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Boxplots of the weight change of male voles separated by treatment. Asterisks symbolize a significant difference from the control group at P > 0.05.

Boxplots of the weight change of male voles separated by treatment. Asterisks symbolize a significant difference from the control group at P > 0.05.

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Article
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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 s...

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... Conversely, Haapakoski et al. (2018) demonstrated that secondary exposure of wild bank voles (Myodes glareolus) to bedding used by individuals who had been directly exposed to predator odors increased the former's subsequent litter size. Sievert et al. (2019) also found that in bank voles, exposure to predator odors and conspecific alarm pheromones led to higher pregnancy rates and increased offspring birth weights. Defensive responses in rodent species may also be sensitive to other environmental cues, besides predator olfactory cues, in the immediate vicinity. ...
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In rodents, defensive behaviors increase the chances of survival during a predator encounter. Observable rodent defensive behaviors have been shown to be influenced by the presence of predator odors and nearby environmental cues such as cover, odors from conspecifics and food availability. Our experiment tested whether a predator scent cue influenced refuge preference in meadow voles within a laboratory setting. We placed voles in an experimental apparatus with bedding soaked in mink scent versus olive oil as a control across from four tubes that either contained (a) a dark plastic covering, (b) opposite-sex conspecific odor, (c) a food pellet, or (d) an empty, unscented space. A three-way interaction of tube contents, subject sex, and the presence of mink or olive oil on the preference of meadow voles to spend time in each area of the experimental apparatus and their latency to enter each area of the apparatus revealed sex differences in the environmental preference of meadow voles facing the risk of predation. The environmental preference of female, but not male, meadow voles was altered by the presence of mink urine or olive oil. A similar trend was found in the latency of males and females to enter each area of the experimental apparatus. These differences suggest that each sex utilizes different methods to increase their fitness when experiencing a predation risk. The observed sex differences may be explained by the natural history of voles owing to the differences in territorial range and the dynamics of evasion of terrestrial predators.
... This assumes that the odors are carried into the nest in the fur of the mother and the combination of the odor and potential changes in maternal care and/or increased stress hormone levels in the milk will trigger aversive behavior. Third, we predicted that offspring would forage less in the presence of PO and CAC, regardless of their mother's treatment (Brown, 1988;Sievert et al., 2019). Fourth, we predicted increased latencies to investigate foraging options, reduced time spent in foraging chambers, and fewer foraging chamber visits in chambers with PO or CAC compared to the control chamber (Apfelbach et al., 2015;Sievert and Laska, 2016;Parsons et al., 2018;Sievert et al., 2019). ...
... Third, we predicted that offspring would forage less in the presence of PO and CAC, regardless of their mother's treatment (Brown, 1988;Sievert et al., 2019). Fourth, we predicted increased latencies to investigate foraging options, reduced time spent in foraging chambers, and fewer foraging chamber visits in chambers with PO or CAC compared to the control chamber (Apfelbach et al., 2015;Sievert and Laska, 2016;Parsons et al., 2018;Sievert et al., 2019). Prediction three and four assume that PO and CAC carries information about an increased risk and therefore these compartments will be largely avoided and not used for foraging (Brown, 1988). ...
... For example, exposure might communicate more about the unfamiliar conspecific male (Eccard et al., 2017) than about the predator that male encountered. While this possibility cannot be ruled out in the current study, previous work in bank voles revealed different reactions to the CAC produced by predator exposed male voles and the "normal" odors produced by unexposed male voles Sievert et al., 2019). Furthermore, we have recently analyzed possible molecular candidates for alarm substances in the bank vole (Sievert, 2020) showing that differences in chemical odor composition are only caused by the treatments (i.e., no handling, handling, and weasel exposure) and show no significant differences based on the sex of the individual. ...
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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 common predator, the least weasel, (2) odor produced by predator-exposed conspecifics, which we call conspecific alarm cue (CAC), or (3) control odor (C). We monitored postnatal pup growth, and we quantified foraging and exploratory behaviors of 4-week-old pups following exposure of their mothers to each of the three odour treatments. Exposure to odors associated with predation risk during development affected the offspring behavior, but the timing of exposure, i.e., pre-vs. postnatally, had only a weak effect. The two non-control odors led to different behavioral changes: an attraction to CAC and an avoidance of PO. Additionally, pup growth was affected by an interaction between litter size and maternal treatment, again regardless of timing. Pups from the CAC maternal treatment grew faster in larger litters; pups from the PO maternal treatment tended to grow faster in smaller litters. Thus, in rodents, offspring growth and behavior are seemingly influenced differently by the type of predation risk perceived by their mothers.
... After perceiving increased predation risk, multiple mechanisms and adaptations by prey animals are possible, from simple immediate behavioural responses to long-term physiological or even intergenerational adaptations (Abrams 2000). Anti-predatory behaviours employed in prey range from simple avoidance of high-risk areas (Ferrero et al. 2011;Clinchy et al. 2013;Pérez-Gómez et al. 2015) and freezing to decrease detectability (Wallace and Rosen 2000;Sundell and Ylönen 2004), over changes in vigilance and foraging (Brown 1999;Ylönen and Brown 2007;Embar et al. 2011), to drastic changes in the reproductive behaviours (Ylönen and Ronkainen 1994;Sih 1994;Mappes and Ylönen 1997;Mönkkönen et al. 2009;Haapakoski et al. 2012Haapakoski et al. , 2018Sievert et al. 2019). ...
... Several of the aforementioned species live in social groups, so the secretion of AP serves to warn the group, family or colony. Previous behavioural studies have already shown alarm pheromone effects on reproductive behaviour in bank voles, specifically differences in the number of offspring , the amount of parturitions (Sievert et al. 2019), and several transgenerational effects (Sievert et al. 2020). While the effects of an alarm pheromone exposure have been studied, the actual nature remains unclear. ...
... In our field experiment, no clear difference in foraging effort was observed in the AP GUD was observed on the first day, which is in line with our previous results (Sievert et al. 2019). However, a clear increase in foraging effort in AP patches after just one day, we suggest two factor for explaining this result. ...
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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 chromatography–mass spectrometry, we identified that 1-octanol, 2-octanone, and one unknown compound as the most likely candidates to function as alarm signals. These compounds were independent of the vole’s sex. In a field experiment, voles were foraging less, i.e. they were more afraid in the AP odour foraging trays during the first day, as the odour was fresh, than in the second day. This verified the short lasting effect of volatile APs. Our results clarified the chemistry of alarming body odour compounds in mammals, and enhanced our understanding of the ecological role of AP and chemical communication in mammals.
... This might raise the question whether the method to collect AP is suitable. However, studies using a similar method Sievert et al. 2019) clearly showed significant changes in voles when presented with the AP cue. ...
Thesis
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Predator-prey interactions are a major evolutionary driver, affecting not only the direct mortality of prey species, but also their behaviours and reproduction. Prey species behavioural adaptations aim to mitigate the effects of predation and to maximise survival and individual fitness. These adaptations include the ability to signal a threat to conspecifics, e.g. via alarm calls or alarm secretions, or to detect predator presence via odours. In this thesis, I studied the effects of predator odours and conspecific alarm secretions on behaviour and reproduction bank voles (Myodes glareolus), a small mammal species inhabiting boreal forests. My work focused on three major points in comparing the direct predator cue and indirect conspecific cue: first, how the reproductive behaviour is affected by the predator odour or alarm pheromone, second, whether there are transgenerational effects and how they are exhibited in offspring, and third, what the chemical nature of these alarm secretions is. I conducted four experiments, which included both trials in semi-natural enclosures and under controlled laboratory conditions. I found evidence that exposure to conspecific alarm secretions causes a shift in voles’ reproductive behaviour, switching towards terminal investment. This became apparent with an increase in parturitions and an increased growth rate in larger litters, which did not occur when exposed to predator odour. I also found evidence of transgenerational effects, which affect aspects of the offspring’s exploratory and foraging behaviour. Additionally, I discovered that these behavioural effects are context-dependent and do not occur in every environment. Lastly, I identified a group of chemicals from voles’ alarm secretion, which are likely to be responsible for the observed effects. The results of my thesis fill a knowledge gap concerning chemical communication in mammals, and help to further understand the implications of predator presence on prey behaviour and reproduction.
... When the chance of survival for offspring is already low, it would benefit Brandt's voles to produce more female offspring. Sievert et al. (2019) found similar results, wherein both predator odors and alarm pheromones enhanced reproduction compared to that observed with exposure to a control odor. The impact of a predator can be socially transmitted, as predation risk can exert population-level effects through alarm pheromones, which are pheromones released by predatorstressed conspecifics (Haapakoski et al. 2018). ...
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Animals may use different reproductive strategies depending on environmental conditions. This study investigated the effects of maternal stress induced by exposure to predator odors on reproductive output and adult offspring quality in pregnant Brandt’s voles (Lasiopodomys brandtii). We exposed pregnant Brandt’s voles to cat urine, rabbit urine, or distilled water for 18 days (1 h/day). Our results indicated that pregnant voles in the cat odor-exposed group tended to produce more offspring and the number of viable female offspring was larger. However, we did not observe any differences in the sex ratios of vole offspring among the three treatment groups. Compared with the control (distilled water) group, female offspring of voles in the cat odor-exposed group had lower body weights, lengths, and smaller body weights in relation to body length, whereas they had larger ovaries in relation to body weight. Furthermore, the female offspring of the voles exposed to the cat odor had higher concentrations of serum estradiol and higher levels of gonadotropin-releasing hormone mRNA in the hypothalamus compared with the female offspring of the voles in the control group. However, we observed no differences among the male offspring in the three treatment groups. Our findings suggest that pregnant Brandt’s voles suffering from chronic exposure to predator odors will produce greater numbers of low-weight female offspring that probably possess higher breeding potential to improve the fitness via regulation of the hypothalamic-pituitary-gonadal axis.
... This might raise the question whether the method to collect AP is suitable. However, studies using a similar method (Haapakoski et al. 2018;Sievert et al. 2019) clearly showed significant changes in voles when presented with the AP cue. ...
Article
Full-text available
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.
... The partly contradictory studies may provide a synthesis in the form of variability of breeding strategies in animals: whether to invest in own survival and decrease breeding activity, suppressing or delaying reproduction (Ylönen 1994;Ylönen & Ronkainen 1994), along with other activities like moving and foraging. Alternatively, the second option is to invest in intensive reproduction, even with the risk of being the last one, with the hope that at least one pup will survive over the period of high risk (Duffield et al. 2017;Haapakoski et al. 2018;Sievert et al. 2019). The latter theoretical strategy, bet-hedging or terminal investment, has been documented in numerous taxa depending on either intrinsic factors like individuals' age or extrinsic threat factors for survival, like predation or parasitism (see tables 1 and 2 in the review by Duffield et al. 2017). ...
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Climate change, habitat loss and fragmentation are major threats for populations and 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 years 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 arms race between prey voles and weasels along the multiannual density fluctuation, affected by the climate change, and especially the change in duration and stability of snow cover. Snow provides for ground‐dwelling small mammals thermoregulation, shelter for nest sites, and hide from most predators. Predicted increase in instability of winter forms a major challenge for species with coat color change between brown summer camouflage and white winter coat. One of these is the least weasel, Mustela nivalis nivalis. Increased vulnerability of wrong‐colored weasels to predation affect vole populations and may have dramatic effects on vole dynamics. It may have cascading effects to other small rodent – predator interactions and even to plant – animal interactions and forest dynamics.
Technical Report
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Updated tables, figures and references of Palme, 2019, and the respective supplements (Date: 2nd Jan 2023)
Article
Scent marks are an important means of transmitting information between rodents, and they can be produced from several body sources. Previous studies have shown that scents from multiple sources can convey the same information; female meadow voles, for example, have three scent sources that communicate sex. However, possessing three separate sources that convey the same information is likely costly due to the metabolic energy required to produce these signals and the increased chance that eavesdropping individuals may intercept information present in these signals. In this study, we investigated if these scent sources could communicate other information, in addition to scent donor sex, by determining if male meadow voles could distinguish scent marks taken from different sources of a single female scent donor. This was accomplished with a habituation-test method, that allowed us to compare how male meadow voles differently investigate scent from a familiar and novel source of a female scent donor. Male meadow voles could distinguish between faeces and urine scent marks of a female, but could only distinguish mouth from urine and faeces scent marks when first familiarized with mouth scent marks. Our findings suggest that mouth, urine, and faeces scent marks of female meadow voles produce both redundant and distinct information. The overlap in information between scent marks produced from separate sources may be needed to provide social context, which allows receiving individuals to accurately weigh the tradeoffs associated with responding to an olfactory cue. While this overlap in information remains costly, this cost may be minimized by the different fade-out times of scent marks from distinct body sources, which may limit the amount of time information in a scent mark is available to a time period where this information is socially relevant.