Population cycles and outbreaks of small rodents : ten essential questions we still need to solve

Correction: 10.1007/s00442-021-04856-4, Oecologia (2021)Most 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 important issues that are essential for understanding the generality of small rodent population dynamics.Peer reviewe

Behavioural responses of mice to predator odour components

Having means to detect and avoid potential predators is a necessity for prey species. Most mammalian prey species are able to detect odours emitted by predators and to adapt their behaviour accordingly. These odour cues are therefore considered to act as semiochemicals. Predator odours consist of several dozen different odourants. In order to assess if single odourants elicit aversive behavioural reactions, predator-naïve CD-1 mice were presented with six odourants which are part of body-borne odours of different mammalian predator species. A two-compartment chamber was used in order to assess place-preference, motor activity and faecal excretions when the animals were simultaneously presented with a predator odourant and a blank control. Further trials were performed to assess whether the odourant concentrations had an influence on the behaviours. The only odourant that elicited a significant aversion was 3-methyl-1-butanethiol, a compound found in the anal gland secretion of skunks, when presented at a factor of 100 above the olfactory detection threshold of mice. Two other concentrations of 3-methyl-1-butanethiol did not elicit significant behavioural changes. Based on the present study, only one out of six selected predator odourants elicited a significant aversive response in CD-1 mice. This suggests that more than one odour component, or perhaps even the full mixture of odourants, may be necessary for CD-1 mice to respond to a predator odour with aversive behaviour

Indirect and Transgenerational Effects of Predation Risk: Predator Odour and Alarm Pheromones in the Bank Vole

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. Keywords: Behaviour; chemical communication; cross-generational effect; fear effect; predator-prey-interaction; terminal investment.Pedon ja saaliin evolutiivinen kilpajuoksu ilmenee kahtaalla, saaliin kuolleisuutena sekä selvinneen saaliin käyttäytymisen ja lisääntymisen muutoksina, jotka parantavat sen hengissä säilymistä ja kelpoisuutta. Saalis pystyy välttämään pedon, jos se havaitsee sen. Saaliseläin voi aistia pedon suoraan sen jättämistä ärsykkeistä, kuten äänistä tai hajuista, tai epäsuorasti varoituksena muilta oman lajin yksilöiltä. Väitöstutkimukseni keskittyi petoriskisignaalien, pedon hajun ja petoriskille altistuneen oman lajin yksilön hajun, vaikutuksiin saaliin käyttäytymiseen ja lisääntymiseen. Tutkimuslajini olivat maamme metsien yleinen jyrsijä, metsämyyrä, ja sen merkittävä spesialistipeto, lumikko. Tutkimukseni neljä osatutkimusta keskittyivät kolmeen pääkysymykseen: miten suora pedon haju tai epäsuora, lajitoverin kautta tuleva hälytyshaju vaikuttaa metsämyyrän lisääntymiseen; onko vanhempien, etenkin äidin, altistumisella korkeaan petoriskiin vaikutuksia raskausajan tai imetyksen kautta poikasten pedonvälttämiskäyttäytymiseen; sekä mitkä kemialliset yhdisteet olisivat hälytysferomonin välittämän informaation taustalla. Metsämyyrän lisääntyminen ja käyttäytyminen muuttuivat suoran ja epäsuoran petoärsykkeen vaikutuksesta. Hälytysferomoni näytti muuttavan myyrän lisääntymisstrategiaa siten, että naaras lisääntyi tehokkaammin. Tämä näkyi niin lisääntyvien yksilöiden määrässä kuin poikasten kasvunopeudessakin, etenkin isoissa poikueissa. Ilmiö on yhteensopiva niin sanotun ”terminaalivaiheen investointi” -hypoteesin kanssa. Tutkimukseni vahvisti myös mahdollisten sukupolvien välisten petoriskivaikutusten olemassaolon. Lisäksi osoitin, että erityisesti kahdella yhdisteellä, 2- ja 1-oktanolilla, saattaisi olla merkittävä rooli petoriskin kemiallisessa signaloinnissa, sekä todensin, että oletustemme mukaisesti hälytysferomonin vaikutus luonnossa oli lyhytaikainen. Avainsanat: Hajuainekommunikaatio; hälytysferomoni; käyttäytyminen; lisääntymisstrategiat; peto-saalis –suhde; sukupolvien väliset vaikutukset

Pre- and Postnatal Predator Cues Shape Offspring Anti-predatory Behavior Similarly in the Bank Vole

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.peerReviewe

In utero behavioral imprinting to predation risk in pups of the bank vole

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.peerReviewe

Bank vole alarm pheromone chemistry and effects in the field

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.peerReviewe