Janne Sundell

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.

Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent

Predation risk has been shown to alter various behaviours in prey. Risk alters activity, habitat use and foraging, and weight decrease might be a consequence of that. In mammals, studies on physiological measures affected by risk of predation, other than weight, are rare. We studied in two separate laboratory experiments foraging, hoarding behaviour and expression of stress measured non-invasively from the faeces in the bank vole (Clethrionomys glareolus), a common boreal rodent. Voles were exposed to predation risk using odours of the least weasels (Mustela nivalis nivalis). Distilled water served as control. In the first experiment, we found that foraging effort, measured as sunflower seeds taken from seed trays filled with sand, was significantly lower in trays scented with weasel odour. Both immediate consumption of seeds and hoarding were affected negatively by the weasel odour. Females hoarded significantly more than males in autumn. In the second experiment, the negative effect of weasel odour on foraging was consistent over a 3-day experiment, but the strongest effect was observed in the first night. Foraging increased over the time of the experiment, which might reflect either energetic compensation during a longer period of risk, predicted in the predation risk allocation hypothesis, or habituation to the odour-simulated risk. Despite decreased foraging under predation risk, stress measured as corticosteroid metabolite concentration in vole faeces was not affected by the weasel odour treatment. In conclusion, we were able to verify predation-risk-mediated changes in the foraging effort of bank voles but no physiological stress response was measured non-invasively, probably due to great individual variation in secretion of stress hormones.

Variation in predation risk and vole feeding behaviour: a field test of the risk allocation hypothesis

Many prey animals experience temporal variation in the risk of predation and therefore face the problem of allocating their time between antipredator efforts and other activities like feeding and breeding. We investigated time allocation of prey animals that balanced predation risk and feeding opportunities. The predation risk allocation hypothesis predicts that animals should forage more in low- than in high-risk situations and that this difference should increase with an increasing attack ratio (i.e. difference between low- and high-risk situations) and proportion of time spent at high risk. To test these predictions we conducted a field test using bank voles (Clethrionomys glareolus) as a prey and the least weasel (Mustela nivalis nivalis) as a predator. The temporal pattern and intensity of predation risk were manipulated in large outdoor enclosures and the foraging effort and patch use of voles were measured by recording giving-up densities. We did not observe any variation in feeding effort due to changes in the level of risk or the proportion of time spent under high-risk conditions. The only significant effect was found when the attack ratio was altered: the foraging effort of voles was higher in the treatment with a low attack ratio than in the treatment with a high attack ratio. Thus the results did not support the predation risk allocation hypothesis and we question the applicability of the hypothesis to our study system. We argue that the deviation between the observed pattern of feeding behaviour of bank voles and that predicted by the predation risk allocation hypothesis was mostly due to the inability of voles to accurately assess the changes in the level of risk. However, we also emphasise the difficulties of testing hypotheses under outdoor conditions and with mammals capable of flexible behavioural patterns.

WEASELS’ (MUSTELA NIVALIS NIVALIS) PREFERENCE FOR OLFACTORY CUES OF THE VOLE (CLETHRIONOMYS GLAREOLUS)

Many studies on life history strategies of small mammals under predation risk are based on assumptions that mammalian predators use scent marking from prey in searching and hunting. This is especially true for small mustelids hunting in the tunnels and cavities of their prey. It is assumed that weasels use the estrous signs of female voles as hunting cues, which exposes such females to a more pronounced risk of predation. We studied the preferences of 57 least weasels (Mustela nivalis nivalis) toward odor cues from four different reproductive categories of the bank vole (Clethrionomys glareolus). In the first experiment, weasels selected clearly for vole odors over clean bedding in a Y-maze arena. The second experiment demonstrated that there was no difference in weasel preference between estrous and pregnant or lactating females. Thirdly, there was no preference for odors from dominant vs. subordinate males. Finally, we offered weasels a dyadic choice between olfactory signs of six possible combinations ...

A New GPS–GSM-Based Method to Study Behavior of Brown Bears

Abstract We report a new method of studying brown bear (Ursus arctos) behavior. The method combines the technologies of Global Positioning Systems (GPS) and Global System for Mobile Communication (GSM). A GPS–GSM collar on a bear locates itself with the help of a GPS module, while the GSM module sends the location information to the researcher as SMS (short) message via a GSM mobile phone network. The collar is interactive and can receive SMS commands, for instance, to adjust the interval at which location information is transmitted. We tested the method in experiments in which people equipped with GPS–GSM mobile phones approached a GPS–GSM-collared bear. Spatial locations of the bear and the approaching persons are displayed on the digital map on the computer screen in real-time. The dispersion of spatial information was 2.5 m, and the success rate in the experiments was 81.2% (new spatial locations successfully received when requested). The method proved to be useful and accurate enough to study the behavior of bears (e.g., escape initiation distance) in the proximity of humans. We believe the methodology presented will help researchers to better understand bear behavior and develop strategies to minimize negative bear–human interactions. Rapid data transmission creates new opportunities for animal tracking in general. We believe that the GPS mobile phone-based tracking will become the most cost-effective method for studying large animals in areas serviced by mobile phone networks.

Behaviour and choice of refuge by voles under predation risk

Animals often show a strong antipredatory response when they are exposed to their most deadly predator. In northern vole populations, the least weasel, Mustela nivalis nivalis, is probably the most important predator of voles. Because of its small size and slender body shape, the least weasel is capable of hunting voles in their burrows. However, small voles can potentially escape weasel predation by selecting holes smaller than those weasels can enter. We studied the choice of nest holes and refuges by two species of voles under simulated predation risk. In a laboratory experiment, voles were provided with four nest boxes as refuges, with individually adjusted entrance sizes. When exposed to the odour of a weasel, voles did not choose the smallest opening; they rather seemed to trade full protection for easy and immediate access by choosing the nest box with an intermediate entrance size. When outside the nest at the time when a weasel entered the arena, voles avoided the refuges with the smallest holes. In addition to using refuges on ground level, voles climbed on top of the boxes as an escape reaction, as well as exhibiting a variety of behavioural responses, such as fast running, freezing and sneaking.

SPACE USE, CIRCADIAN ACTIVITY PATTERN, AND MATING SYSTEM OF THE NOCTURNAL TREE RAT THALLOMYS NIGRICAUDA

Abstract We present results of a radiotracking study of the black-tailed tree rat Thallomys nigricauda, based on 3 males and 4 females in the breeding season and 2 males and 5 females in the nonbreeding season. The study was conducted in the southern Kalahari thornveld, South Africa, a savanna landscape of acacia trees and patchy acacia bush. Nocturnal activity patterns, vegetation use, space use, and interactions were followed for 8–17 days. During the breeding season, males were active with 2 synchronous activity peaks shortly after sunset and late at night. Home ranges included the nests of 8–10 females, 6 different daytime resting places, and 3–5 areas of high activity. Males were mobile within home ranges of 5–10 ha (90% minimal convex polygons) that overlapped with other males and covered home ranges of several females. Activity of females was high shortly after sunset and before sunrise with 6 h of low activity between. Home ranges of nursing females were 0.001–0.03 ha and included 2 small areas of high activity (nest and foraging site) where no other adult females were observed. Animals preferred small acacia shrubs (Acacia mellifera, A. luederitzi) for foraging. During the nonbreeding season, activity of both sexes was low, with only 1 peak shortly after sunset. Although small acacia shrubs did not have foliage, they were preferred by both sexes for foraging, and rats were observed feeding on buds. Home-range size of males was 1–2 ha and of females was 0.1–0.3 ha. Contrary to earlier reports, we found tree rats living solitarily or with young offspring. We suggest that the species has a promiscuous mating system.

Spatio‐temporal patterns of habitat use in voles and shrews modified by density, season and predators

1. Although the intrinsic habitat preferences of a species can be considered to be fixed, the realized habitat use depends on the prevailing abiotic and biotic conditions. Often the core habitats are occupied by dense and stable populations, while marginal habitats become occupied only at times of high density. In a community of interacting species, habitat uses of different species become inter-related, for example an increased density of a strong competitor forcing a weaker competitor to use more marginal habitats. 2. We studied the spatio-temporal distribution patterns of three common small mammal species, the bank vole Myodes glareolus; the field vole Microtus agrestis; and the common shrew Sorex araneus, in a 4-year trapping study carried out on six large islands, each containing a mixture of three main habitat types (forest, field and clear-cut). We experimentally released least weasels (Mustela n. nivalis) to some of the islands to see how the focal species respond to increased predation pressure. 3. Both vole species were largely restricted to their core habitats (bank voles to forests and field voles to fields) at times of low population density. With increasing density, the relative habitat use of both species increased in the clear-cut areas. The common shrew was a generalist in its habitat use at all population densities. 4. The release of the weasels changed the habitat use of all study species. 5. The vole species showed a stronger aggregated pattern than the common shrew, especially at low population density. The vole aggregations remained in the same localities between seasons, except in the case of bank voles after the weasels were released. 6. Bank voles and field voles avoided each other at high density. 7. We conclude that intrinsically differential habitat requirements and flexibility to modify habitat use facilitate the coexistence of the two competing vole species in mosaic landscapes consisting of boreal forests and open habitats.

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.

Predator-vole interactions in Northern Europe: the role of small mustelids revised.

The cyclic population dynamics of vole and predator communities is a key phenomenon in northern ecosystems, and it appears to be influenced by climate change. Reports of collapsing rodent cycles have attributed the changes to warmer winters, which weaken the interaction between voles and their specialist subnivean predators. Using population data collected throughout Finland during 1986–2011, we analyse the spatio-temporal variation in the interactions between populations of voles and specialist, generalist and avian predators, and investigate by simulations the roles of the different predators in the vole cycle. We test the hypothesis that vole population cyclicity is dependent on predator–prey interactions during winter. Our results support the importance of the small mustelids for the vole cycle. However, weakening specialist predation during winters, or an increase in generalist predation, was not associated with the loss of cyclicity. Strengthening of delayed density dependence coincided with strengthening small mustelid influence on the summer population growth rates of voles. In conclusion, a strong impact of small mustelids during summers appears highly influential to vole population dynamics, and deteriorating winter conditions are not a viable explanation for collapsing small mammal population cycles.