Hannu Ylönen

Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment

SummaryIn northern Fennoscandia, microtine rodent populations fluctuate cyclically. The environment of an individual vole can be considered to be predictable when the risks of predation and intra- and interspecific competition change with the cycle, such that both are high during the population highs of voles. The risk of predation is also high during the vole crash. After the crash, the vole population is characterized by low intra- and interspecific competition and low predation pressure. The main predators affecting voles during the crash are the small mustelids, least weasel and stoat. The density of these specialist predators declines drastically during the winter after the vole crash. We studied experimentally the impact of the perceived presence of stoats on the breeding and mating behaviour of voles. In a series of breeding experiments with bank voles,Clethrionomys glareolus, both old and young females suppressed breeding when exposed to the odour of stoats,Mustela erminea. The weights of females decreased in both experimental and control groups, but more among the voles under odour exposition. It seems that females actively avoided copulations under high predation risk and that breeding suppression is mediated by a change in female mating behaviour. There was no change in male behaviour or physical condition between the experimental and control treatments. An alternative mechanism for the observed breeding suppression could be the one caused by decreased feeding in females mediated with low energy intake which does not allow breeding. Regardless of its mechanism, delay of breeding should increase the probability of non-breeding females to survive to the next breeding season. The females surviving the crash should gain a strong selective advantage in a predator-free environment of the subsequent breeding season, which could explain the adaptive function of this antipredatory strategy.

Behaviour of cyclic bank voles under risk of mustelid predation: do females avoid copulations?

Mustelid odours have been shown to suppress breeding in captive bank voles (Clethrionomys glareolus) from cyclic populations (Ylönen 1989; Ylönen and Ronkainen 1994). The mechanism behind the suppression is unknown. Based on a series of behavioural trials and breeding experiments with pairs of bank voles in breeding condition, we suggest that the primary cause for breeding suppression is a change in female mating behaviour. Experimental female-male pairs (n=34) exposed to mustelid odour decreased their general activity compared to control pairs (n=34). When encountering males in behavioural trials, females exposed to stoat odour were more aggressive and actively avoided precopulatory behaviours of males. No copulations were observed in experimental pairs compared to five in control pairs during the behavioural trials. Males actively approached females in general but male behaviour did not change under exposure to mustelid odours. We suggest that females are more vulnerable to mustelid predators than males and therefore actively avoid copulations in the (indirect) presence of mustelids. As well as this behavioural response, internal abortive mechanisms (cf. Bruce 1959) could play a role in the observed breeding suppression.

Considerations of optimal litter size in mammals

Recent advances in understanding mammalian reproductive patterns mirror general developments in phylogenetic, physiological, and ecological research. We provide an overview of the diverse approaches used in studying mammalian litter size and discuss recent advances in evolutionary ecological theory and experimental data concerning reproductive patterns. Extensively documented natural history studies and breeding data from work in applied zoology and animal husbandry constitute a rich source of information for comparative studies. Such studies have helped identify fundamental differences in reproductive strategies depending on whether taxa produce altricial or precocial young and whether a given reproductive effort results in a single offspring or a litter. On the other hand, research on ecological and physiological correlates of litter size is providing new insights about reproductive energetics, the relationship between resource availability and litter size, and optimality in varying environments in general. Continuing experimental approaches are broadening our understanding of the mechanistic bases of patterns of mammalian litter size, but such studies, especially those involving manipulation of litter size, must carefully consider the potential biases introduced by experimentally induced non-congruence between preand postnatal litter sizes. For example, without accounting for the effects of placental hormones on mammogenesis and lactation, postnatal manipulations of litter size might be based on faulty assumptions implicit in such manipulations. To conclude, despite substantial advances in these diverse approaches, our degree of understanding of optimal litter size in mammals remains unclear because of inconsistencies in data often used in comparative studies and because of physiological and ecological constraints on litter size adjustments that hinder or bias experimental approaches. These areas should be addressed in future studies.

Reproductive effort of female bank voles in a risky environment

SummaryIn cyclically fluctuating vole populations, strong intraspecific competition and intense predation simultaneously or separately increase the costs of reproduction and so may set the framework for the optimal breeding tactic of voles. In a factorial experiment, we manipulated two factors in the breeding environment of bank vole (Clethrionomys glareolus) pairs, each with two treatment levels: no predation risk or high risk of specialist predators and low or high density of voles. In the manipulation, we used odours of conspecific voles and/or mustelid predators. Both over-wintered and young, summer-born, wild-caught bank vole females and males in breeding condition were used. Each female-male pair of voles was placed in a cage and the cages were distributed in large outdoor enclosures. All animals were fed ad libitum. Under predation risk, both old and young females suppressed breeding significantly. The density of conspecific voles did not affect overall breeding. However, there was some evidence that population density stimulated breeding of old females but suppressed breeding of young ones. Both risk factors appeared to increase litter sizes of those individuals who ‘decided’ to breed. Our results indicate that the risk of predation may be an important factor determining reproductive tactics of bank vole females. In risky environments, females seemed to choose between two totally opposite tactics: they suppressed breeding, which may increase their own survival to the next breeding event, or they continued to breed in spite of expected high survival costs. Females seemed to compensate the latter costs with a higher effort to the current and probably the last reproduction.

Behaviour and choice of refuge by voles under predation risk

Animals often show a strong antipredatory response when they are exposed to their most deadly predator. In northern vole populations, the least weasel, Mustela nivalis nivalis, is probably the most important predator of voles. Because of its small size and slender body shape, the least weasel is capable of hunting voles in their burrows. However, small voles can potentially escape weasel predation by selecting holes smaller than those weasels can enter. We studied the choice of nest holes and refuges by two species of voles under simulated predation risk. In a laboratory experiment, voles were provided with four nest boxes as refuges, with individually adjusted entrance sizes. When exposed to the odour of a weasel, voles did not choose the smallest opening; they rather seemed to trade full protection for easy and immediate access by choosing the nest box with an intermediate entrance size. When outside the nest at the time when a weasel entered the arena, voles avoided the refuges with the smallest holes. In addition to using refuges on ground level, voles climbed on top of the boxes as an escape reaction, as well as exhibiting a variety of behavioural responses, such as fast running, freezing and sneaking.

Effects of competition and season on survival and maturation of young bank vole females

In territorial microtines intra-specific density dependent processes can limit the maturation of individuals during the summer of their birth. This may have demographic consequences by affecting the number and the age distribution of breeding individuals in the population. Little is known about this process on a community level, though populations of many northern microtine species fluctuate in synchrony and are known to interfere socially with each other. We experimentally studied the influence of the field vole Microtus agrestis on maturation, breeding, space use and survival of weanling bank voles, Clethrionomys glareolus. Two additive competition experiments on bank vole populations were conducted in large outdoor enclosures, half of them additionally housing a field vole population. In a mid-summer experiment low population density and absence of older breeding females minimised intra-specific competition. Survival was not affected by the presence of field voles. Season had a significant effect on both the probability of maturation and breeding of the weanlings. Competition with field voles significantly delayed breeding, and coupled with seasonal effects decreased the probability of breeding. In a late-summer experiment breeding and survival of bank vole weanlings were studied for three weeks as part of a high density breeding bank vole population. Weanlings did not mature at all nor were their space use and survival affected by the presence of field voles. Our results show that competition with other species can also have an impact on breeding of immatures. In an extreme seasonal environment, even a short delay of breeding may decrease survival chances of offspring. Seasonal and competition effects together may thus limit the contribution of year born females to reproductive output of the population. Other studies have shown that adult breeding bank voles suffer lower survival in the presence of field voles, but this study showed no survival effects on the weanlings. Thus it might be beneficial for weanlings to stay immature especially in the end of the breeding season and postpone reproduction to the next breeding season if densities of competing species are high.

Phenotypic Flexibility in the Social Organization of Clethrionomys

I review the flexibility of social organization and spacing behavior in Clethrionomys. This review is based on a 6-year comparative study and several experimental studies on cyclic populations of the bank vole, C. glareolus, in Central Finland. The social organization of Clethrionomys populations shows great flexibility during both the breeding and nonbreeding season, and is dependent on habitat patchiness, food availability, Predation, kinship, philopatry, and familiarity between individuals. The first three factors are most important in destabilizing a population, whereas the last three stabilize a population without exhausting its resources. Female territoriality can weaken in a productive environment perhaps due to increasing kinship between reproductive females during the breeding season. During the winter, food availability seems to determine the social structure of the population, which consists of either large or small aggregations of both sexes. Winter territoriality may be influenced by relatively homogenous habitat with low productivity. Forest-dwelling species of Clethrionomys seem to adopt behavioral tactics different from those of most Microtus that live in a productive, but unstable habitat. Despite these behavioral differences, both genera cycle synchronously in northern Fennoscandia. This leads to the conclusion that we have to seek explanations for microtine cycles not based on the behavior of individual voles.

Animal protein as a reproductive constraint in spring reproduction of the bank vole

ABSTRACT Survival conditions over the winter and determinants of variability in the onset of reproduction are major factors shaping the life history of most organisms in strongly seasonal environments. During the long non-breeding season availability and quality of food may be major constraints determining the onset of reproduction. We studied the effects of supplemental animal protein over winter on the onset of reproduction in the bank vole, Clethrionomys glareolus, an iteroparous seasonal breeder, granivorous-herbivorous, with small amounts of animal food in its diet. We predicted that animal protein would be especially important during spring, when energy demands are increasing due to the onset of reproduction and availability of new plant food is still limited. Field experiments were conducted in 6 open forest plots (2.25 ha each), and bank voles were fed supplemental whey protein during the winter and spring. Supplemented males were heavier at the onset of reproduction than non-supplemented males. Maturation and parturition of first litter occurred significantly earlier in females fed supplemental animal protein. No differences in litter size and litter mass were detected between treatments. We conclude that animal protein in the form of whey may play an important role in the timing of spring reproduction. Therefore, natural animal protein food sources like insects, pupae, and possibly carcasses of mammals and birds gain importance for the onset of breeding even in an granivorous-herbivorous species like the bank vole.

Who eats first? Uptake of pellet bait by target and non-target species

House mice (Mus domesticus) are an important vertebrate pest in Australian agriculture. We studied the uptake of non-toxic placebo bait pellets targeted on house mice from bait stations in the grain-growing region of southeastern Australia. Bait stations allowed access for either ants; ants and mice or ants, mice, and birds. Soy meal bait pellets offered in December were of low preference for both ants and mice, but were eaten by birds in one study plot. In January, there were no differences between bait stations in the amount of wheat bait pellets removed indicating that the pellet bait had been primarily removed by ants. Most pellet bait was removed during the first 12 h after distribution. The results indicate that non-target species consumed pellet bait quicker than house mice. This has to be taken into account if similar bait pellets are to be used as carriers of lethal or sterility agents to manage house mouse populations.

Behaviour and resource use of two competing vole species under shared predation risk

Indirect interaction between two competing species via a shared predator may be an important determinant of population and community dynamics. We studied the effect of predation risk imposed by the least weasel Mustela nivalis nivalis on space use, foraging and activity of two competing vole species, the grey-sided vole Myodes rufocanus, and the bank vole Myodes glareolus. The experiment was conducted in a large indoor arena, consisting of microhabitat structures providing food, shelter, trees for refuge and separated areas with high and low predation risk. Voles were followed for 5xa0days: 2xa0days before, 1xa0day during and 2xa0days after the presence of weasel. Our results suggest an effect of weasel presence on the vole community. Voles of both species shifted their activity from risky to less risky areas, climbed trees more often and were less active. Seed consumption was not affected by weasel presence. The time spent in the risky and less risky area did not differ between species, but bank voles spent more time in trees than grey-sided voles. Males of both species were more exposed to predation risk than females, i.e. generally spent more time in the risky area. Proportion of time spent in the risky area, the use of area, trees and food stations were sex dependent. Activity and use of trees were species dependent. We found no evidence for despotic distribution between our two species, although bank voles seemed to be more affected by coexistence, since they lost weight during the experiment. Based on our results we conclude that predator response was largely similar between species, while the sex-specific responses dominated. Besides a stronger escape response in the bank vole, the strongest individual differences were sex specific, i.e. males were more prone to take risks in space use and activity.