Demography of fluctuating prairie vole populations: comparison of demographic variables among phases of fluctuations

We tested for differences in the proportion of reproductively active males and females, proportion of the population composed of young and immigrants, and monthly survival (total, adult, young) among phases (trough, increase, and decline) and among habitats (alfalfa, bluegrass, and tallgrass) of 30 population fluctuations ofMicrotus ochrogaster Wagner, 1842 over 25 years in east-central Illinois USA. Total population survival and survival of adults and young were greatest during the increase phase, among fluctuations, irrespective of habitat. The proportion of reproductively active adult males and females was lowest during the decline phase, an effect of lower reproduction during the winter. These results suggest that phase-specific changes in survival were the primary demographic factor driving population fluctuations ofM. ochrogaster in our study sites. We conclude that small-scale spatially different population fluctuations may be explained by the same mechanisms that explain fluctuations within a population.     

The influence of immigration on demography of sympatric voles

We studied the influence of immigration on the dynamics ofMicrotus ochrogaster Wagner, 1842 andM. pennsylvanicus Ord, 1815 populations in alfalfa, bluegrass, and tallgrass prairie in east-central Illinois for 25 years. The numbers of immigrants in a site were positively correlated with overall population densities of the species in the vicinity of the study sites and within the study site. Population density of the other species was not correlated with immigration of either species. Immigrants did not differ significantly from residents with respect to sex-ratio and reproductive condition. Persistence of immigrantM. pennsylvanicus was lower than that of resident adults in all three habitats, while that of immigrantM. ochrogaster was lower than that of resident adults in alfalfa, where the species was most abundant. Neither the absolute number of immigrants nor the proportion of the population composed of immigrants indicated an effect of immigrants on among- and within-habitat differences in demography and population fluctuations of either species. Immigrants may have been an important factor in maintenance ofM. pennsylvanicus in alfalfa, a low-quality habitat, but the influence of immigration on the dynamics of populations inhabiting other habitats was insubstantial.     

Vole population dynamics: factors affecting peak densities and amplitudes of annual population fluctuations of<Emphasis Type="Italic">Microtus pennsylvanicus</Emphasis>

We studied factors affecting peak densities and amplitudes of fluctuation during 20 annual population fluctuations ofMicrotus pennsylvanicus Ord, 1815 in alfalfa and bluegrass habitats over a 25-year period. Survival was correlated with population density over the 25 years and was the most consistent variable associated with stoppage of population growth. Although not correlated with population density over the 25 years, a decline in the proportion of reproductively active adult females contributed to cessation of growth of population fluctuations that peaked in late autumn-winter, and to cessation of growth of eight of eleven population fluctuations that peaked during summer-early autumn. We conclude variation in survival to be the primary factor affecting peak densities and amplitudes of population fluctuation ofM. pennsylvanicus.     

Agonistic behaviour in males of five species of voles Microtus

Agonistic behaviour of Microtus pennsylvanicus, M. montanus, M. californicus, M. longicaudus, and M. ochrogaster was observed in 160 staged encounters; a natural observation of sympatric species is included. No difference in the character and movements of agonistic behaviour was apparent when arena size was reduced; only a difference in the frequency of postures and movements was observed. In the smaller arena, M. montanus and M. ochrogaster exhibited a significant increase in frequency of agonistic components. The other three species did not show a significant increase. In interspecific pairings, M. montanus won over M. pennsylvanicus, M. californicus and M. longicaudus; M. ochrogaster won over M. montanus and M. pennsylvanicus. Three species used mutual avoidance in maintaining individual distance.     

Effects of conspecific and heterospecific residents on patterns of immigration in two species of voles

Studies with birds have shown that presence and density of resident conspecifics and heterospecifics can influence patterns of habitat selection. There have been few studies on the effects of social cues on rates of immigration in mammals. We report results from a long-term live trapping study of immigration in two species of voles, Microtus ochrogaster Wagner, 1842 and Microtus pennsylvanicus Ord, 1815, in bluegrass habitat in east-central Illinois, USA. We compare immigration into control sites from which no individuals of either species were removed with immigration into experimental sites from which either conspecifics or heterospecifics were removed. We focus on characteristics of immigrants and rates of immigration in relation to density in destination habitats. Within each species, immigrants into control and removal sites were similar with respect to body mass and reproductive condition, indicating no major differences in the physical condition of immigrants into sites with established populations and sites without established populations. For both species, density of conspecifics at a site positively influenced rate of immigration at that site. Density of heterospecifics at destination sites did not significantly influence rate of immigration for either species. These results suggest that site selection by dispersing M. ochrogaster and M. pennsylvanicus is characterized by conspecific attraction.     

The development of social behaviour between siblings and non-siblings of the voles Microtus ochrogaster and Microtus pennsylvanicus

It has been suggested that the strength and duration of sibling relations during the juvenile period may reflect the social structure of mammal species. Two Microtus species with contrasting social systems, M. ochrogaster and M. pennsylvanicus, were chosen for a comparative study of juvenile social behaviour. Young were observed in sibling and non-sibling dyadic encounters from the second until the seventh week of age. Social interactions consisted mainly of body nosing of the partner, and included behaviours interpreted as investigation, socialization and settling. Only minor sex differences in body nosing scores occurred, but some ontogenetic trends were noted. When the species were compared, M. ochrogaster received higher scores for body nosing and sitting in contact, and displayed more reciprocity in their nosing, than did M. pennsylvanicus, whether siblings or non-siblings were considered. When the sibling types were compared, non-sibling dyads received higher nosing scores than did siblings in both species, but the disparity was greater in M. ochrogaster than in M. pennsylvanicus. These results are interpreted with reference to known behavioural and developmental correlates of the extended family system in naturally occurring M. ochrogaster and the less communal social system in M. pennsylvanicus.     

A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus,the pine vole M. pinetorum and the prairie vole M. cchrogaster

Paternal care in microtines has been studied infrequently and few studies have compared patterns of direct and indirect paternal investment. The paternal behaviour of three vole species, the meadow vole (Microtus pennsylvanicus), the pine vole (M. pinetorum) and the prairie vole (M. ochrogaster) was examined in a semi-natural setting. Prairie and pine voles were found to exhibit high levels of paternal care. Prairie vole males contributed the most direct care by remaining in the natal nest for long periods of time in contact with the pups. Pine voles contributed less direct care than prairie voles as they spent less time in the natal nest with their offspring. In addition, both prairie and pine vole males were observed to groom their pups and retrieve them back to the nest area. Prairie vole males also engaged in such indirect forms of care as nest construction and maintenance, while pine voles provided indirect care in the form of tunnel construction and food caching. Meadow vole males were the least paternal of the three species and rarely engaged in either direct or indirect care. These findings support predictions that M. pennsylvanicus is promiscuous and that male and female meadow voles occupy separate territories. They are also consistent with studies which indicate that prairie and pine voles are monogamous and have a structured social organization with members interacting closely with one another.     

The correlation between demography and metabolic rate: a test using the beach vole (Microtus breweri) and the meadow vole (Microtus pennsylvanicus)

Summary This study examines the hypothesis that mammalian species with wide fluctuations in population size will have greater metabolic rates than species with smaller population fluctuations. We tested this hypothesis using two microtine rodents — the beach vole (Microtus breweri) and the meadow vole (M. pennsylvanicus). Although these species experience similar climatic regimes, eat similar foods, and have a very close phylogenetic relationship, they show marked differences in demography. Microtus pennsylvanicus is prone to large supraannual fluctuations in population size, while M. breweri is essentially acyclical. Metabolic rate (oxygen consumption) of each species was measured using open-flow respirometry at ambient temperatures ranging from 2 to 34° C. Basal metabolic rate of M. pennsylvanicus (1.81 ml O₂ g^–1 h^–1) was significantly greater than that of M. breweri (1.39 ml O₂ g^–1 h^–1). The lower critical temperature, estimated by continuous two-phase regression, was 28.9° C for M. pennsylvanicus and 29.8° C for M. breweri. Regression lines below thermoneutrality did not differ in slope, but the elevation for M. pennsylvanicus was significantly higher. Thus, M. pennsylvanicus has a higher metabolic rate at all temperatures examined. These results support the hypothesis that metabolic rate is positively correlated with the extent of population fluctuation. We suggest that further evidence for, or against, this hypothesis should be found by comparing closely matched species pairs, rather than resorting to confounded allometric comparisons of ecologically and phylogenetically diverse taxa.     

Pregnancy initiation in postpartum estrus in three species of muroid rodents.

Pregnancy initiation in postpartum estrus was studied in 14 male-female pairs of white-footed mice, Peromyscus leucopus; 12 pairs of prairie voles, Microtus ochrogaster; and 14 pairs of montane voles, M. montanus. When mated for one ejaculatory series, the percentages of females pregnant were 25, 43, and 71% for M. ochrogaster, M. montanus, and P. leucopus, respectively. Whereas mating to satiety produced a significant increase in the probability of pregnancy relative to mating for one ejaculatory series in M. montanus, there was no significant difference in P. leucopus. M. ochrogaster did not differ significantly when mated for one ejaculation versus two. P. leucopus resemble P. maniculatus in having a lower stimulus requirement for pregnancy initiation in postpartum than in cycling estrus. M. ochrogaster resemble laboratory rats in having a higher stimulus requirement for pregnancy initiation in postpartum estrus. M. montanus show no significant difference.     

Emigration to new habitats by voles: the cost of dispersal paradox

We tested the hypothesis that dispersal and philopatry are components of a mixed evolutionarily stable strategy (ESS). The hypothesis predicts that fitness of dispersers should be equal to that of philopatric individuals. Alternatively, fitness of dispersers could be lower (the resident fitness hypothesis) or greater (the cost of dispersal hypothesis) than that of philopatric individuals. We compared fitness of individuals that moved to new habitats (emigrants) and those that remained within habitat boundaries (residents) in populations of the prairie vole, Microtus ochrogaster, and the meadow vole, M. pennsylvanicus. We established vole populations in four enclosures (). Within each enclosure, voles were free to move between four types of habitats that varied in the availability of supplemental food and the amount of vegetative cover. We analysed two fitness components: the survival rates of all individuals, and pregnancy rates of females. Our study showed that emigrants generally had greater fitness than residents and that the difference in fitness was habitat dependent (i.e. was greater when individuals were emigrating from low-quality habitats than from high-quality habitats). High-food, high-cover habitats were the only habitat types for which fitness of emigrants was lower than that of residents. Similar patterns occurred in both prairie voles and meadow voles. Our results support the cost of dispersal hypothesis.     

Heterochromatin (C-bands) in somatic and male germ cells in three species ofMicrotinae

The C-banding patterns in the chromosomes ofMicrotus oeconomus, M. arvalis andM. ochrogaster demonstrate differences in the amount and distribution of heterochromatin. Autosomal centromeric heterochromatin appears as conspicuous blocks or as small dots, and in several chromosomes no heterochromatin was detected; interstitial heterochromatin was observed in one autosome pair ofM. ochrogaster. The sex chromosomes also demonstrate differences in the C-banding pattern. InM. oeconomus, the X chromosome exhibits a block of centromeric heterochromatin which is larger than that of the autosomes; this characteristic helps to recognize the X chromosomes in the karyotype. InM. arvalis no heterochromatin was appreciated in the sex chromosomes. The Y chromosomes ofM. ochrogaster andM. oeconomus are entirely heterochromatic. During male meiosis heterochromatin shows condensation, association and chiasma prevention; the sex chromosomes pair end to end in the three species. At pairing, the Y chromosome ofM. arvalis is despiralized, but it appears condensed again shortly before separation of the bivalent.     

Multiple captures provide evidence of small mammal social behavior

Social behavior of small mammals living under natural conditions often is inferred from live-trapping data, particularly from incidents in which two or more individuals are captured together in a trap. We examined whether multiple-capture data from a long-term study of prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) were consistent with well-known species differences in social behavior (whereas prairie voles are highly social and display monogamy, meadow voles are less social and promiscuous). When possible, we also examined multiple captures of two nontarget species, northern short-tailed shrews (Blarina brevicauda) and western harvest mice (Reithrodontomys megalotis). Percent of total captures that were multiple captures and percent of total adult captures that were male–female captures were highest for prairie voles and lowest for meadow voles; values for harvest mice and shrews were in between those of the vole species, but more similar to values for meadow voles. Repeat captures of the same male–female pair occurred most commonly in prairie voles, and multiple captures of this species typically involved individuals from the same social group. Multiple captures of adults and juveniles were more common in prairie voles than meadow voles, except for captures of at least one adult male and at least one juvenile, which did not differ between the two vole species. Multiple capture data for prairie voles and meadow voles were largely consistent with established species differences in social behavior, suggesting that such data can provide an accurate indication of social and mating systems of small mammals.     

Microsatellite markers for the common vole (<Emphasis Type="Italic">Microtus arvalis</Emphasis>) and their cross-species utility

Fragmentation of natural habitats of the common vole (Microtus arvalis) provides an excellent model system to study the consequences of restricted gene flow and small population sizes for isolated populations. Here we describe the isolation and characteristics of 10 autosomal and one X-linked microsatellite marker. These new markers were tested in 24 voles from a natural population in eastern Germany. Loci were highly polymorphic with numbers of alleles per locus ranging from three to 26 and expected heterozygosities from 0.51 to 0.97. All loci except for the X-linked locus Mar105 followed Hardy–Weinberg expectations. Cross-species amplifications revealed that most loci were polymorphic as well in M. agrestis, M. thomasi, and M. pennsylvanicus.     

Population growth and habitat distribution in cyclic small rodents: to expand or to change?

Habitat selection determined by intraspecific interactions (social behaviour), being either free or despotic, should result in the largest densities in the most favourable habitat at least in late increase and decline phases of cyclic populations. Habitat distribution determined by interspecific effects such as herbivore-plant or predator-prey interactions may result in higher densities in inferior habitats at late peaks and/or declines due to overgrazing of preferred habitats, or invasion of such habitats by specialist predators. An examination of the distributions of the rodent species Clethrionomys glareolus and Microtus agrestis during a population cycle on forest clearcuts at Grimsö, south-central Sweden, demonstrated clear changes towards less preferred habitats during the decline phase, particularly in M. agrestis. Intraspecific competition could be excluded as a cause since the numbers of both species declined simultaneously. There was no sign of overgrazing, while weasels, Mustela nivalis, invaded the preferred M. agrestis habitat during peak–decline. Predation thus appears more important for the local occurrence at early decline, rather than territoriality or other social behaviour. It is concluded that distributions in various habitats do not always reveal any primary habitat selection but, rather, habitat-dependent survival.     

The cost of habitat selection in prairie voles: an empirical assessment using isodar analysis

The ideal free distribution assumes that habitat selection is without cost and predicts that fitness should be equal in different habitats. If habitat selection has a cost, then individuals should only move to another habitat when potential fitness in the new habitat exceeds that in the source habitat by an amount greater than the cost of habitat selection. We used isodar techniques to assess the cost of habitat selection. In an experimental landscape, we monitored density, movement, and reproductive success of adult female prairie voles, Microtus ochrogaster, in adjacent paired habitats with low and high cover. We tested the following hypotheses: (1) adult female prairie voles exhibited density-dependent habitat selection; (2) the cost of habitat selection was density-independent. Habitat quality based on population density and fitness of adult females was higher in high cover habitats. Net movement was from low cover to high cover habitats. The results indicated that adult female prairie voles exhibited density-dependent habitat selection. Furthermore, there was a significant cost of habitat selection, and the cost was density-independent.     

Self-grooming and sibling recognition in meadow voles,Microtus pennsylvanicus,and prairie voles,M. ochrogaster

Self-grooming in response to the odours of an opposite-sex conspecific may reflect sexual motivation on the part of the actor. We tested the hypothesis that meadow voles, Microtus pennsylvanicus, and prairie voles,M. ochrogaster , both self-groom at different rates when exposed to the odours of their siblings as compared to those of nonsiblings. This prediction was studied under the context of social memory for siblings and the effects of isolation on memory for siblings. The hypothesis explains the self-grooming responses of meadow voles isolated from their siblings for 10 days and of prairie voles isolated from their siblings for 20 days. However, 20 days of isolation for male and female meadow voles, and 30 days of isolation for male prairie voles were sufficient to induce these animals to self-groom at a similar rate to both sibling and nonsibling odours, suggesting that after isolation these animals no longer recognized their opposite-sex siblings. Female prairie voles isolated for 30 days self-groomed more in response to the odours of male nonsiblings than to those of male siblings, suggesting that female prairie voles still recognize their male siblings after isolation. This study is the first to provide empirical evidence that, in the context of sibling recognition, self-grooming behaviour is directed at unfamiliar opposite-sex conspecifics, and that the communicative function of self-grooming (sexual motivation) is associated with social memory for siblings. Differences in the self-grooming behaviour of meadow voles and prairie voles may be associated with several aspects of their life history characteristics.     

Ecosystem dynamics through the past 2000 years as revealed by fossil mammals from Lamar cave in Yellowstone National Park,USA

Lamar Cave, a late Holocene paleontological site in Yellowstone National Park, USA, has yielded 36 fossil mammal species from 10 stratigraphic units representing about 2000 years. The fossil fauna is similar to the mammals in the park today and affords a unique opportunity to investigate paleocommunity and ecosystem dynamics through time.

Remains of an extralimital species in Yellowstone today, Microtus ochrogaster are found only in the oldest cave deposits, dated at 1695 ± 60 yr B.P. Disappearance of this species by about 1550 years ago marks evolution into the ecosystem that has persisted into the present and is recognizable by a fossil mammal assemblage that is virtually identical to the modern one. Relative abundance fluctuations in the mammal populations imply community resilience through the past 2000 years. Trends in relative abundances of small mammals, particularly the inverse relationship between Microtus and Spermophilus are interpreted as evidence of declining grass cover near Lamar Cave between approximately 1500 and 1000 years ago. The initiation of this environmental change may well have stimulated the ecosystem change marked by Microtus ochrogaster extirpation. Support for this hypothesis is found in a pollen record from a nearby lake.     

Small rodents in the shrub tundra of Yamal (Russia): Density dependence in habitat use?

Northern small rodents are well known for their population cycles which represent a key process for the functioning of arctic and boreal ecosystems. Habitat use often changes in the course of the cycle. Higher densities can either lead to spill-over into secondary habitats or to increased habitat specificity because of interspecific competition. Here we investigate whether voles in the shrub tundra of southern Yamal exhibit density dependent habitat use. Voles were trapped at the Erkuta Tundra Monitoring Site (N 68.2°, E 69.2°) in three characteristic habitats over five years covering all phases of the population cycle. Our analyses focused on the two most numerous species Microtus gregalis (52% of individuals caught) and M. middendorffii (36%). A small-scale spill-over effect was observed for M. gregalis, which increasingly used the open habitat adjacent to their preferred willow thickets at high abundance. At a larger scale no such effect was observed for the two Microtus species – a result which is explained by the overall moderate densities of voles and the large spatial extent of the primary habitat of M. middendorffii: moist moss dwarf shrub tundra.     

A new intermediate host for Echinococcus multilocularis: The southern red-backed vole (Myodes gapperi) in urban landscape in Calgary,Canada

Human Alveolar Echinococcosis (HAE) is a potentially fatal parasitic disease caused by Echinococcus multilocularis, a cestode characterized by a sylvatic life-cycle involving several species of rodents and lagomorphs as intermediate hosts and canids as definitive hosts. Despite the wide distribution of the parasite in North America, the number of competent intermediate host species identified to date is still relatively small, and mainly includes the northern vole (Microtus oeconomus), brown lemming (Lemmus sibiricus), northern red-backed vole (Myodes rutilus), deer mouse (Peromyscus maniculatus) and meadow vole (Microtus pennsylvanicus).By monitoring the infections in rodents in the city of Calgary (Alberta, Canada), we have detected a case of severe alveolar echinococcosis in a southern red-backed vole (Myodes gapperi), a species never reported before as an intermediate host for this parasite. Observation of protoscolices in the intra-abdominal multilocular cysts indicates that M. gapperi could act as a competent intermediate host for the transmission of E. multilocularis.Since M. gapperi can be found in close proximity to, and within metropolitan areas, this species could play a role in the establishment and maintenance of the sylvatic life-cycle of E. multilocularis in urban landscapes, where the potential for zoonotic transmission is higher. The new intermediate host reported needs to be taken into account in future surveys and transmission models for this parasite.     

The neurobiology of pair bond formation,bond disruption,and social buffering

Enduring social bonds play an essential role in human society. These bonds positively affect psychological, physiological, and behavioral functions. Here, we review the recent literature on the neurobiology, particularly the role of oxytocin and dopamine, of pair bond formation, bond disruption, and social buffering effects on stress responses, from studies utilizing the socially monogamous prairie vole (Microtus ochrogaster).