Chemical alarm communication in mammals

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.

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 subsequently affects recipient behavior. Parents may also transfer their experience with predators to their offspring. In two experiments, we assessed how direct and indirect predation cues affect bank vole (Myodes glareolus) foraging behavior, reproduction, and pup fitness. Weasel (Mustela nivalis) odor served as the direct cue, whereas the odor of weasel‐scared conspecifics, alarm pheromones, was used as an indirect cue and both of those were compared to a control odor, clean wood shavings. Alarm pheromones attracted female voles, measured as time in proximity to the treatment and foraging. Both predator odor and alarm pheromones enhanced reproduction compared to the control odor. Females treated with alarm pheromone had significantly higher pregnancy rates, and pups from predator‐treated mothers were significantly heavier at birth. Our study provides two novel ideas. First, the impact of a predator can be socially transmitted. Second, predation risk likely triggers terminal investment in reproduction.

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.

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.