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; or a control treatment without added scents. Parents were treated in semi-natural field enclosures, but pups were born in the lab and assayed in an open-field arena. Before each behavioral test, one of the three scent treatments was spread throughout the test arena. The tests followed a full factorial design (3 parental treatments × 3 area treatments). Regardless of the parents’ treatment, pups exposed to predator odor in the arena moved more. Additionally, pups spend more time in the center of the arena when presented with predator odor or alarm pheromone compared with the control. Pups from predator odor–exposed parents avoided the center of the arena under control conditions, but they spent more time in the center when either predator odor or alarm pheromone was present. Our experiment shows that cross-generational effects are context-sensitive, depending on the perceived risk. Future studies should examine cross-generational behavioral effects in ecologically meaningful environments instead of only neutral ones. Significance statement We exposed bank voles to odors signaling predation risk to assess the effects parental predation exposure on the behavior of their offspring. Besides predator odor, we also assessed the role of a conspecific alarm cue as a novel way of spreading the predation risk information. Pup behaviors were assessed in the open-field arena, a standard way of assessing animal behavior in a wide range of contexts. We found that also alarm pheromone increased the time pups spend in the center of the arena similarly to predator odor. While previous studies suggested that offspring would be more fearful, our results indicate that the cross-generational effects are very context-dependent; i.e., they differ significantly depending on which scent cue is presented in the open-field arena. This shows the need for better tools or measurements to translate laboratory results into ecologically meaningful frameworks.

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Predation risk and reproduction in the bank vole

Wildlife Research ◽

10.1071/wr12012 ◽

2012 ◽

Vol 39 (5) ◽

pp. 463 ◽

Cited By ~ 9

Author(s):

Lenka Trebatická ◽

Paula Suortti ◽

Janne Sundell ◽

Hannu Ylönen

Keyword(s):

Predation Risk ◽

Breeding Season ◽

Bank Vole ◽

Life History Strategies ◽

Boreal Summer ◽

Myodes Glareolus ◽

Adaptive Behaviour ◽

Optimal Timing ◽

Small Rodent ◽

Risk Of Predation

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 caged-live weasels and spread weasel scent to simulate increased predation risk in four of eight 0.25-ha outdoor enclosures. We monitored females’ reproduction in three periods (May, July, August), i.e. during the breeding season over the course of summer. Key results Contrary to our main prediction, predation risk did not affect timing of mating, pregnancy rate or litter size in any study period. Conclusions and implications We conclude that during the short but resource-rich breeding season of boreal summer, postponing breeding does not seem to be an optimal strategy for females, even under high risk of predation. Under favourable summer condition, i.e. in circumstances without any constraining factors such as food or conspecific density, females manage to balance the costs of predation against benefits of resource availability and do not suppress breeding. Although the BSH has been studied widely, also our results reveal the intricacies of this adaptive behaviour.

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Molecular Detection and Characterization of the First Cowpox Virus Isolate Derived from a Bank Vole

Viruses ◽

10.3390/v11111075 ◽

2019 ◽

Vol 11 (11) ◽

pp. 1075 ◽

Cited By ~ 2

Author(s):

Kathrin Jeske ◽

Saskia Weber ◽

Florian Pfaff ◽

Christian Imholt ◽

Jens Jacob ◽

...

Keyword(s):

Bank Vole ◽

Large Scale ◽

Reservoir Host ◽

Myodes Glareolus ◽

Phenotypic Characterization ◽

Cowpox Virus ◽

Bank Voles ◽

Wide Range ◽

Common Voles

Cowpox virus (CPXV) is a zoonotic orthopoxvirus (OPV) that infects a wide range of mammals. CPXV-specific DNA and antibodies were detected in different vole species, such as common voles (Microtus arvalis) and bank voles (Myodes glareolus). Therefore, voles are the putative main reservoir host of CPXV. However, CPXV was up to now only isolated from common voles. Here we report the detection and isolation of a bank vole-derived CPXV strain (GerMygEK 938/17) resulting from a large-scale screening of bank voles collected in Thuringia, Germany, during 2017 and 2018. Phylogenetic analysis using the complete viral genome sequence indicated a high similarity of the novel strain to CPXV clade 3 and to OPV “Abatino” but also to Ectromelia virus (ECTV) strains. Phenotypic characterization of CPXV GerMygEK 938/17 using inoculation of embryonated chicken eggs displayed hemorrhagic pock lesions on the chorioallantoic membrane that are typical for CPXV but not for ECTV. CPXV GerMygEK 938/17 replicated in vole-derived kidney cell lines but at lower level than on Vero76 cell line. In conclusion, the first bank vole-derived CPXV isolate provides new insights into the genetic variability of CPXV in the putative reservoir host and is a valuable tool for further studies about CPXV-host interaction and molecular evolution of OPV.

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A large panel of novel microsatellite markers for the bank vole (Myodes glareolus)

Molecular Ecology Resources ◽

10.1111/j.1755-0998.2008.02228.x ◽

2008 ◽

Vol 8 (5) ◽

pp. 1164-1168 ◽

Cited By ~ 23

Author(s):

K. RIKALAINEN ◽

A. GRAPPUTO ◽

E. KNOTT ◽

E. KOSKELA ◽

T. MAPPES

Keyword(s):

Microsatellite Markers ◽

Bank Vole ◽

Myodes Glareolus ◽

Large Panel ◽

Bank Vole Myodes Glareolus

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Rodent host population dynamics drive zoonotic Lyme Borreliosis and Orthohantavirus infections in humans in Northern Europe

Scientific Reports ◽

10.1038/s41598-021-95000-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Mahdi Aminikhah ◽

Jukka T. Forsman ◽

Esa Koskela ◽

Tapio Mappes ◽

Jussi Sane ◽

...

Keyword(s):

Population Dynamics ◽

Lyme Borreliosis ◽

Bank Vole ◽

Myodes Glareolus ◽

Northern Europe ◽

Time Lags ◽

Rodent Population ◽

Vole Cycles ◽

Infection Dynamics ◽

Abundance Fluctuations

AbstractZoonotic diseases, caused by pathogens transmitted between other vertebrate animals and humans, pose a major risk to human health. Rodents are important reservoir hosts for many zoonotic pathogens, and rodent population dynamics affect the infection dynamics of rodent-borne diseases, such as diseases caused by hantaviruses. However, the role of rodent population dynamics in determining the infection dynamics of rodent-associated tick-borne diseases, such as Lyme borreliosis (LB), caused by Borrelia burgdorferi sensu lato bacteria, have gained limited attention in Northern Europe, despite the multiannual abundance fluctuations, the so-called vole cycles, that characterise rodent population dynamics in the region. Here, we quantify the associations between rodent abundance and LB human cases and Puumala Orthohantavirus (PUUV) infections by using two time series (25-year and 9-year) in Finland. Both bank vole (Myodes glareolus) abundance as well as LB and PUUV infection incidence in humans showed approximately 3-year cycles. Without vector transmitted PUUV infections followed the bank vole host abundance fluctuations with two-month time lag, whereas tick-transmitted LB was associated with bank vole abundance ca. 12 and 24 months earlier. However, the strength of association between LB incidence and bank vole abundance ca. 12 months before varied over the study years. This study highlights that the human risk to acquire rodent-borne pathogens, as well as rodent-associated tick-borne pathogens is associated with the vole cycles in Northern Fennoscandia, yet with complex time lags.

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Low-level environmental metal pollution is associated with altered gut microbiota of a wild rodent, the bank vole (Myodes glareolus)

The Science of The Total Environment ◽

10.1016/j.scitotenv.2021.148224 ◽

2021 ◽

pp. 148224

Author(s):

Ilze Brila ◽

Anton Lavrinienko ◽

Eugene Tukalenko ◽

Frauke Ecke ◽

Ilia Rodushkin ◽

...

Keyword(s):

Gut Microbiota ◽

Bank Vole ◽

Metal Pollution ◽

Myodes Glareolus ◽

Wild Rodent ◽

Low Level ◽

Bank Vole Myodes Glareolus

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

Wildlife Research ◽

10.1071/wr08031 ◽

2010 ◽

Vol 37 (4) ◽

pp. 273 ◽

Cited By ~ 11

Author(s):

Karen Fey ◽

Peter B. Banks ◽

Hannu Ylönen ◽

Erkki Korpimäki

Keyword(s):

Baltic Sea ◽

Predation Risk ◽

Myodes Glareolus ◽

The Baltic Sea ◽

Short Term ◽

Behavioural Responses ◽

Alien Predator ◽

Risk Of Predation ◽

The Baltic ◽

The Impact

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) and a recently invading alien predator, the American mink (Mustela vison), in laboratory. We also studied the short-term responses of free-ranging field voles and bank voles (Myodes glareolus) to simulated predation risk by alien mink on small islands in the outer archipelago of the Baltic Sea. Key results. In the laboratory, voles avoided odour cues of native weasel but not of alien mink. It is possible that the response to mink is a context dependent learned response which could not be induced in the laboratory, whereas the response to weasel is innate. In the field, however, voles reduced activity during their normal peak-activity times at night as a response to simulated alien-mink predation risk. No other shifts in space use or activity in safer microhabitats or denser vegetation were apparent. Conclusions. Voles appeared to recognise alien minks as predators from their odours in the wild. However, reduction in activity is likely to be only a short-term immediate response to mink presence, which is augmented by longer-term strategies of habitat shift. Because alien mink still strongly suppresses vole dynamics despite these anti-predator responses, we suggest that behavioural naiveté may be the primary factor in the impact of an alien predator on native prey. Implications. Prey naiveté has long been considered as the root cause of the devastating impacts of alien predators, whereby native prey simply fail to recognise and respond to the novel predation risk. Our results reveal a more complex form of naiveté whereby native prey appeared to recognise alien predators as a threat but their response is ultimately inadequate. Thus, recognition alone is unlikely to afford protection for native prey from alien-predator impacts. Thus, management strategies that, for example, train prey in recognition of novel threats must induce effective responses if they are expected to succeed.

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The spatial genetic structure of bank vole (Myodes glareolus) and yellow-necked mouse (Apodemus flavicollis) populations: The effect of distance and habitat barriers

Animal Biology ◽

10.1163/157075609x437691 ◽

2009 ◽

Vol 59 (2) ◽

pp. 169-187 ◽

Cited By ~ 19

Author(s):

Michal Kozakiewicz ◽

Alicja Gryczyńska–Siemiątkowska ◽

Hanna Panagiotopoulou ◽

Anna Kozakiewicz ◽

Robert Rutkowski ◽

...

Keyword(s):

Genetic Diversity ◽

Genetic Structure ◽

Bank Vole ◽

Microsatellite Loci ◽

Myodes Glareolus ◽

Apodemus Flavicollis ◽

Island Populations ◽

Local Populations ◽

Bank Vole Myodes Glareolus ◽

Yellow Necked Mouse

AbstractHabitat barriers are considered to be an important factor causing the local reduction of genetic diversity by dividing a population into smaller sections and preventing gene flow between them. However, the “barrier effect” might be different in the case of different species. The effect of geographic distance and water barriers on the genetic structure of populations of two common rodent species – the yellow-necked mouse (Apodemus flavicollis) and the bank vole (Myodes glareolus) living in the area of a lake (on its islands and on two opposite shores) was investigated with the use of microsatellite fragment analysis. The two studied species are characterised by similar habitat requirements, but differ with regard to the socio-spatial structure of the population, individual mobility, capability to cross environmental barriers, and other factors. Trapping was performed for two years in spring and autumn in north-eastern Poland (21°E, 53°N). A total of 160 yellow-necked mouse individuals (7 microsatellite loci) and 346 bank vole individuals (9 microsatellite loci) were analysed. The results of the differentiation analyses (FST and RST) have shown that both the barrier which is formed by a ca. 300 m wide belt of water (between the island and the mainland) and the actual distance of approximately 10 km in continuous populations are sufficient to create genetic differentiation within both species. The differences between local populations living on opposite lake shores are the smallest; differences between any one of them and the island populations are more distinct. All of the genetic diversity indices (the mean number of alleles, mean allelic richness, as well as the observed and expected heterozygosity) of the local populations from the lakeshores were significantly higher than of the small island populations of these two species separated by the water barrier. The more profound “isolation effect” in the case of the island populations of the bank vole, in comparison to the yellow-necked mouse populations, seems to result not only from the lower mobility of the bank vole species, but may also be attributed to other differences in the animals' behaviour.

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The Sexual and Reproductive Functions, Normal and Perverted, in Relation to Insanity. I. Menstruation: its Commencement, Irregularities, and Cessation. II. the Sexual Instinct and its Abuse. III. Pregnancy, Parturition, etc

Journal of Mental Science ◽

10.1192/bjp.34.147.383 ◽

1888 ◽

Vol 34 (147) ◽

pp. 383-393

Author(s):

Campbell Clark

Keyword(s):

Open Field ◽

Mental Disease ◽

General Medicine ◽

Wide Range ◽

Psychological Medicine ◽

Collective Experience ◽

The Subject ◽

Present Opportunity

In undertaking to introduce a discussion on this very large and important question, I am conscious of my inability to do it justice. No one can possibly cover the wide range of subjects comprised in it; and I am anxious rather to elicit the convictions of more experienced men than to obtrude my own crude and imperfect ideas. My purpose is, therefore, to state the case as briefly as possible, and to introduce questions for discussion in preference to merely ventilating my own ideas. In this way we may arrive at some common points of agreement and materially advance our knowledge of the subject. There can be no two opinions as to the advantage of bringing to a focus the collective experience and conclusions of the various sections of our profession interested in this field of research, and the present opportunity is a particularly good one. The title of the discussion embraces a great deal, and yet does not strictly include topics which might be considered relevant, particularly therapeutics. My aim at the outset will be to invite your special attention to a few questions only, and in order to make the most of our time and concentrate the discussion as much as possible I propose to take each division separately. The subject, viewed as a whole, is so far-reaching and practical as to possess uncommon interest, for it links together medicine and psychological medicine, it gives an open field of discussion to general medicine, obstetrics, and psychology, and it views insanity on its less speculative side, because the more materialistic functions are brought out in strong relief, and sometimes even overshadow the characters of mental disease.

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