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Welcome to the Dark Side
(2022)
Differences in natural light conditions caused by changes in moonlight are known to affect perceived predation risk in many nocturnal prey species. As artificial light at night (ALAN) is steadily increasing in space and intensity, it has the potential to change movement and foraging behavior of many species as it might increase perceived predation risk and mask natural light cycles. We investigated if partial nighttime illumination leads to changes in foraging behavior during the night and the subsequent day in a small mammal and whether these changes are related to animal personalities. We subjected bank voles to partial nighttime illumination in a foraging landscape under laboratory conditions and in large grassland enclosures under near natural conditions. We measured giving-up density of food in illuminated and dark artificial seed patches and video recorded the movement of animals. While animals reduced number of visits to illuminated seed patches at night, they increased visits to these patches at the following day compared to dark seed patches. Overall, bold individuals had lower giving-up densities than shy individuals but this difference increased at day in formerly illuminated seed patches. Small mammals thus showed carry-over effects on daytime foraging behavior due to ALAN, i.e., nocturnal illumination has the potential to affect intra- and interspecific interactions during both night and day with possible changes in personality structure within populations and altered predator-prey dynamics.
The complete mitochondrial genome of the common vole, Microtus arvalis (Rodentia: Arvicolinae)
(2018)
The common vole, Microtus arvalis belongs to the genus Microtus in the subfamily Arvicolinae. In this study, the complete mitochondrial genome of M. arvalis was recovered using shotgun sequencing and an iterative mapping approach using three related species. Phylogenetic analyses using the sequence of 21 arvicoline species place the common vole as a sister species to the East European vole (Microtus levis), but as opposed to previous results we find no support for the recognition of the genus Neodon within the subfamily Arvicolinae, as this is, as well as the genus Lasiopodomys, found within the Microtus genus.
The Bruce effect revisited
(2017)
Pregnancy termination after encountering a strange male, the Bruce effect, is regarded as a counterstrategy of female mammals towards anticipated infanticide. While confirmed in caged rodent pairs, no verification for the Bruce effect existed from experimental field populations of small rodents. We suggest that the effect may be adaptive for breeding rodent females only under specific conditions related to populations with cyclically fluctuating densities. We investigated the occurrence of delay in birth date after experimental turnover of the breeding male under different population composition in bank voles (Myodes glareolus) in large outdoor enclosures: one-male–multiple-females (n = 6 populations/18 females), multiple-males–multiple-females (n = 15/45), and single-male–single-female (MF treatment, n = 74/74). Most delays were observed in the MF treatment after turnover. Parallel we showed in a laboratory experiment (n = 205 females) that overwintered and primiparous females, the most abundant cohort during population lows in the increase phase of cyclic rodent populations, were more likely to delay births after turnover of the male than year-born and multiparous females. Taken together, our results suggest that the Bruce effect may be an adaptive breeding strategy for rodent females in cyclic populations specifically at low densities in the increase phase, when isolated, overwintered animals associate in MF pairs. During population lows infanticide risk and inbreeding risk may then be higher than during population highs, while also the fitness value of a litter in an increasing population is higher. Therefore, the Bruce effect may be adaptive for females during annual population lows in the increase phases, even at the costs of delaying reproduction.
State-dependent foraging
(2015)
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 presence” and “season.” We monitored use of feeding stations near and far from the nest as measurement of foraging activity and strategic foraging behavior. Vole mothers adapted their strategies to shrew presence and optimized their foraging behavior according to seasonal constraints, resulting in an interaction of treatment and season. In summer, shrew presence reduced food intake from feeding stations, while it enhanced intake in autumn. Shrew presence decreased the number of visited feeding stations in autumn and concentrated mother’s foraging efforts to fewer stations. Independent of shrew presence or season, mothers foraged more in patches further away from the nest than near the nest. Results indicate that females are not investing in nest guarding but try to avoid the accumulation of olfactory cues near the nest leading a predator to the young. Additionally, our study shows how foraging strategies and nest attendance are influenced by seasonal food provision.
Seed traits matter
(2021)
Although many plants are dispersed by wind and seeds can travel long distances across unsuitable matrix areas, a large proportion relies on co-evolved zoochorous seed dispersal to connect populations in isolated habitat islands. Particularly in agricultural landscapes, where remaining habitat patches are often very small and highly isolated, mobile linkers as zoochorous seed dispersers are critical for the population dynamics of numerous plant species. However, knowledge about the quali- or quantification of such mobile link processes, especially in agricultural landscapes, is still limited. In a controlled feeding experiment, we recorded the seed intake and germination success after complete digestion by the European brown hare (Lepus europaeus) and explored its mobile link potential as an endozoochoric seed disperser. Utilizing a suite of common, rare, and potentially invasive plant species, we disentangled the effects of seed morphological traits on germination success while controlling for phylogenetic relatedness. Further, we measured the landscape connectivity via hares in two contrasting agricultural landscapes (simple: few natural and semi-natural structures, large fields; complex: high amount of natural and semi-natural structures, small fields) using GPS-based movement data. With 34,710 seeds of 44 plant species fed, one of 200 seeds (0.51%) with seedlings of 33 species germinated from feces. Germination after complete digestion was positively related to denser seeds with comparatively small surface area and a relatively slender and elongated shape, suggesting that, for hares, the most critical seed characteristics for successful endozoochorous seed dispersal minimize exposure of the seed to the stomach and the associated digestive system. Furthermore, we could show that a hare's retention time is long enough to interconnect different habitats, especially grasslands and fields. Thus, besides other seed dispersal mechanisms, this most likely allows hares to act as effective mobile linkers contributing to ecosystem stability in times of agricultural intensification, not only in complex but also in simple landscapes.
Background: Short lived, iteroparous animals in seasonal environments experience variable social and environmental conditions over their lifetime. Animals can be divided into those with a "young-of-the-year" life history (YY, reproducing and dying in the summer of birth) and an "overwinter" life history (OW, overwintering in a subadult state before reproducing next spring).
We investigated how behavioural patterns across the population were affected by season and sex, and whether variation in behaviour reflects the variation in life history patterns of each season. Applications of pace-of-life (POL) theory would suggest that long-lived OW animals are shyer in order to increase survival, and YY are bolder in order to increase reproduction. Therefore, we expected that in winter and spring samples, when only OW can be sampled, the animals should be shyer than in summer and autumn, when both OW and YY animals can be sampled. We studied common vole (Microtus arvalis) populations, which express typical, intra-annual density fluctuation. We captured a total of 492 voles at different months over 3 years and examined boldness and activity level with two standardised behavioural experiments.
Results: Behavioural variables of the two tests were correlated with each other. Boldness, measured as short latencies in both tests, was extremely high in spring compared to other seasons. Activity level was highest in spring and summer, and higher in males than in females.
Conclusion: Being bold in laboratory tests may translate into higher risk-taking in nature by being more mobile while seeking out partners or valuable territories. Possible explanations include asset-protection, with OW animals being rather old with low residual reproductive value in spring. Therefore, OW may take higher risks during this season. Offspring born in spring encounter a lower population density and may have higher reproductive value than offspring of later cohorts. A constant connection between life history and animal personality, as suggested by the POL theory, however, was not found. Nevertheless, correlations of traits suggest the existence of animal personalities. In conclusion, complex patterns of population dynamics, seasonal variation in life histories, and variability of behaviour due to asset-protection may cause complex seasonal behavioural dynamics in a population.
Infanticide, the killing of unrelated young, is widespread and frequently driven by sexual conflict. especially in mammals with exclusive maternal care, infanticide by males is common and females suffer fitness costs. Recognizing infanticide risk and adjusting offspring protection accordingly should therefore be adaptive in female mammals. Using a small mammal (Myodes glareolus) in outdoor enclosures, we investigated whether lactating mothers adjust offspring protection, and potential mate search behaviour, in response to different infanticide risk levels. We presented the scent of the litter’s sire or of a stranger male near the female’s nest, and observed female nest presence and movement by radiotracking. While both scents simulated a mating opportunity, they represented lower (sire) and higher (stranger) infanticide risk. compared to the sire treatment, females in the stranger treatment left their nest more often, showed increased activity and stayed closer to the nest, suggesting offspring protection from outside the nest through elevated alertness and vigilance. females with larger litters spent more time investigating scents and used more space in the sire but not in the stranger treatment. Thus, current investment size affected odour inspection and resource acquisition under higher risk. Adjusting nest protection and resource acquisition to infanticide risk could allow mothers to elicit appropriate (fitness-saving) counterstrategies, and thus, may be widespread.
Background
In Europe, bank voles (Myodes glareolus) are widely distributed and can transmit Puumala virus (PUUV) to humans, which causes a mild to moderate form of haemorrhagic fever with renal syndrome, called nephropathia epidemica. Uncovering the link between host and virus dynamics can help to prevent human PUUV infections in the future. Bank voles were live trapped three times a year in 2010–2013 in three woodland plots in each of four regions in Germany. Bank vole population density was estimated and blood samples collected to detect PUUV specific antibodies.
Results
We demonstrated that fluctuation of PUUV seroprevalence is dependent not only on multi-annual but also on seasonal dynamics of rodent host abundance. Moreover, PUUV infection might affect host fitness, because seropositive individuals survived better from spring to summer than uninfected bank voles. Individual space use was independent of PUUV infections.
Conclusions
Our study provides robust estimations of relevant patterns and processes of the dynamics of PUUV and its rodent host in Central Europe, which are highly important for the future development of predictive models for human hantavirus infection risk.
Of city and village mice
(2020)
A fundamental question of current ecological research concerns the drives and limits of species responses to human-induced rapid environmental change (HIREC). Behavioural responses to HIREC are a key component because behaviour links individual responses to population and community changes. Ongoing fast urbanization provides an ideal setting to test the functional role of behaviour for responses to HIREC. Consistent behavioural differences between conspecifics (animal personality) may be important determinants or constraints of animals’ adaptation to urban habitats. We tested whether urban and rural populations of small mammals differ in mean trait expression, flexibility and repeatability of behaviours associated to risk-taking and exploratory tendencies. Using a standardized behavioural test in the field, we quantified spatial exploration and boldness of striped field mice (Apodemus agrarius, n = 96) from nine sub-populations, presenting different levels of urbanisation and anthropogenic disturbance. The level of urbanisation positively correlated with boldness, spatial exploration and behavioural flexibility, with urban dwellers being bolder, more explorative and more flexible in some traits than rural conspecifics. Thus, individuals seem to distribute in a non-random way in response to human disturbance based on their behavioural characteristics. Animal personality might therefore play a key role in successful coping with the challenges of HIREC.
Migration phenology determines niche use of East Asian buntings (Emberizidae) during stopover
(2018)
Stopover niche utilization of birds during migration has not gained much attention so far, since the majority of the studies focuses on breeding or wintering areas. However, stopover sites are crucial for migratory birds. They are often used by a multitude of species, which could lead to increased competition. In this work, we investigated niche use of 8 migratory and closely related Emberiza bunting species at a stopover site in Far East Russia, situated on the poorly studied East Asian flyway. We used bird ringing data to evaluate morphological similarity as well as niche overlap on the trophic, spatial, and temporal dimension. Bill morphology was used as a proxy for their trophic niche. We were able to prove that a majority of the species occupies well-defined stopover niches on at least one of the dimensions. Niche breadth and niche overlap differ between spring and autumn season with higher overlap found during spring. Morphological differences are mostly related to overall size and wing pointedness. The temporal dimension is most important for segregation among the studied species. Furthermore, all species seem to exhibit a rather strict and consistent phenological pattern. Their occurrence at the study site is highly correlated with their geographic origin and the length of their migration route. We assume that buntings are able to use available resources opportunistically during stopover, while trying to follow a precise schedule in order to avoid competition and to ensure individual fitness.
Background
A territory as a prerequisite for breeding limits the maximum number of breeders in a given area, and thus lowers the proportion of breeders if population size increases. However, some territorially breeding animals can have dramatic density fluctuations and little is known about the change from density-dependent processes to density-independence of breeding during a population increase or an outbreak. We suggest that territoriality, breeding suppression and its break-down can be understood with an incomplete-control model, developed for social breeders and social suppression.
Results
We studied density dependence in an arvicoline species, the bank vole, known as a territorial breeder with cyclic and non-cyclic density fluctuations and periodically high densities in different parts of its range. Our long-term data base from 38 experimental populations in large enclosures in boreal grassland confirms that breeding rates are density-regulated at moderate densities, probably by social suppression of subordinate potential breeders. We conducted an experiment, were we doubled and tripled this moderate density under otherwise the same conditions and measured space use, mortality, reproduction and faecal stress hormone levels (FGM) of adult females. We found that mortality did not differ among the densities, but the regulation of the breeding rate broke down: at double and triple densities all females were breeding, while at the low density the breeding rate was regulated as observed before. Spatial overlap among females increased with density, while a minimum territory size was maintained. Mean stress hormone levels were higher in double and triple densities than at moderate density.
Conclusions
At low and moderate densities, breeding suppression by the dominant breeders, But above a density-threshold (similar to a competition point), the dominance of breeders could not be sustained (incomplete control). In our experiment, this point was reached after territories could not shrink any further, while the number of intruders continued to increase with increasing density. Probably suppression becomes too costly for the dominants, and increasing number of other breeders reduces the effectiveness of threats. In wild populations, crossing this threshold would allow for a rapid density increase or population outbreaks, enabling territorial species to escape density-dependency.
Background: Artificial light at night (ALAN) is one form of human-induced rapid environmental changes (HIREC) and is strongly interfering with natural dark–light cycles. Some personality types within a species might be better suited to cope with environmental change and therefore might be selected upon under ongoing urbanization.
Results: We used LED street lamps in a large outdoor enclosure to experimentally investigate the effects of ALAN on activity patterns, movement and interaction of individuals of two species, the bank vole (Myodes glareolus) and the striped field mouse (Apodemus agrarius). We analyzed effects combined with individual boldness score. Both species reduced their activity budget during daylight hours. While under natural light conditions home ranges were larger during daylight than during nighttime, this difference vanished under ALAN. Conspecifics showed reduced home range overlap, proximity and activity synchrony when subjected to nighttime illumination. Changes in movement patterns in reaction to ALAN were not associated with differences in boldness score of individuals.
Conclusions: Our results suggest that light pollution can lead to changes in movement patterns and individual interactions in small mammals. This could lead to fitness consequences on the population level.
Artificial light at night (ALAN) is altering the behaviour of nocturnal animals in a manifold of ways. Nocturnal invertebrates are particularly affected, due to their fatal attraction to ALAN. This selective pressure has the potential to reduce the strength of the flight-to-light response in insects, as shown recently in a moth species. Here we investigated light attraction of ground beetles (Coleoptera: Carabidae).We compared among animals (three genera) from a highly light polluted (HLP) grassland in the centre of Berlin and animals collected at a low-polluted area in a Dark Sky Reserve (DSR), captured using odour bait. In an arena setting tested at night time, HLP beetles (n = 75 across all genera) showed a reduced attraction towards ALAN. Tested during daytime, HLP beetles were less active in an open field test (measured as latency to start moving), compared to DSR (n = 143). However, we did not observe a reduced attraction towards ALAN within the species most common at both sides, Calathus fuscipes (HLP = 37, DSR = 118 individuals) indicating that not all species may be equally affected by ALAN. Reduced attraction to ALAN in urban beetles may either be a result of phenotypic selection in each generation removing HLP individuals that are attracted to light, or an indication for ongoing evolutionary differentiation among city and rural populations in their light response. Reduced attraction to light sources may directly enhance survival and reproductive success of urban individuals. However, decrease in mobility may negatively influence dispersal, reproduction and foraging success, highlighting the selective pressure that light pollution may have on fitness, by shaping and modifying the behaviour of insects.
Landscape and scale-dependent spatial niches of bats foraging above intensively used arable fields
(2017)
Introduction
Bats are threatened by agricultural intensification, and although bat ecology in agricultural landscapes is in the focus of current research, the effects of interacting spatiotemporal factors on species-specific bat activity above farmland remain understudied. Our aim was to identify spatiotemporal factors and their interactions relevant for the activity of bat species above conventionally managed arable fields.
Methods
We repeatedly monitored relative bat activity above open arable fields in Germany using acoustic monitoring. We used site-related biotic and abiotic factors and landscape characteristics across five spatial scales, their combinations, and interactions to identify those factors which best explain variation in bat activity.
Results
Numerous interactions between landscape characteristics and the insect abundance affected bat activity above fields. For instance, Pipistrellus pipistrellus became more active with increasing insect abundance, but only above fields with a low proportion of woody vegetation cover in the surroundings. Additionally, the level of bat activity in summer depended on landscape characteristics. For example, the activity of Pipistrellus nathusii was relatively low in summer above fields that were surrounded by vegetation patches with a high degree of edge complexity (e.g., hedgerow). However, the activity remained at a relatively high level and did not differ between seasons above fields that were surrounded by vegetation patches with a low degree of edge complexity (e.g., roundly shaped forest patch).
Conclusions
Our results revealed that landscape characteristics and their interactions with insect abundance affected bat activity above conventionally managed fields and highlighted the opportunistic foraging behavior of bats. To improve the conditions for bats in agricultural landscapes, we recommend re-establishing landscape heterogeneity to protect aquatic habitats and to increase arthropod availability.
Movement of organisms is one of the key mechanisms shaping biodiversity, e.g. the distribution of genes, individuals and species in space and time. Recent technological and conceptual advances have improved our ability to assess the causes and consequences of individual movement, and led to the emergence of the new field of ‘movement ecology’. Here, we outline how movement ecology can contribute to the broad field of biodiversity research, i.e. the study of processes and patterns of life among and across different scales, from genes to ecosystems, and we propose a conceptual framework linking these hitherto largely separated fields of research. Our framework builds on the concept of movement ecology for individuals, and demonstrates its importance for linking individual organismal movement with biodiversity. First, organismal movements can provide ‘mobile links’ between habitats or ecosystems, thereby connecting resources, genes, and processes among otherwise separate locations. Understanding these mobile links and their impact on biodiversity will be facilitated by movement ecology, because mobile links can be created by different modes of movement (i.e., foraging, dispersal, migration) that relate to different spatiotemporal scales and have differential effects on biodiversity. Second, organismal movements can also mediate coexistence in communities, through ‘equalizing’ and ‘stabilizing’ mechanisms. This novel integrated framework provides a conceptual starting point for a better understanding of biodiversity dynamics in light of individual movement and space-use behavior across spatiotemporal scales. By illustrating this framework with examples, we argue that the integration of movement ecology and biodiversity research will also enhance our ability to conserve diversity at the genetic, species, and ecosystem levels.
Balancing foraging gain and predation risk is a fundamental trade-off in the life of animals. Individual strategies to acquire, process, store and use information to solve cognitive tasks are likely to affect speed and flexibility of learning, and ecologically relevant decisions regarding foraging and predation risk. Theory suggests a functional link between individual variation in cognitive style and behaviour (animal personality) via speed-accuracy and risk-reward trade-offs. We tested whether cognitive style and personality affect risk-reward trade-off decisions posed by foraging and predation risk. We exposed 21 bank voles (Myodes glareolus) that were bold, fast learning and inflexible and 18 voles that were shy, slow learning and flexible to outdoor enclosures with different risk levels at two food patches. We quantified individual food patch exploitation, foraging and vigilance behaviour. Although both types responded to risk, fast animals increasingly exploited both food patches, gaining access to more food and spending less time searching and exercising vigilance. Slow animals progressively avoided high-risk areas, concentrating foraging effort in the low-risk one, and devoting >50% of visit to vigilance. These patterns indicate that individual differences in cognitive style/personality are reflected in foraging and anti-predator decisions that underlie the individual risk-reward bias.
Background
Many animals live in environments where different types of predators pose a permanent threat and call for predator specific strategies. When foraging, animals have to balance the competing needs of food and safety in order to survive. While animals sometimes can choose between microhabitats that differ in their risk of predation, many habitats are uniform in their risk distribution. So far, little is known about adaptive antipredator behavior under uniform risk. We simulated two predator types, avian and mammalian, each representing a spatially uniform risk in the artificial resource landscapes. Voles served as experimental foragers.
Results
Animals were exposed to factorial combinations of weasel odour and ground cover to simulate avian and/or mammalian predation. We measured short and long term responses with video analysis and giving-up densities. The results show that previously experienced conditions cause delayed effects. After these effects ceased, the risks of both types of predation caused a reduction in food intake. Avian predation induced a concentration on a smaller number of feeding patches. While higher avian risk caused a delay in activity, the weasel odour shortened the latency until the voles started to be active.
Conclusion
We show that the voles differed in risk types and adjusted their feeding strategies accordingly. Responses to avian and mammalian risk differed both in strength and time scales. Uniformity of risk resulted in a concentration of foraging investment and lower foraging efficiency.
Perceived predation risk varies in space and time. Foraging in this landscape of fear alters forager-resource interactions via cascading nonconsumptive effects. Estimating these indirect effects is difficult in natural systems. Here, we applied a novel measure to quantify the diversity at giving-up density that allows to test how spatial variation in perceived predation risk modifies the diversity of multispecies resources at local and regional spatial levels. Furthermore, we evaluated whether the nonconsumptive effects on resource species diversity can be explained by the preferences of foragers for specific functional traits and by the forager species richness. We exposed rodents of a natural community to artificial food patches, each containing an initial multispecies resource community of eight species (10 items each) mixed in sand. We sampled 35 landscapes, each containing seven patches in a spatial array, to disentangle effects at local (patch) and landscape levels. We used vegetation height as a proxy for perceived predation risk. After a period of three nights, we counted how many and which resource species were left in each patch to measure giving-up density and resource diversity at the local level (alpha diversity) and the regional level (gamma diversity and beta diversity). Furthermore, we used wildlife cameras to identify foragers and assess their species richness. With increasing vegetation height, i.e., decreasing perceived predation risk, giving-up density, and local alpha and regional gamma diversity decreased, and patches became less similar within a landscape (beta diversity increased). Foragers consumed more of the bigger and most caloric resources. The higher the forager species richness, the lower the giving-up density, and alpha and gamma diversity. Overall, spatial variation of perceived predation risk of foragers had measurable cascading effects on local and regional resource species biodiversity, independent of the forager species. Thus, nonconsumptive predation effects modify forager-resource interactions and might act as an equalizing mechanism for species coexistence.
Fat loads were quantified for 2125 Yellow-browed Warblers Phylloscopus inornatus trapped at a stop-over site in Far East Russia during autumn migration. Flight ranges of 660–820 km were estimated for the fattest individuals, suggesting that they would need to stop for refuelling at least six times to reach their wintering areas in South East Asia.