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 chromatography-mass spectrometry, we identified that 1-octanol, 2-octanone, and one unknown compound as the most likely candidates to function as alarm signals. These compounds were independent of the vole's sex. In a field experiment, voles were foraging less, i.e. they were more afraid in the AP odour foraging trays during the first day, as the odour was fresh, than in the second day. This verified the short lasting effect of volatile APs. Our results clarified the chemistry of alarming body odour compounds in mammals, and enhanced our understanding of the ecological role of AP and chemical communication in mammals.

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

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.

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.

Interspecific information on predation risk affects nest site choice in a passerine bird.

BACKGROUND: Breeding site choice constitutes an important part of the species niche. Nest predation affects breeding site choice, and has been suggested to drive niche segregation and local coexistence of species. Interspecific social information use may, in turn, result in copying or rejection of heterospecific niche characteristics and thus affect realized niche overlap between species. We tested experimentally whether a migratory bird, the pied flycatcher Ficedula hypoleuca, collects information about nest predation risk from indirect cues of predators visiting nests of heterospecific birds. Furthermore, we investigated whether the migratory birds can associate such information with a specific nest site characteristic and generalize the information to their own nest site choice. RESULTS: Our results demonstrate that flycatchers can use the fate of heterospecific nesting attempts in their own nest site choice, but do so selectively. Young flycatcher females, when making the decision quickly, associated the fate of an artificial nest with nest-site characteristics and avoided the characteristic associated with higher nest predation risk. CONCLUSIONS: Copying nest site choices of successful heterospecifics, and avoiding choices which led to failed attempts, may amplify or counter effects of nest predation on niche overlap, with important consequences for between-species niche divergence-convergence dynamics, species coexistence and predator-prey interactions.

The Bruce effect revisited: is pregnancy termination in female rodents an adaptation to ensure breeding success after male turnover in low densities?

Pregnancy termination after encountering a strange male, the Bruce effect, is regarded as a counterstrategy of female mammals towards anticipated infanticide. While confirmed in caged rodent pairs, no verification for the Bruce effect existed from experimental field populations of small rodents. We suggest that the effect may be adaptive for breeding rodent females only under specific conditions related to populations with cyclically fluctuating densities. We investigated the occurrence of delay in birth date after experimental turnover of the breeding male under different population composition in bank voles (Myodes glareolus) in large outdoor enclosures: one-male-multiple-females (n = 6 populations/18 females), multiple-males-multiple-females (n = 15/45), and single-male-single-female (MF treatment, n = 74/74). Most delays were observed in the MF treatment after turnover. Parallel we showed in a laboratory experiment (n = 205 females) that overwintered and primiparous females, the most abundant cohort during population lows in the increase phase of cyclic rodent populations, were more likely to delay births after turnover of the male than year-born and multiparous females. Taken together, our results suggest that the Bruce effect may be an adaptive breeding strategy for rodent females in cyclic populations specifically at low densities in the increase phase, when isolated, overwintered animals associate in MF pairs. During population lows infanticide risk and inbreeding risk may then be higher than during population highs, while also the fitness value of a litter in an increasing population is higher. Therefore, the Bruce effect may be adaptive for females during annual population lows in the increase phases, even at the costs of delaying reproduction.

Excretion and measurement of corticosterone and testosterone metabolites in bank voles (Myodes glareolus).

The bank vole is a commonly used model species in behavioral and ecophysiological studies. Thus, presenting a validated method for noninvasive monitoring of corticosterone and testosterone secretion is of high relevance. Here, we evaluated the effect of time of day and an ACTH challenge test on measured fecal corticosterone (FCM) and testosterone (FTM) metabolites in both sexes. Furthermore, we performed radiometabolism experiments for both steroids and sexes to study metabolism and excretion of 3H-corticosterone and 3H-testosterone. FCM and FTM were analysed with a 5α-pregnane-3ß,11ß,21-triol-20-one enzyme immunoassay (EIA) and a testosterone (measuring 17ß-hydroxyandrostanes) EIA, respectively. Males had significantly higher FCM levels than females and their main excretion route was via the feces (∼72%), whereas females excreted nearly equal portions in both feces and urine. For testosterone the main excretion route was via the feces in both sexes (∼80%). The time course of excretion was similar in both sexes, but for the first time a significant difference between injected steroids was found: Corticosterone was excreted faster than testosterone, both in urine (median of peak levels: 4h vs 6h) and feces (6h vs 8h). Several metabolites were present in the feces and the tested EIAs reacted with some of them. Time of day had a significant effect on measured fecal steroid metabolites. As expected, males had significantly higher FTM levels than females. ACTH administration significantly increased FCM values; peaks were observed 4-8h after injection. In conclusion, both tested EIAs proved suited for a noninvasive measurement of glucocorticoids and androgens in bank voles.

Summer time predation on the obligatory off-host stage of an invasive ectoparasite.

Predation can regulate populations and strongly affect invasion success of novel prey. The deer ked (Lipoptena cervi; Linnaeus 1758) is an invasive ectoparasite of cervids that spends a long period of its life cycle outside the host. Prior to this study, virtually nothing was known about natural summer time predation on the deer ked. We aimed to evaluate the magnitude of summer time predation on L. cervi pupae in different habitats and to identify potential predators. We conducted a set of field experiments, where we exposed L. cervi pupae to various ground-dwelling vertebrate and invertebrate predators. The loss of pupae was monitored for different predator guilds. Three habitats of the moose, the main host species, were studied: (1) moist heath forest; (2) dry, logged heath forest; and (3) moist meadow. The results indicate notable summer time predation on L. cervi pupae, and the pupal predation varied within and between habitats, being lowest in the meadow habitat. We found a positive correlation between pupal loss and abundance of the common lizard (Zootoca vivipara), harvestmen (Opiliones), ground spiders (Gnaphosidae) and Formicinae-ants. We conclude that summer time predation during the pupal phase can have a notable local importance for the L. cervi abundance.

Passive sinking into the snow as possible survival strategy during the off-host stage in an insect ectoparasite.

Abiotic and biotic factors determine success or failure of individual organisms, populations and species. The early life stages are often the most vulnerable to heavy mortality due to environmental conditions. The deer ked (Lipoptena cervi Linnaeus, 1758) is an invasive insect ectoparasite of cervids that spends an important period of the life cycle outside host as immobile pupa. During winter, dark-coloured pupae drop off the host onto the snow, where they are exposed to environmental temperature variation and predation as long as the new snowfall provides shelter against these mortality factors. The other possible option is to passively sink into the snow, which is aided by morphology of pupae. Here, we experimentally studied passive snow sinking capacity of pupae of L. cervi. We show that pupae have a notable passive snow sinking capacity, which is the most likely explained by pupal morphology enabling solar energy absorption and pupal weight. The present results can be used when planning future studies and when evaluating possible predation risk and overall survival of this invasive ectoparasite species in changing environmental conditions.

Acute impacts of the deer ked (Lipoptena cervi) infestation on reindeer (Rangifer tarandus tarandus) behaviour.

Blood-sucking ectoparasites have often a strong impact on the behaviour of their hosts. The annual insect harassment of reindeer (Rangifer tarandus tarandus) has increased in the southern part of the Finnish reindeer herding area because of the recent invasion of a blood-feeding ectoparasitic louse-fly, the deer ked (Lipoptena cervi). We studied the impact of the deer ked on the behaviour of reindeer. Twelve reindeer were infested with a total of 300 keds/reindeer on six occasions in a 5-week period during the deer ked flight season in autumn, while six non-infested reindeer were used as controls. Behavioural patterns indicating potential stress were monitored by visual observation from August to December. The infested reindeer displayed more incidences of restless behaviour than the controls. Shaking and scratching were the most common forms of restless behaviour after infestation of deer keds. Increased grooming was also observed after the transplantation and also later, 1 month after the infestation. Based on the results, the deer ked infestation can cause acute behavioural disturbance in reindeer and, thus, could pose a potential threat to reindeer welfare. Antiparasitic treatment with, e.g. ivermectin, may increase the welfare of parasitized reindeer by reducing deer keds. If the deer ked infestation intensity on the reindeer herding area increases and restless behaviour of reindeer becomes more common, the present results can help in further evaluation of the duration and magnitude of behavioural changes.

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.

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.

Does personality in small rodents vary depending on population density?

Personality means an individual's unique way of behaving and reacting to the environment. It is a stable and heritable trait, which is expressed consistently in different situations. The aim of our study was to develop novel tests to depict the personality structure of the bank vole Myodes glareolus, and to determine if the phase of the population cycle, i.e. population density, affects personality. We focused on some central aspects of bank vole behaviour: mobility, risk taking, exploratory behaviour, dominance, and aggressive behaviour towards pups. These behaviours were chosen because they directly affect bank vole survival or fitness or are classified as important factors of personality in other species. In total, 192 males from different populations went through four behavioural tests, in which 20 variables were measured. The tests were repeated after 3 weeks, which verified that all traits were stable, i.e. repeatable between trials. Three personality compounds emerged, named extroversion, novelty seeking and infanticide. Extroversion included dominance and mobility, while novelty seeking consisted of risk taking and exploration. Infanticide encompassed all indices measuring harmful behaviour towards pups. Mobility and dominance were connected, possibly because both seem to depend on condition. Time spent in captivity increased extroversion, which may be explained by good food, stable conditions and acclimation to strong social cues. Novelty seeking was connected to repeatability which could mean that novelty avoiding individuals adjust their behaviour to match new environments. Population density affected the infanticide trait but not novelty seeking or extroversion.

Breeding state and season affect interspecific interaction types: indirect resource competition and direct interference.

Indirect resource competition and interference are widely occurring mechanisms of interspecific interactions. We have studied the seasonal expression of these two interaction types within a two-species, boreal small mammal system. Seasons differ by resource availability, individual breeding state and intraspecific social system. Live-trapping methods were used to monitor space use and reproduction in 14 experimental populations of bank voles Myodes glareolus in large outdoor enclosures with and without a dominant competitor, the field vole Microtus agrestis. We further compared vole behaviour using staged dyadic encounters in neutral arenas in both seasons. Survival of the non-breeding overwintering bank voles was not affected by competition. In the spring, the numbers of male bank voles, but not of females, were reduced significantly in the competition populations. Bank vole home ranges expanded with vole density in the presence of competitors, indicating food limitation. A comparison of behaviour between seasons based on an analysis of similarity revealed an avoidance of costly aggression against opponents, independent of species. Interactions were more aggressive during the summer than during the winter, and heterospecific encounters were more aggressive than conspecific encounters. Based on these results, we suggest that interaction types and their respective mechanisms are not either-or categories and may change over the seasons. During the winter, energy constraints and thermoregulatory needs decrease direct aggression, but food constraints increase indirect resource competition. Direct interference appears in the summer, probably triggered by each individual's reproductive and hormonal state and the defence of offspring against conspecific and heterospecific intruders. Both interaction forms overlap in the spring, possibly contributing to spring declines in the numbers of subordinate species.

Geographical variation in host use of a blood-feeding ectoparasitic fly: implications for population invasiveness.

Invasive generalist ectoparasites provide a tool to study factors affecting expansion rates. An increase in the number of host species may facilitate geographic range expansion by increasing the number of suitable habitats and by affecting local extinction and colonization rates. A geographic perspective on parasite host specificity and its implications on range expansion are, however, insufficiently understood. We conducted a field study to explore if divergent host specificity could explain the observed variation in expansion rates between Fennoscandian populations of the deer ked (Lipoptena cervi), which is a blood-feeding ectoparasitic fly of cervids. We found that the rapidly expanding eastern population in Finland appears to specialize on moose, whereas the slowly expanding western population in Norway breeds successfully on both moose and roe deer. The eastern population was also found to utilize the wild forest reindeer as an auxiliary host, but this species is apparently of low value for L. cervi in terms of adult maintenance, reproductive output and offspring quality. Abundant numbers of roe deer and white-tailed deer were observed to be apparently uninfected in Finland, suggesting that host use is not a plastic response to host availability, but rather a consequence of population-level evolutionary changes. Locally compatible hosts were found to be the ones sharing a long history with the deer ked in the area. Cervids that sustained adult deer keds also allowed successful reproduction. Thus, host use is probably determined by the ability of the adult to exploit particular host species. We conclude that a wide host range alone does not account for the high expansion rate or wide geographic distribution of the deer ked, although loose ecological requirements would increase habitat availability.

Northward invasion of the parasitic deer ked ( Lipoptena cervi), is there geographical variation in pupal size and development duration?

The deer ked (Lipoptena cervi) is a common ectoparasite of cervids. During the last decades the species has rapidly invaded in northern Europe, especially in Finland, towards the north and increased its prevalence on the moose population. Consequently, during this rapid invasion the deer ked has faced more severe climatic conditions. We studied whether pupal size (measured as pupal weight) and pupal development duration of the deer ked varies along historical invasion zones and temperature zones towards north in Finland. Moreover, we explored possible size- and gender-dependent variation in pupal development duration. We divided wild-collected pupae in respect to their origin in two ways: (1) temperature zones (from south-west to colder north-east) and (2) invasion history (from early to late establishment). We reared pupae in the controlled laboratory conditions in identical temperature and light conditions. Pupal size decreased towards north and the smaller pupae developed faster. However, the results do not show differences in pupal size or developmental characteristics between the invasion zones. This supports the idea of rapid developmental plasticity of the deer ked and that not the invasion history but the current temperature regime determines the life history of the deer ked when invading towards a colder environment.

Loss of density-dependence and incomplete control by dominant breeders in a territorial species with density outbreaks.

BACKGROUND: A territory as a prerequisite for breeding limits the maximum number of breeders in a given area, and thus lowers the proportion of breeders if population size increases. However, some territorially breeding animals can have dramatic density fluctuations and little is known about the change from density-dependent processes to density-independence of breeding during a population increase or an outbreak. We suggest that territoriality, breeding suppression and its break-down can be understood with an incomplete-control model, developed for social breeders and social suppression. RESULTS: We studied density dependence in an arvicoline species, the bank vole, known as a territorial breeder with cyclic and non-cyclic density fluctuations and periodically high densities in different parts of its range. Our long-term data base from 38 experimental populations in large enclosures in boreal grassland confirms that breeding rates are density-regulated at moderate densities, probably by social suppression of subordinate potential breeders. We conducted an experiment, were we doubled and tripled this moderate density under otherwise the same conditions and measured space use, mortality, reproduction and faecal stress hormone levels (FGM) of adult females. We found that mortality did not differ among the densities, but the regulation of the breeding rate broke down: at double and triple densities all females were breeding, while at the low density the breeding rate was regulated as observed before. Spatial overlap among females increased with density, while a minimum territory size was maintained. Mean stress hormone levels were higher in double and triple densities than at moderate density. CONCLUSIONS: At low and moderate densities, breeding suppression by the dominant breeders, But above a density-threshold (similar to a competition point), the dominance of breeders could not be sustained (incomplete control). In our experiment, this point was reached after territories could not shrink any further, while the number of intruders continued to increase with increasing density. Probably suppression becomes too costly for the dominants, and increasing number of other breeders reduces the effectiveness of threats. In wild populations, crossing this threshold would allow for a rapid density increase or population outbreaks, enabling territorial species to escape density-dependency.

Polyandry enhances offspring survival in an infanticidal species.

The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus. Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing but sperm, but commit infanticide, can gain non-genetic fitness benefits from polyandry.

Fennoscandian distribution of an important parasite of cervids, the deer ked (Lipoptena cervi), revisited.

The deer ked [Lipoptena cervi (L. 1758) (Dipt., Hippoboscidae)] is a blood-sucking ectoparasite of cervids. The species has been resident in Sweden for more than two centuries, whereas in Finland ( approximately 50 years) and Norway ( approximately 30 years), it has established itself relatively recently. L. cervi may cause serious health problems in its natural hosts, act as a vector for zoonotic diseases, and pose a socioeconomic threat to forest-based activity. In this paper, we review the distribution and former expansion of the species in Fennoscandia. The current distribution of L. cervi appears bimodal, and the geographical range expansion of the species shows notable differences across Fennoscandia. The western population in Norway and Sweden has its northern edge of range at respective latitudes of 61 degrees N and 62 degrees N, whereas the eastern population in Finland reaches 65 degrees N. The future expansion of L. cervi is dependent on several interdependent extrinsic and intrinsic factors. International multidisciplinary collaboration is needed to achieve a synthesis on the factors affecting expansion rates and to understand the effects of L. cervi on wildlife, human health, and the rural societies of Fennoscandia.

Monitoring of ticks and tick-borne pathogens through a nationwide research station network in Finland.

In 2015 a long-term, nationwide tick and tick-borne pathogen (TBP) monitoring project was started by the Finnish Tick Project and the Finnish Research Station network (RESTAT), with the goal of producing temporally and geographically extensive data regarding exophilic ticks in Finland. In the current study, we present results from the first four years of this collaboration. Ticks were collected by cloth dragging from 11 research stations across Finland in May-September 2015-2018 (2012-2018 in Seili). Collected ticks were screened for twelve different pathogens by qPCR: Borrelia afzelii, Borrelia garinii, Borrelia valaisiana, Borrelia burgdorferi sensu stricto, Borrelia miyamotoi, Babesia spp., Anaplasma phagocytophilum, Rickettsia spp., Candidatus Neoehrlichia mikurensis, Francisella tularensis, Bartonella spp. and tick-borne encephalitis virus (TBEV). Altogether 15 067 Ixodes ricinus and 46 Ixodes persulcatus were collected during 68 km of dragging. Field collections revealed different seasonal activity patterns for the two species. The activity of I. persulcatus adults (only one nymph detected) was unimodal, with activity only in May-July, whereas Ixodes ricinus was active from May to September, with activity peaks in September (nymphs) or July-August (adults). Overall, tick densities were higher during the latter years of the study. Borrelia burgdorferi sensu lato were the most common pathogens detected, with 48.9 ±â€¯8.4% (95% Cl) of adults and 25.3 ±â€¯4.4% of nymphs carrying the bacteria. No samples positive for F. tularensis, Bartonella or TBEV were detected. This collaboration project involving the extensive Finnish Research Station network has ensured enduring and spatially extensive, long-term tick data collection to the foreseeable future.