risky matrix area increased along the habitat fragmentation. Our experiment showed that long-lasting stable snow cover protects overwintering individuals in otherwise exposed and risky ground habitats. We conclude that a stable winter climate and snow cover should even out habitat fragmentation effects on small mammals. However, along prolonged snow-free early winter and in an earlier spring thaw, this means loss of protection by snow cover both in terms of thermoregulation and predation. Thus, habitat cover is important for the survival of small ground-dwelling boreal mammals also during the non-breeding season.

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 and nutritional conditions in spring, affect the onset of breeding in a boreal small rodent, the bank vole, Myodes glareolus. We exposed wild-trapped individuals to four different treatments manipulating temperature (stable vs. variable) and food quality (high vs. low protein content) over five weeks in the laboratory. We monitored body-mass development, food consumption, and initiation of breeding. We found sex-specific responses to temperature variability, as males achieved their breeding condition faster in variable temperature treatments, whereas female maturation was delayed. Food quality had no effect on the onset of breeding. To test for possible reproductive trade-offs caused by reproductive decisions made in early spring, the experiment was continued in large outdoor enclosures. There seemed to be no significant long-term effects on reproduction, but early summer survival was affected by climate conditions experienced in spring. Our results show clear sex differences in the response to environmental cues regulating the onset of reproduction in bank voles. Hence, our study suggests that when an organism experiences rapid environmental changes, as are occurring on a global scale, divergent cues may lead to a reproductive mismatch between the sexes. This could noticeably decrease the fitness of many seasonally breeding species.

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 hormone levels, such as testosterone, often induce aggressive behavior. To test if the winter survival of females in a boreal rodent is better than that of males, and to assess the role of females in the winter aggregations, we generated bank vole (Myodes glareolus) populations of three different sex ratios (male-biased, female-biased and even density) under semi-natural conditions. We monitored survival, spatial behavior and hormonal status (stress and testosterone) during two winter months. We observed no significant differences in survival between the sexes or among populations with differing sex-ratios. The degree of movement area overlap was used as an indicator of social tolerance and potential communal nesting. Individuals in male biased populations showed a tendency to be solitary, whereas in female biased populations there was an indication of winter aggregation. Females living in male-biased populations had higher stress levels than the females from the other populations. The female-biased sex-ratio induced winter breeding and elevated testosterone levels in males. Thus, our results suggest that the sex-ratio of the overwintering population can lead to divergent overwintering strategies in bank voles.

Mammalian predator–prey interaction in a fragmented landscape: weasels and voles

The relationship between predators and prey is thought to change due to habitat loss and fragmentation, but patterns regarding the direction of the effect are lacking. The common prediction is that specialized predators, often more dependent on a certain habitat type, should be more vulnerable to habitat loss compared to generalist predators, but actual fragmentation effects are unknown. If a predator is small and vulnerable to predation by other larger predators through intra-guild predation, habitat fragmentation will similarly affect both the prey and the small predator. In this case, the predator is predicted to behave similarly to the prey and avoid open and risky areas. We studied a specialist predator’s, the least weasel, Mustela nivalis nivalis, spacing behavior and hunting efficiency on bank voles, Myodes glareolus, in an experimentally fragmented habitat. The habitat consisted of either one large habitat patch (non-fragmented) or four small habitat patches (fragmented) with the same total area. The study was replicated in summer and autumn during a year with high avian predation risk for both voles and weasels. As predicted, weasels under radio-surveillance killed more voles in the non-fragmented habitat which also provided cover from avian predators during their prey search. However, this was only during autumn, when the killing rate was also generally high due to cold weather. The movement areas were the same for both sexes and both fragmentation treatments, but weasels of both sexes were more prone to take risks in crossing the open matrix in the fragmented treatment. Our results support the hypothesis that habitat fragmentation may increase the persistence of specialist predator and prey populations if predators are limited in the same habitat as their prey and they share the same risk from avian predation.

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 presence” and “season.” We monitored use of feeding stations near and far from the nest as measurement of foraging activity and strategic foraging behavior. Vole mothers adapted their strategies to shrew presence and optimized their foraging behavior according to seasonal constraints, resulting in an interaction of treatment and season. In summer, shrew presence reduced food intake from feeding stations, while it enhanced intake in autumn. Shrew presence decreased the number of visited feeding stations in autumn and concentrated mother’s foraging efforts to fewer stations. Independent of shrew presence or season, mothers foraged more in patches further away from the nest than near the nest. Results indicate that females are not investing in nest guarding but try to avoid the accumulation of olfactory cues near the nest leading a predator to the young. Additionally, our study shows how foraging strategies and nest attendance are influenced by seasonal food provision.

Infanticide effects on behavior of the bank vole (Myodes glareolus) in the fragmented breeding habitat

Habitat fragmentation affects individual movements between favorable resource patches. In many small mammal species, an important intrinsic factor affecting recruitment of young is infanticide, committed especially by males. We predict that habitat fragmentation hinders movements of males between patches due to predation risk in the open areas. Thus, fragmentation reduces the number of males to which young litters are exposed to and decreases risk of infanticide in isolated habitat patches. Nonfragmented habitat provides not only breeding possibilities for more females but also safe movements to mate or commit infanticide for males. In a replicated enclosure experiment, we tested how infanticidal status of male bank voles (Myodes glareolus) affects their movements in fragmented vs. nonfragmented habitats with same total area and how this affects female spacing and offspring recruitment into population. We found no difference in the number of offspring recruited per female between infanticidal and fragmentation treatments. Females in the fragmented enclosures had smaller movement areas and stayed closer to their nests, suggesting better protection of pups against intruders. Infanticidal males moved more in general but especially in fragmented enclosures, whilst noninfanticidal males were moving more in nonfragmented enclosures. Our results suggest that behavior of females is affected by the habitat fragmentation, as we expected, but males searching for mates move similarly in safe and risky habitats. Thus, the threat of infanticide was not reflected in the recruitment of young into the population as probably the male–female interactions and effective nest protection by the mothers remained similar in both habitats.