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…

Urban forest soils harbour distinct and more diverse communities of bacteria and fungi compared to less disturbed forest soils.

Anthropogenic changes to land use drive concomitant changes in biodiversity, including that of the soil microbiota. However, it is not clear how increasing intensity of human disturbance is reflected in the soil microbial communities. To address this issue, we used amplicon sequencing to quantify the microbiota (bacteria and fungi) in the soil of forests (n=312) experiencing four different land uses, national parks (set aside for nature conservation), managed (for forestry purposes), suburban (on the border of an urban area) and urban (fully within a town or city), which broadly represent a gradient of anthropogenic disturbance. Alpha diversity of bacteria and fungi increased with increasin…

Supporting information for The impact of wildlife and environmental factors on hantavirus infection in host and its translation into human risk

It contains describtive plot for data, supplementary methods and results

Sex–biased maternal investment in voles: importance of environmental conditions

Adaptive bias in sex allocation is traditionally proposed to be related to the condition of mothers as well as to the unequal fitness values of produced sexes. A positive relationship between mother condition and investment into male offspring is often predicted. This relationship was also recently found to depend on environmental conditions. We studied these causalities experimentally using a design where winter food supply was manipulated in eight outdoor-enclosed populations of field voles Microtus agrestis. At the beginning of the breeding season in spring, food-supplemented mothers seemed to be in a similar condition, measured as body mass, head width, body condition index and parasite…

Are habitat loss, predation risk and climate related to the drastic decline in a Siberian flying squirrel population? A 15 year study

To devise effective conservation actions, it is important to know which factors are associated with the population parameters of a declining population. Using mark–recapture methods, we estimated the annual population size, growth rate and survival probability of an ear-tagged flying squirrel population over a 15-year period in a 4,500 ha study area in western Finland. The species is considered vulnerable, but detailed knowledge concerning population sizes or trends is lacking. The population parameters and changes therein were regressed against habitat availability, an indicator of predation pressure, and mean winter temperature (an indicator of climate change), to reveal potential reasons…

Experimental investigation of a hantavirus host-switch between arvicoline rodents Lemmus lemmus and Myodes glareolus

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…

Density-dependent vole damage in silviculture and associated economic losses at a nationwide scale

Voles inflict damage to silviculture by debarking or severing tree seedlings. The large-scale impacts of vole damage to silviculture, both in terms of severity and financial losses are, however, poorly known. In autumn 2005, cyclically fluctuating vole populations were at their highest in Finland for over 15 years, which led to extensive damage to silviculture during the winter 2005/06. We carried out a nationwide assessment of the incidence, spatial extent and economic value of damage and its relation to vole abundance in privately owned forests during this winter. Damage data were obtained with a questionnaire addressed to the directors of all Forest Management Associations (FMAs) operati…

Climate change reshuffles northern species within their niches

Climate change is a pervasive threat to biodiversity. While range shifts are a known consequence of climate warming contributing to regional community change, less is known about how species' positions shift within their climatic niches. Furthermore, whether the relative importance of different climatic variables prompting such shifts varies with changing climate remains unclear. Here we analysed four decades of data for 1,478 species of birds, mammals, butterflies, moths, plants and phytoplankton along a 1,200 km high latitudinal gradient. The relative importance of climatic drivers varied non-uniformly with progressing climate change. While species turnover among decades was limited, the …

Food provisioning alters infection dynamics in populations of a wild rodent

While pathogens are often assumed to limit the growth of wildlife populations, experimental evidence for their effects is rare. A lack of food resources has been suggested to enhance the negative effects of pathogen infection on host populations, but this theory has received little investigation. We conducted a replicated two-factor enclosure experiment, with introduction of the bacteriumBordetella bronchisepticaand food supplementation, to evaluate the individual and interactive effects of pathogen infection and food availability on vole populations during a boreal winter. We show that prior to bacteria introduction, vole populations were limited by food availability.Bordetella bronchisept…

Description of research methods and results tables from Food limitation constrains host immune responses to nematode infections

Trade-offs in the allocation of finite-energy resources among immunological defences and other physiological processes are believed to influence infection risk and disease severity in food-limited wildlife populations. However, this prediction has received little experimental investigation. Here we test the hypothesis that food limitation impairs the ability of wild field voles (Microtus agrestis) to mount an immune response against parasite infections. We conducted a replicated experiment on vole populations maintained in large outdoor enclosures during boreal winter, using food supplementation and anthelmintic treatment of intestinal nematodes. Innate immune responses against intestinal p…

Food resources and intestinal parasites as limiting factors for boreal vole populations during winter

Processes limiting the growth of cyclic vole populations have stimulated considerable research and debate over several decades. In Fennoscandia, the peak density of cyclic vole populations occurs in fall, and is followed by a severe winter decline. Food availability and intestinal parasites have been demonstrated to independently and synergistically limit wildlife populations. The purpose of this study was to directly compare competing food and parasite hypotheses on the limitation of overwintering high-density vole populations. Moreover, we evaluated the ability of food limitation and nematode infection to interact and thereby intensify population declines. A two-factor experiment with foo…

Curvilinear interspecific density-range size relationship in small mammals in Finland

ABSTRACTAim Macroecological patterns have mainly been depicted as atemporal, withexisting research covering only short time periods. One fundamental pattern inmacroecology is the interspecific relationship between local abundance andregional range size, which is generally considered to be positively linear. Here,we examine structural details of the relationship between abundance and rangesize in cyclic populations of small mammals and its long-term temporal varia-tion.Location Finland.Methods We analysed 39 years of trapping data of Rodentia and Soricomor-pha collected in field and forest habitats across Finland. Abundance was mea-sured as the mean population density of individuals, and range…

Experimental Infection of Voles with Francisella tularensis Indicates Their Amplification Role in Tularemia Outbreaks

Tularemia outbreaks in humans have been linked to fluctuations in rodent population density, but the mode of bacterial maintenance in nature is unclear. Here we report on an experiment to investigate the pathogenesis of Francisella tularensis infection in wild rodents, and thereby assess their potential to spread the bacterium. We infected 20 field voles (Microtus agrestis) and 12 bank voles (Myodes glareolus) with a strain of F. tularensis ssp. holarctica isolated from a human patient. Upon euthanasia or death, voles were necropsied and specimens collected for histological assessment and identification of bacteria by immunohistology and PCR. Bacterial excretion and a rapid lethal clinical …

Serological Survey of Rodent-Borne Viruses in Finnish Field Voles

In northern Europe, rodent populations display cyclic density fluctuations, which can be correlated with the human incidence of zoonotic diseases they spread. During density peaks, field voles (Microtus agrestis) become one of the most abundant rodent species in northern Europe, yet little is known of the viruses they host. We screened 709 field voles, trapped from 14 sites over three years, for antibodies against four rodent-borne, potentially zoonotic viruses or virus groups: hantaviruses, lymphocytic choriomeningitis virus (LCMV), Ljungan virus (LV) and orthopoxviruses (OPV). Antibodies against all four viruses were detected. However, seroprevalence of hantaviruses, LV and LCMV was low. …

The impact of wildlife and environmental factors on hantavirus infection in the host and its translation into human risk

Identifying factors that drive infection dynamics in reservoir host populations is essential in understanding human risk from wildlife-originated zoonoses. We studied zoonotic Puumala orthohantavirus (PUUV) in the host, the bank vole ( Myodes glareolus ), populations in relation to the host population, rodent and predator community and environment-related factors and whether these processes are translated into human infection incidence. We used 5-year rodent trapping and bank vole PUUV serology data collected from 30 sites located in 24 municipalities in Finland. We found that PUUV seroprevalence in the host was negatively associated with the abundance of red foxes, but this process did no…

Solutions to replace quantity with quality in science.

In their recent letter, Joern Fischer and others [1xAcademia's obsession with quantity. Fischer, J. et al. Trends Ecol. Evol. 2012; 27: 463–474See all References[1] tackled one of the major problems in modern science: the obsession with quantity. Perspicaciously, they showed how targeting for quantity has faded out creativity and reflection from science. Fischer and others ended their letter with the words: ‘Starting with our own university departments (but not stopping there), it is time to take stock of what we are doing. We must recreate spaces for reflection, personal relationships, and depth. More does not equal better.’ Utopian as it may be, we applaud this statement.Unfortunately, Fi…

Food limitation constrains host immune responses to nematode infections.

Trade-offs in the allocation of finite-energy resources among immunological defences and other physiological processes are believed to influence infection risk and disease severity in food-limited wildlife populations. However, this prediction has received little experimental investigation. Here we test the hypothesis that food limitation impairs the ability of wild field voles ( Microtus agrestis ) to mount an immune response against parasite infections. We conducted a replicated experiment on vole populations maintained in large outdoor enclosures during boreal winter, using food supplementation and anthelmintic treatment of intestinal nematodes. Innate immune responses against intestina…

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…

Diet Quality Limits Summer Growth of Field Vole Populations

Marked variation occurs in both seasonal and multiannual population density peaks of northern European small mammal species, including voles. The availability of dietary proteins is a key factor limiting the population growth of herbivore species. The objective of this study is to investigate the degree to which protein availability influences the growth of increasing vole populations. We hypothesise that the summer growth of folivorous vole populations is positively associated with dietary protein availability. A field experiment was conducted over a summer reproductive period in 18 vegetated enclosures. Populations of field voles (Microtus agrestis) were randomised amongst three treatment…

Data from: Food limitation constrains host immune responses to nematode infections

Trade-offs in the allocation of finite-energy resources among immunological defences and other physiological processes are believed to influence infection risk and disease severity in food-limited wildlife populations. However, this prediction has received little experimental investigation. Here we test the hypothesis that food limitation impairs the ability of wild field voles (Microtus agrestis) to mount an immune response against parasite infections. We conducted a replicated experiment on vole populations maintained in large outdoor enclosures during boreal winter, using food supplementation and anthelmintic treatment of intestinal nematodes. Innate immune responses against intestinal p…

Appendix A. Structure of missing data (see data analysis of Methods section).

Structure of missing data (see data analysis of Methods section).

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…

Data from: Food provisioning alters infection dynamics in populations of a wild rodent

While pathogens are often assumed to limit the growth of wildlife populations, experimental evidence for their effects is rare. A lack of food resources has been suggested to enhance the negative effects of pathogen infection on host populations, but this theory has received little investigation. We conducted a replicated two-factor enclosure experiment, with introduction of the bacterium Bordetella bronchiseptica and food supplementation, to evaluate the individual and interactive effects of pathogen infection and food availability on vole populations during a boreal winter. We show that prior to bacteria introduction, vole populations were limited by food availability. Bordetella bronchis…

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…