Polyandrous females produce sons that are successful at post-copulatory competition.

Some of the genetic benefit hypotheses put forward to explain multiple male mating (polyandry) predict that sons of polyandrous females will have an increased competitive ability under precopulatory or post-copulatory competition via paternally inherited traits, such as attractiveness or fertilization efficiency. Here, we tested these predictions by comparing the competitive ability of sons of experimentally monandrous and polyandrous female bank voles (Myodes glareolus), while controlling for potential material and maternal effects. In female choice experiments, we found no clear preference for sons of either monandrous or polyandrous mothers. Moreover, neither male type was dominant over …

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 …

Reply from H. Ylönen

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-3β,11β,21-triol-20-one enzyme immunoassay (EIA) and a testosterone (measuring 17β-hydroxyandrostanes) EIA, respect…

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…

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…

WHO BEARS THE COSTS OF INTERSPECIFIC COMPETITION IN AN AGE-STRUCTURED POPULATION?

Social and density-dependent life history processes may differ according to age and the reproductive history of individuals. Arvicoline rodents have a typical, season-dependent, bimodal, age distribution of breeding individuals within a population. This distribution may influence population fluctuations. In this study, we measured effects of interspecific competition from field voles (Microtus agrestis) on various fitness components of female bank voles (Clethrionomys glareolus) in an age-structured breeding population in large (0.25 ha) outdoor enclosures. We monitored survival, reproduction, and space use of experimental bank vole populations with females from two different age groups. Wi…

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

Abstract 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 terri…

Infanticide and effectiveness of pup protection in bank voles: does the mother recognise a killer?

Infanticide, the killing of conspecific young, has been documented in numerous species of mammals, especially rodents. In that infanticide is costly to the victim mother, natural selection should favour counter-strategies by females to protect their pups. We studied the frequency of infanticide by male and female bank voles (Clethrionomys glareolus) and the effectiveness of dams in recognising and deterring infanticide. In trials in which unprotected pups were exposed to voles of both sexes, one third of male and female intruders killed pups. When mothers were present at the nest site, not a single female and only 2 of 25 males were able to commit infanticide. Females acted aggressively tow…

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…

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 p…

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 sp…

Changing female spacing behaviour and demography in an enclosed breeding population of Clethrionomys glareolus

The social organization of Clethrionomys glareolus Schreber was studied by live trapping in an enclosure of 0.8 ha in Central Finland between the years 1982–1986. The enclosure consisted of three habitats: abandoned field, brushwood, and moist spruce heath forest. The population density increased from 50 voles ha−1 in 1982 and 1983 to 150 ha−1 in 1984 and 1985. In the summer of 1986 the population crashed to almost zero. In the summer of 1984 after winter breeding the number of breeding females grew to 22 compared with 6–7 in previous years. In 1984 the mature females changed from territorial to group behaviour. During the high population density in 1984 and 1985 breeding stopped already in…

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…

Infanticide and Population Growth in the Bank Vole (Myodes glareolus): The Effect of Male Turnover and Density

One major intrinsic factor affecting recruitment of young into a population is infanticide, the killing of conspecific young by adult males. It occurs in most mammal species, like our study species the bank vole (Myodes glareolus), and is widely accepted as an adaptive behavior, which may increase male fitness via nutritional gain, decreased competition, or an increased access to mates. A turnover of males in a population increases the risk of infanticide owing to a disruption of social structures. In a controlled field study, we tested the effects of total male turnover and density on juvenile recruitment and female space use in experimental bank vole populations. Juvenile recruitment decl…

Les histoires de vie chez les mammifères : Les bases revisitées

Avian predation on a parasitic fly of cervids during winter: can host-related cues increase the predation risk?

The deer ked (Lipoptena cervi) is an ectoparasitic fly on cervids that has expanded its distribution rapidly in Northern Europe. However, the regulating biotic factors such as predation remain unknown. The host-independent pupal stage of the fly lasts for several months. Blackish pupae are visible against snow, especially on the bedding sites of hosts, and are thus exposed to predators. To evaluate the role of predation on the invasion dynamics and evolution of L. cervi, we monitored pupal predation on artificial bedding sites in three geographical areas in Finland during winter. We explored: (1) possible predators; (2) magnitude of predation; and (3) whether predation risk is affected by h…

Coat darkness is associated with social dominance and mating behaviour in a mountain sheep hybrid lineage

Natural hybridization can produce novel traits when morphologically different populations hybridize, and can introduce variation in traits that become associated with sexual selection. Evidence from breeding experiments and genetic markers indicate that the great variation in coat darkness and the unique coat patterns found in Stone's sheep Ovis dalli stonei, populations, have resulted from an ancient hybridization event between thinhorn sheep, O. dalli, and bighorn sheep, O. canadensis. Behavioural evidence gathered in 2003 and 2004 in Yukon Territory, Canada, showed that higher dominance rank was correlated with increasing darkness in rams, and comparatively darker rams were seen more oft…

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

SUMMARYPredation 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 onL. cervipupae in different habitats and to identify potential predators. We conducted a set of field experiments, where we exposedL. cervipupae to various ground-dwelling vertebrate and invertebrate predators. The loss of pupae was monitored for different predator guilds. Three habitats of the…

Predation risk and reproduction in the bank vole

Context Life-history strategies are the means that organisms use to achieve successful reproduction in environments that vary in time and space. Individual animals maximise life-time reproductive success (LRS) through optimal timing of reproduction and investment in offspring. A crucial factor affecting LRS is predation risk in a highly seasonal environment. According to the breeding-suppression hypothesis (BSH), females should delay breeding under short periods of high predation risk. Delayed breeding under risk is suggested to have substantial consequences for females’ fitness. Aims We tested the BSH in an iteroparous boreal small rodent, the bank vole, Myodes glareolus. Methods We used …

Otter Lutra lutra predation on farmed and free‐living salmonids in boreal freshwater habitats

In this paper we aim to define whether fish farms or stocked trout streams substantially contribute to the diet of otters Lutra lutra living in freshwater habitats of Mid-Finland. Diet was assessed using spraint analysis. We especially focused on areas with fish farms and stocked trout Salmo trutta streams (salmonid-rich habitat) and used ‘normal’ (salmonid-poor) habitats as control. Frequency of salmonid remains in spraints was significantly higher in salmonid-rich habitats than elsewhere in all seasons, the difference increasing from summer to winter. In salmonid-rich habitats, however, salmonid consumption was not strongly seasonal. Data from spraint collection indicated a shift in activ…

Who eats first? Uptake of pellet bait by target and non-target species

House mice (Mus domesticus) are an important vertebrate pest in Australian agriculture. We studied the uptake of non-toxic placebo bait pellets targeted on house mice from bait stations in the grain-growing region of southeastern Australia. Bait stations allowed access for either ants; ants and mice or ants, mice, and birds. Soy meal bait pellets offered in December were of low preference for both ants and mice, but were eaten by birds in one study plot. In January, there were no differences between bait stations in the amount of wheat bait pellets removed indicating that the pellet bait had been primarily removed by ants. Most pellet bait was removed during the first 12 h after distributio…

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…

Predation risk allocation or direct vigilance response in the predator interaction between perch (Perca fluviatilis L.) and pike (Esox lucius L.)?

Predation risk allocation hypothesis predicts that a prey's response to predator depends on prey's previous experience on predator. Here we tested whether the group of three perch respond differentially to pike, predator of perch, depending on the timing of high constant (HC) and high unpredictable (HU) risk periods within low constant risk periods in short-term (10 h) experiments, and whether the response is stronger during a HU risk period than during a HC risk period. Perch clearly erected the dorsal fin in response to predation risk treatments (pike odour only, odour and visible pike). Decrease in activity and increase in shoaling behaviour were observed mainly during high risk periods.…

Variable mode of estrus affects female decision for multiple mating

Investigating patterns of variation in mating strategies may shed light on their evolutionary importance as well as their impact on the strength and shape of sexual selection. Multimale mating (polyandry) and mate choice are intensely studied subjects in the area of sexual selection, but little is known about intraspecific patterns of variation that may respond to dynamic cost-benefit balances. In a laboratory study, we investigated the mating behavior of female bank voles (Myodes glareolus) with distinctly different time and energy budgets: They were either in cycling estrus (CE) or postpartum estrus (PPE) shortly after delivery. Postpartum mating is highly constrained by time and energy d…

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…

Is Mating Alone Enough to Inhibit Infanticide in Male Bank Voles?

Infanticide, the killing of conspecific young, is commonly recognized as an adaptive behavioural strategy enhancing the fitness of the perpetrator. Infanticide is supposed to be inhibited in several male rodent species after mating with a time lag to the time when perpetrators own offspring would be born. This is because males with no parental care do not recognize their own offspring. It has been suggested that copulation alone is enough to inhibit infanticidal behaviour in male rodents. Infanticidal behaviour occurs in more than 50% of male bank voles (Myodes glareolus), and offspring loss because of infanticide may have a great effect on breeding success and population recruitment. In a …

Social overwintering and food distribution in the bank vole Clethrionomys glareolus

We studied overwintering in the bank vole Clethrionomys glareolus in four 0.5 ha enclosures in an abandoned field in central Finland in the winter 1987/88. In two of the enclosures food was offered evenly distributed over the whole enclosed area (Even Enclosures = EE), in the two others food was offered in one feeding patch with four feeding chambers 2 m apart (Patchy Enclosures = PE). Food was provided in about the same amount in both enclosures. The experiment commenced in early October, with 13 females and 11 males in EEs and 12 + 13 voles in PEs. After two months the voles in the PEs were concentrated around the feeding patches. Territoriality was not observed in EEs, instead the voles …

Density dependence of infanticide and recognition of pup sex in male bank voles

[Infanticide — the killing of conspecific young — is a common phenomenon in many invertebrate and vertebrate species, particularly common in rodents. It can increase juvenile mortality and, thus, affect population growth. Male infanticide is explained by adaptive hypotheses based on sexual selection. Removing future competitors for mating opportunities would require recognition of pup sex and directing infanticide against male pups. We studied whether the sex of a pup and population density affect male bank voles' ( Myodes glareolus ) aggressive behaviour towards conspecific pups. Population density increased aggressiveness. Against our predictions, male bank voles from high density populat…

Reproductive costs and litter size in the bank vole.

The potential reproductive costs for free-ranging bank vole (Clethrionomys glareolus) offspring and mothers were assessed by manipulating litter size and by determining the effects of nursing varied numbers of offspring. Litter enlargement did not increase the number of weanlings per mother. The mass of juveniles was significantly lower in the enlarged litters and higher in the reduced litters, compared to the control group. However, the survival of juveniles from weaning aged three months did not depend on their mass at weaning. Data from a previous study (Mappes et al. 1995) indicated that a higher mass at weaning may increase juveniles' abilities to maturate and breed during their summer…

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…

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

SUMMARYThe 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 …

Female bank voles ( Clethrionomys glareolus ) prefer dominant males; but what if there is no choice?

Both intra-sexual competition between males and female mate choice have been found to affect mating behaviour in rodents. We studied female choice in the bank vole (Clethrionomys glareolus) under circumstances where male-male competition was excluded and the female could interact and mate freely with the males. Mating behaviour was observed in two situations: (1) the female encountered two males with a clear dominance relationship; and (2) the two males were equal in their social status. In all tests where a female in postpartum oestrus had a choice between males of different social rank she mated with the dominant one. When choosing between an even pair of males there was no difference in …

Fungal-Mediated Multitrophic Interactions : Do Grass Endophytes in Diet Protect Voles from Predators?

Plant-associated micro-organisms such as mycotoxin-producing endophytes commonly have direct negative effects on herbivores. These effects may be carried over to natural enemies of the herbivores, but this has been rarely explored. We examined how feeding on Neotyphodium endophyte infected (E+) and endophyte free (E−) meadow ryegrass (Scherodonus pratensis) affects body mass, population size and mobility of sibling voles (Microtus levis), and whether the diet mediates the vulnerability of voles to least weasel (Mustela nivalis nivalis) predation. Because least weasels are known to be olfactory hunters, we also examined whether they are able to distinguish olfactory cues of voles fed on E+ a…

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…

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 over…

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…

Experimental infection of the deer ked (Lipoptena cervi) has no negative effects on the physiology of the captive reindeer (Rangifer tarandus tarandus)

The deer ked (Lipoptena cervi) is a haematophagous parasitic fly of cervids that spread to Finland in the early 1960's. Presently its northern distribution limit lies at approximately 65°N and it is gradually spreading northwards. In Finland the principal host species has been the moose (Alces alces), but the deer ked is about to establish contact with another potential host, the semi-domesticated reindeer (Rangifer tarandus tarandus) causing possible threats to reindeer health and management. The aim of this study was to investigate if the deer ked would have an influence on the welfare of the reindeer. Eighteen adult reindeer were divided into three experimental groups: the control group …

Is reproduction really costly? Energy metabolism of bank vole (Clethrionomys glareolus) females through the reproductive cycle

Energetic requirements during reproduction are important determinants of the onset of reproduction and of breeding strategy (e.g., breeding post-partum) and therefore affect female reproductive output in seasonally varying environments. To balance the energetic needs of breeding with energy availability, females must optimize energy allocation between their own energy use and energy allocated to their litter. Here, we studied energetic costs and potential energetic trade-offs of reproduction in female bank voles (Clethrionomys glareolus). We measured energy consumption, i.e., metabolic rates as determined from carbon dioxide production of females either with their pups (breeding unit) to fi…

Different demography of friends and strangers: an experiment on the impact of kinship and familiarity in Clethrionomys glareolus.

We examined demographic effects of familiarity and relatedness in the bank vole Clethrionomys glareolus (Schreber) in four 0.5-ha enclosures in Central Finland. In two enclosures were mature voles which had overwintered together and some of their mature off-spring (hereafter referred to as “Friends”), and in the other two individuals of the same species captured from different localities near the study area (“Strangers”). The experiment lasted from June to September. The populations of Friends reached densities twice as high as those of Strangers with a significantly higher rate of recruitment and survival of the young. This may have been due to mutual familiarity decreasing antagonism towa…

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 …

Phenotypic Flexibility in the Social Organization of Clethrionomys

I review the flexibility of social organization and spacing behavior in Clethrionomys. This review is based on a 6-year comparative study and several experimental studies on cyclic populations of the bank vole, C. glareolus, in Central Finland. The social organization of Clethrionomys populations shows great flexibility during both the breeding and nonbreeding season, and is dependent on habitat patchiness, food availability, Predation, kinship, philopatry, and familiarity between individuals. The first three factors are most important in destabilizing a population, whereas the last three stabilize a population without exhausting its resources. Female territoriality can weaken in a producti…

Horn growth rate and longevity: implications for natural and artificial selection in thinhorn sheep (Ovis dalli).

We used horn measurements from natural and hunted mortalities of male thinhorn sheep Ovis dalli from Yukon Territory, Canada, to examine the relationship between rapid growth early in life and longevity. We found that rapid growth was associated with reduced longevity for sheep aged 5 years and older for both the hunted and natural mortality data sets. The negative relationship between growth rate and longevity in hunted sheep can at least partially be explained by morphologically biased hunting regulations. The same trend was evident from natural mortalities from populations that were not hunted or underwent very limited hunting, suggesting a naturally imposed mortality cost directly or in…

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…

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

Abstract 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 w…

Specialist predator in a multi-species prey community: boreal voles and weasels.

Dissimilar vulnerabilities of different prey types and preferences of predators are factors likely to contribute to community dynamics. This may happen via differential individual properties of prey animals (e.g. vigilance, escape) or via habitat effects making hunting by a predator easier and more rewarding in some habitats, or both. Furthermore, community dynamics may be influenced by predator mediated apparent competition, in which an increase in one prey type has negative effects on another prey type indirectly via the shared predator. We summarize the current knowledge from the field in a model predator-prey system consisting of sympatric boreal vole species and their common specialist…

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…

Mammalian life histories: The basics revisited

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…

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…

Why do female bank voles, Clethrionomys glareolus, mate multiply?

Females of many species actively engage in multiple mating, with either a single male or several males, but the adaptive function of this behaviour is often unclear. We conducted a laboratory experiment on a small mammal species, the bank vole, testing the possible benefits of multiple mating on a female's short-term reproductive success (pregnancy rate, litter size and early postnatal survival). Such benefits may affect a female's fitness either directly or indirectly (genetic benefit). We assigned females to three treatments: a single mating treatment in which females mated once with a single male and two multiple mating treatments in which females mated either twice with a single male or…

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…

Do small mammals prey upon an invasive ectoparasite of cervids?

Predation is often considered an important factor for population regulation and in some cases for the invasion success of prey. Small mammalian predation may be a major force in the population regulation of many ground-dwelling in- vertebrate species. The deer ked (Lipoptena cervi (L., 1758)) is an ectoparasitic fly of cervids. The species has a large distri- bution area and it has relatively rapidly spread in northern Europe during the previous four decades. The factors possibly regulating the distribution and invasion of this fly are poorly known. During the off-host stage of several months, pupae of deer ked are likely exposed to many ground-dwelling predators. To study whether small mam…

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…

Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature.

AbstractThe deer ked (Lipoptena cervi) can fail in its host search. Host search fails when an individual deer ked irreversibly accepts a host unsuitable for its reproduction (e.g. a human) and drops its wings. In northern Europe, the main host of the deer ked is the moose (Alces alces). The deer ked is increasingly causing serious problems for humans (for example, causing deer ked dermatitis) and is considered a threat for the recreational use of forests. The adult deer ked flies in early and mid-autumn to search for a host. Our aims were: (i) to study whether there are ways to avoid deer ked attacks by wearing particular clothing, and (ii) to evaluate deer ked host choice. Using human targ…

Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment

In northern Fennoscandia, microtine rodent populations fluctuate cyclically. The environment of an individual vole can be considered to be predictable when the risks of predation and intra- and interspecific competition change with the cycle, such that both are high during the population highs of voles. The risk of predation is also high during the vole crash. After the crash, the vole population is characterized by low intra- and interspecific competition and low predation pressure. The main predators affecting voles during the crash are the small mustelids, least weasel and stoat. The density of these specialist predators declines drastically during the winter after the vole crash. We stu…

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…

HERITABILITIES OF DOMINANCE-RELATED TRAITS IN MALE BANK VOLES (CLETHRIONOMYS GLAREOLUS)

A number of studies have shown that in several animal species females prefer dominant males as mating partners, but fewer attempts have been made to measure possible indirect benefits of this choice. One reason for this may be that, even though dominance is a widely used concept, the definition of dominance still remains controversial. Furthermore, defining and measuring the heritability of social behaviors is problematic because they are not individual traits but, by definition, involve interactions between at least two individuals. In this study we estimated heritabilities and coefficients of additive genetic variances (CVA) for male traits that are closely associated with dominance and f…

Is the reproductive potential of wild house mice regulated by extrinsic or intrinsic factors?

The regulation of reproductive performance in small mammals may be determined by extrinsic or intrinsic parameters. In a large-scale, replicated field experiment we monitored the seasonal fluctuation in food availability and tested the effects of food addition on the reproductive performance of wild house mice (Mus domesticus) in south-eastern Australia. Ovulation rates and litter size increased during spring and peaked in October/November. Ovulation rate was consistently higher than litter size by approximately 1.2 embryos (19%). None of the extrinsic parameters measured (food quality and quantity, mouse abundance) had an impact on reproductive performance. The addition of food did not pre…

Direct interference or indirect exploitation? An experimental study of fitness costs of interspecific competition in voles

Studies on competing mammalian species in the past have focused mainly on the competitive exclusion of one species from the preferred habitat of the other. Investigations on effects of competition and coexistence on individual fitness are rare. In this study we were able to measure effects of interspecific competition on major fitness components, using a system with two vole species in asymmetric competition. Survival, reproduction and space use of bank vole Clethrionomys glareolus females were monitored in 32 enclosed populations over four replicates of eight parallel run enclosures. Into half of the enclosures we introduced an additional number of field voles Microtus agrestis, a dominant…

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…

Behaviour of cyclic bank voles under risk of mustelid predation: do females avoid copulations?

Mustelid odours have been shown to suppress breeding in captive bank voles (Clethrionomys glareolus) from cyclic populations (Ylonen 1989; Ylonen and Ronkainen 1994). The mechanism behind the suppression is unknown. Based on a series of behavioural trials and breeding experiments with pairs of bank voles in breeding condition, we suggest that the primary cause for breeding suppression is a change in female mating behaviour. Experimental female-male pairs (n=34) exposed to mustelid odour decreased their general activity compared to control pairs (n=34). When encountering males in behavioural trials, females exposed to stoat odour were more aggressive and actively avoided precopulatory behavi…

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 habitat selection of Australian house mice , Mus domesticus , during an incipient plague: desperate behaviour due to food depletion

We studied habitat selection and foraging behaviour of the house mouse (Mus domesticus) related to increasing mouse densities and depleting food resources over the breeding season. The study was conducted during the increase phase of an incipient outbreak of mice in a grain-growing area of southeastern Australia. A 3-year rotation created a mosaic of large paddocks of grain crop, pasture, and fallow. The narrow fence lines between paddocks provide an important stable habitat for the mice. We monitored population densities with live-trapping and habitat preference by measuring giving-up densities (GUD) using artificial food patches. Food patches were established in crop fields, fence lines, …

Molecular detection of Bartonella spp. in deer ked pupae, adult keds and moose blood in Finland

SUMMARYThe deer ked (Lipoptena cervi) is a haematophagous ectoparasite of cervids that harbours haemotrophic Bartonella. A prerequisite for the vector competence of the deer ked is the vertical transmission of the pathogen from the mother to its progeny and transstadial transmission from pupa to winged adult. We screened 1154 pupae and 59 pools of winged adult deer keds from different areas in Finland for Bartonella DNA using PCR. Altogether 13 pupa samples and one winged adult deer ked were positive for the presence of Bartonella DNA. The amplified sequences were closely related to either B. schoenbuchensis or B. bovis. The same lineages were identified in eight blood samples collected fro…

Does quality of winter food affect spring condition and breeding in female bank voles (Clethrionomys glareolus)?

We studied the effects of food supplementation on 16 bank vole populations in spring. We manipulated food quantity and quality in eight populations that were enclosed and eight other populations th...

Predator odor recognition and antipredatory response in fish: does the prey know the predator diel rhythm?

We studied in a laboratory experiment using stream tanks if two percid prey fish, the perch (Perca fluviatilis) and the ruffe (Gymnocephalus cernuus), can recognize and respond to increased predation risk using odors of two piscivores, the pike (Esox lucius) and the burbot (Lota lota). Burbot is night-active most of the year but pike hunts predominantly visually whenever there is enough light. Perch is a common day-active prey of pike and dark-active ruffe that of burbot. We predicted that besides recognizing the predator odors, the prey species would respond more strongly to odors of the predator which share the same activity pattern. Both perch and ruffe clearly responded to both predator…

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…

Costs of coexistence along a gradient of competitor densities: an experiment with arvicoline rodents

Summary 1 Costs of coexistence for species with indirect resource competition usually increase monotonically with competitor numbers. Very little is known though about the shape of the cost function for species with direct interference competition. 2 Here we report the results of an experiment with two vole species in artificial coexistence in large enclosures, where density of the dominant competitor species (Microtus agrestis) was manipulated. Experimental populations of the subordinate vole species (Clethrionomys glareolus) were composed of same aged individuals to study distribution of costs of coexistence with a dominant species within an age-cohort. 3 Survival and space use decreased …

Kin interactions and population growth

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.…

Behavioural responses of voles to simulated risk of predation by a native and an alien mustelid: an odour manipulation experiment

Context. Potential mammalian prey commonly use the odours of their co-evolved predators to manage their risks of predation. But when the risk comes from an unknown source of predation, odours might not be perceived as dangerous, and anti-predator responses may fail, except possibly if the alien predator is of the same archetype as a native predator. Aims. In the present study we examined anti-predator behavioural responses of voles from the outer archipelagos of the Baltic Sea, south-western Finland, where they have had no resident mammalian predators in recent history. Methods. We investigated responses of field voles (Microtus agrestis) to odours of native least weasels (Mustela nivalis)…

Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus.

Polyandry, i.e. mating with multiple males within one reproductive event, is a common female mating strategy but its adaptive function is often unclear. We tested whether polyandrous females gain genetic benefits by comparing fitness traits of monandrous (mated twice with a single male) and polyandrous (mated twice with two different males) female bank volesClethrionomys glareolus. We raised the offspring in the laboratory until adulthood and measured their body size, before releasing them to outdoor enclosures to overwinter. At the onset of the breeding season in the following spring, we found that offspring of polyandrous females performed significantly better at reproduction than those o…

Does risk of small mustelid predation affect the oestrous cycle in the bank vole,Clethrionomys glareolus?

Female bank voles suppress their reproduction when the risk of small mustelid predation is high. The mechanism for this reproductive suppression is unknown. Because rodents are known to alter their oestrous cycle in response to changing environmental conditions, the eVect of predation risk on the oestrous cycle of bank vole females was studied. The oestrous cycles of 24 females divided into two treatments (predation risk and control) were observed for 20 days using female receptivity as an indication of oestrus. Voles exposed for 2-3 h a day for 20 days to the close presence of a least weasel, Mustela nivalis nivalis, had fewer oestrous cycles than control females exposed to a domestic rabb…

Indirect cues of nest predation risk and avian reproductive decisions

Current life-history theory predicts that increased mortality at early stages of life leads to reduced initial investment (e.g. clutch size) but increased subsequent investment during the reproduction attempt. In a field experiment, migratory pied flycatchers Ficedula hypoleuca perceived differences in mammalian nest predation risk and altered their reproductive strategies in two respects. First, birds avoided nest sites manipulated to reflect the presence of a predator. Second, birds breeding in risky areas nested 4 days earlier and laid 10 per cent larger clutches than those in safe areas, a result that runs counter to the prevailing life-history paradigm. We suggest that the overwhelmin…

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;…

Rodent plagues, immunocontraception and the mousepox virus

Abstract Rodent plagues cause a major problem for agriculture in many temperate regions, and immunocontraception offers a new method to control fertility in these and other pest vertebrates. However, it is difficult to find an effective carrier for contraceptives for large numbers of pest animals in the field. In a new study, Jackson et al. manipulated the mousepox virus to boost the immune response in infected mice Mus musculus when testing the basis for controlling their fecundity rates. However, all infected mice (and half of recently immunized mice) died. Despite these unexpected and dramatic results of the engineering of mousepox virus, immunocontraception remains the most promising me…

Breeding Tubercles, Papillomatosis and Dominance Behaviour of Male Roach (Rutilus rutilus) During the Spawning Period

We studied the relationship between the breeding tubercle ornamentation (i.e. skin roughness) and male pre-spawning dominance and courtship behaviour in roach (Rutilus rutilus) within an experimental laboratory system. Sexually mature fish were caught during their migration to their spawning pond and their behaviours were studied in an artificial spawning arena. Males behaved naturally both in terms of male–male interactions and attempts to achieve spawnings. Males having many, large breeding tubercles (i.e. rough skin) were significantly more often dominant in our dyadic trials than those with smooth skin. The dominant male in the trial exhibited a more active courtship behaviour than its …

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…

Fungal-Mediated Multitrophic Interactions - Do Grass Endophytes in Diet Protect Voles from Predators?

Plant-associated micro-organisms such as mycotoxin-producing endophytes commonly have direct negative effects on herbivores. These effects may be carried over to natural enemies of the herbivores, but this has been rarely explored. We examined how feeding on Neotyphodium endophyte infected (E+) and endophyte free (E−) meadow ryegrass (Scherodonus pratensis) affects body mass, population size and mobility of sibling voles (Microtus levis), and whether the diet mediates the vulnerability of voles to least weasel (Mustela nivalis nivalis) predation. Because least weasels are known to be olfactory hunters, we also examined whether they are able to distinguish olfactory cues of voles fed on E+ a…