0000000001315655
AUTHOR
Janne Sundell
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…
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…
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…
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 …
Conservation implications of change in antipredator behavior in fragmented habitat: Boreal rodent, the bank vole, as an experimental model
Abstract Habitat fragmentation is known to cause population declines but the mechanisms leading to the decline are not fully understood. Fragmentation is likely to lead to changes in predation risk, which may cause behavioral responses with possible population level consequences. It has recently been shown that the awareness of predator presence, resulting in a fear response, strongly affects behavior and physiology of the prey individuals. Costs arising from fear may be as important for the prey population size as the direct killing of prey. We tested how predation risk in the form of scent of a specialist predator, the least weasel (Mustela nivalis nivalis), affects bank vole (Myodes glar…
How Do Infanticidal Male Bank Voles (Myodes glareolus) Find the Nest with Pups?
Infanticide, the killing of conspecific young, occurs in most mammal species, like in our study species, the bank vole (Myodes glareolus). Infanticide by adult males is regarded as a strong factor affecting recruitment of young into population. It is considered as an adaptive behaviour, which may increase male fitness via resource gain or an increased access to mates. When an intruder is approaching the nest, the mother should not be present, as her nest guarding is very aggressive and successful. Pups use ultrasonic vocalisation to call their mother when mother leaves nest for foraging but it is not know which cues do infanticidal males use to find the nest with vulnerable pups to commit i…
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 …
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…
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 …
Large-scale long-term passive-acoustic monitoring reveals spatio-temporal activity patterns of boreal bats
The distribution ranges and spatio-temporal patterns in the occurrence and activity of boreal bats are yet largely unknown due to their cryptic lifestyle and lack of suitable and efficient study methods. We approached the issue by establishing a permanent passive-acoustic sampling setup spanning the area of Finland to gain an understanding on how latitude affects bat species composition and activity patterns in northern Europe. The recorded bat calls were semi-automatically identified for three target taxa; Myotis spp., Eptesicus nilssonii or Pipistrellus nathusii and the seasonal activity patterns were modeled for each taxa across the seven sampling years (2015–2021). We found an increase …
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…
Nonlinear effects of climate on boreal rodent dynamics: mild winters do not negate high-amplitude cycles
Small rodents are key species in many ecosystems. In boreal and subarctic environments, their importance is heightened by pronounced multiannual population cycles. Alarmingly, the previously regular rodent cycles appear to be collapsing simultaneously in many areas. Climate change, particularly decreasing snow quality or quantity in winter, is hypothesized as a causal factor, but the evidence is contradictory. Reliable analysis of population dynamics and the influence of climate thereon necessitate spatially and temporally extensive data. We combined data on vole abundances and climate, collected at 33 locations throughout Finland from 1970 to 2011, to test the hypothesis that warming winte…
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…
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…
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…
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…
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…
Ecology and extent of freshwater browning - What we know and what should be studied next in the context of global change
Water browning or brownification refers to increasing water color, often related to increasing dissolved organic matter (DOM) and carbon (DOC) content in freshwaters. Browning has been recognized as a significant physicochemical phenomenon altering boreal lakes, but our understanding of its ecological consequences in different freshwater habitats and regions is limited. Here, we review the consequences of browning on different freshwater habitats, food webs and aquatic-terrestrial habitat coupling. We examine global trends of browning and DOM/DOC, and the use of remote sensing as a tool to investigate browning from local to global scales. Studies have focused on lakes and rivers while seldo…
SPACE USE, CIRCADIAN ACTIVITY PATTERN, AND MATING SYSTEM OF THE NOCTURNAL TREE RAT THALLOMYS NIGRICAUDA
We present results of a radiotracking study of the black-tailed tree rat Thallomys nigricauda, based on 3 males and 4 females in the breeding season and 2 males and 5 females in the nonbreeding season. The study was conducted in the southern Kalahari thornveld, South Africa, a savanna landscape of acacia trees and patchy acacia bush. Nocturnal activity patterns, vegetation use, space use, and interactions were followed for 8–17 days. During the breeding season, males were active with 2 synchronous activity peaks shortly after sunset and late at night. Home ranges included the nests of 8–10 females, 6 different daytime resting places, and 3–5 areas of high activity. Males were mobile within …
Predation on two vole species by a shared predator: antipredatory response and prey preference
In prey communities with shared predators, variation in prey vulnerability is a key factor in shaping community dynamics. Conversely, the hunting efficiency of a predator depends on the prey community structure, preferences of the predator and antipredatory behavioural traits of the prey. We studied experimentally, under seminatural field conditions, the preferences of a predator and the antipredatory responses of prey in a system consisting of two Myodes species of voles, the grey-sided vole (M. rufocanus Sund.) and the bank vole (M. glareolus Schreb.), and their specialist predator, the least weasel (Mustela nivalis nivalis L.). To quantify the preference of the weasels, we developed a ne…
Changing winter conditions in the boreal forest : the effects of fluctuating temperature and predation risk on activity and physiological stress level in bank voles
Due to global climate change, the winter conditions in the North are predicted to change, as the time with an intact insulating snow cover gets shorter or disappears altogether. For small mammals, this could cause exposure to strong temperature fluctuations and increased predation risk, inducing severe stress and leading to alterations in the physical condition and behavior. To test this, we exposed bank voles (Myodes glareolus) to different temperature regimes and cues of predator threat under laboratory conditions. The test animals experienced either a stable but cool temperature regime resembling the stable conditions under snow cover, or an unstable temperature regime with cold nights a…
Predation risk and food: opposite effects on overwintering survival and onset of breeding in a boreal rodent
1. In seasonal environments, optimal onset of breeding and survival plays major roles in individual fitness. Many physiological and behavioural factors related to breeding increase the risk of predation; thus, breeding decisions should be based on current risks and benefits. According to life-history theory, if current predation risk is high and breeding itself increases the risk, it may be beneficial to postpone breeding. 2. During winter in northern hemispheres, food availability is limited and is at its lowest just prior to the onset of breeding in spring. Food constraint may lead to poor condition and reduced ability to start breeding. 3. We studied the effects of food and predation ris…
Predator–vole interactions in northern Europe: the role of small mustelids revised
The cyclic population dynamics of vole and predator communities is a key phenomenon in northern ecosystems, and it appears to be influenced by climate change. Reports of collapsing rodent cycles have attributed the changes to warmer winters, which weaken the interaction between voles and their specialist subnivean predators. Using population data collected throughout Finland during 1986–2011, we analyse the spatio-temporal variation in the interactions between populations of voles and specialist, generalist and avian predators, and investigate by simulations the roles of the different predators in the vole cycle. We test the hypothesis that vole population cyclicity is dependent on predator…
Data from: Predator–vole interactions in northern Europe: the role of small mustelids revised
The cyclic population dynamics of vole and predator communities is a key phenomenon in northern ecosystems, and it appears to be influenced by climate change. Reports of collapsing rodent cycles have attributed the changes to warmer winters, which weaken the interaction between voles and their specialist subnivean predators. Using population data collected throughout Finland during 1986–2011, we analyse the spatio-temporal variation in the interactions between populations of voles and specialist, generalist and avian predators, and investigate by simulations the roles of the different predators in the vole cycle. We test the hypothesis that vole population cyclicity is dependent on predator…
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…