Lowell L Getz & C Sue Carter. American Scientist. Volume 84, Issue 1. January 1996.
If you part the vegetation and closely examine the surface of almost any grassy field in central North America, you may discover a network of small, tunnel-like runways. Bare soil serves as the floor of such a runway, because the grass gets trampled by countless tiny feet. The dead litter and grass surrounding a runway are chewed away, leaving smooth and rounded walls that allow unhindered movement by a runway’s occupant. If you follow a runway far enough, you will find three or four burrows, each about the centimeters in diameter, that lead underground. The burrows regroup at an underground nest constructed of tightly interwoven and finely shredded grass that fills a chamber, which is from 10 to 15 centimeters in diameter and lies a dozen or so centimeters below the surface. You might also discover a few surface nests of similar size and construction.
Prairie voles–small rodents that weigh between 35 and 45 grams as adults–build these elaborate runway systems and nests. The prairie voles represent one of the most abundant small mammals in the North American grasslands, from the midwestern United States to the Canadian prairie provinces. An adult prairie vole may live alone or in a group, composed either of relatives or genetic strangers. Regardless of the social groupings, prairie-vole populations experience high-amplitude fluctuations in numbers. A population’s density varies from lows of only one or two animals per hectare (about 2.5 acres)–often disappearing completely–to highs that surpass 600 voles per hectare. Some populations reach high densities every three to four years, but others vary erratically. These fluctuations in population density develop from a combination of a high reproductive rate and heavy mortality from predators.
In many cases, male and female prairie voles practice monogamy–living and mating with a single partner. Many recent articles have examined the hormonal and neurobiological bases for such behavior. By monitoring more than 850 free-living social groups, we found that the social and mating systems of prairie voles depend on other factors as well, including the quantity of available food and the population density. In this article, we shall describe the results of 25 years of laboratory and field studies on the social behavior and population dynamics of prairie voles in east-central Illinois.
In addition to building complex living quarters, prairie voles forge equally complicated living arrangements. Three different types of breeding units, or social groups, can be found in prairie-vole populations. A unit may be a male-female pair, a single female or a communal group.
A male-female pair consists of an adult male, an adult female and, perhaps, newborn young. Such adults display traits that are associated with behavioral monogamy. For example, a male and female share a nest and an associated home range, or territory. More over, the male of a pair expends considerable time and effort in constructing and maintaining a nest and in providing care to his young, including grooming and retrieval of pups that wander from the nest. Once paired, a male and a female tend to stay together. In fact, three-quarters of these pairings persist until one member dies.
If a male from such a pair dies, the female rarely acquires a new mate. Instead, she remains alone. Most single-female breeding units consist of a survivor from a male-female pair that was disrupted, usually by the death of a partner. A single-female breeding unit may include juveniles but not an adult male. If the female of a pair dies, the male typically leaves the nest to wander as an unsettled male.
A communal group of prairie voles usually forms from an extended family of a male-female pair or a single female. In such cases, offspring remain in their natal nest, even as adults, and such animals are called philopatric. In fact, most prairie voles can be described as philopatric, because 68 percent of the males and 73 percent of the females born to male-female pairs or single females remain at their natal nests through adulthood. As these offspring mature, they help care for younger offspring. When two or more philopatric offspring reach adulthood, unrelated males and females may join an extended family. Nevertheless, communal groups emerge largely from philopatric behavior, because 70 percent of the additions to an original breeding unit come from offspring that stay at home.
Not all adult voles, however, join a social group. At any given time in a population of voles, approximately 45 percent of the males and 24 percent of the females are not permanent residents of a nest. Most of the roaming males tend to stay that way, wandering through the population but making frequent visits to social groups. Socially unattached females, on the other hand, soon settle into a nest, either singly or as part of a male-female pair or a communal group. The percentage of wandering males in a population remains the same even when population density varies; so a high-density population contains more wandering males than does a low-density one.
The distribution of social groups in a population of voles varies seasonally. In an average population between March and mid-October in central Illinois, for instance, about 36 percent of the groups are male-female pairs, 37 percent are single females and 27 percent are small communal groups, made up of three individuals on average. In mid-October, communal living increases and remains high throughout the winter, when 69 percent of the social groups a communal, 24 percent are male-female pairs and seven percent are single females. From late October through February, an average communal group consists of eight voles, and groups made up of more than a dozen appear frequently. These two general seasons will be called spring-early autumn and late autumn-winter.
The stability of communal groups also varies with season. In spring-early autumn, communal groups stay together an average of 20 days; late autumn-winter groups stay together an average of 87 days. So stability increases in late autumn-winter communal groups. The stability of a communal group depends largely on individual vole behavior. In spring-early autumn, 21 percent of the members of communal groups move from one group to another. During late autumn-winter, on the other hand, only four percent of communal-group members switch groups. In fact, communal groups stick together so tightly during late autumn-winter that they have been observed to move more than 20 meters as a unit to a new nest location–something that has never been observed in a communal group during spring-early autumn.
As winter progresses, however, mortality decreases the size of communal groups. By spring, survivors from various communal groups form male-female pairs. Nearly two-thirds of those pairs will be composed of individuals from different late autumn-winter communal groups. Moreover, fewer than two percent of the pairs consist of related voles. Although prairie voles tend to live throughout most of a year in communal groups comprised primarily of family members, each spring brings a thorough mixing of a breeding population.
Why do prairie voles form communal groups? Other mammals nest communally for various reasons, including enhanced exploitation of a resource, such as food, protection against predators or to conserve energy during cold periods. None of these explanations, however, applies to prairie voles.
Prairie voles do not gain food, safety or warmth from group living. No apparent result of group living should increase an individual vole’s efficiency at feeding on green vegetation. In terms of predation, even a large number of voles could not fight off most of their enemies, especially the large ones, including badgers, domestic cats, coyotes, foxes, hawks, mink, owls, raccoons, skunks, snakes and weasels. Group warming also fails to explain communal living in prairie voles. First, communal groups, albeit small ones, make up one-fourth of the social groups during summer. Second, prairie voles begin forming larger communal groups in mid-October, even though low temperatures do not become significant for another month. Third, nearly half of the winter social groups consist of fewer than three voles–essentially the same number as in summer. Fourth, when natural causes during winter reduce a large communal group to three or fewer voles, nearly half of the survivors never leave the nest. Moreover, voles that do leave nests tend to join smaller groups.
Although many species of rodents form communal groups only during nonreproductive periods, the same cannot be said of prairie voles. In fact, two or more concurrent litters exist in many prairie vole-communal groups. Moreover, all spring-early autumn-communal groups include at least one reproductive adult. In addition, 73 percent of these groups include reproductive, unrelated males, and 86 percent include unrelated, adult females. Unrelated, reproductive adults can also be found regularly in winter communal groups.
Perhaps the cause of communal-group forming can be found by asking: Why are communal groups most prevalent during late autumn-winter? Although the groups arise from young voles remaining in their natal nest, philopatric behavior does not vary seasonally. Seasonal variation in nestling mortality provides a more obvious reason for the prevalence of communal groups during late autumn-winter. During spring-early autumn, an average of only 0.3 offspring per litter survive 30 days, which leaves too few offspring to form extended families, thereby making communal groups rare. By mid-October, however, an average of 1.3 offspring per litter survive 30 days–an increase of more than four times–which leads to most breeding units becoming communal groups.
From spring through early autumn, the most probable cause of increased nestling mortality in central Illinois is believed to be snakes, which are active during that time and do prey on prairie voles, especially nestlings. When snakes were excluded from part of our study site, communal groups of voles formed in August and September, and those groups were similar in size and composition to those normally observed only in late autumn and winter. When snakes are active, it appears that most social groups remain as male-female pairs or single females, and the few communal groups that do form are small. After snakes hibernate in mid-October, nestling survival increases and large communal groups predominate. So communal groups form in the absence of nest predation.
The social organization of a population of prairie voles describes the grouping of individuals in space and time, but it does not reveal which individuals reproduce. Understanding the selective advantage of communal nesting in prairie voles depends on knowing the mating system within social groups. The secrecy of voles, however, prevents observations of their mating under natural conditions, so much of the information about prairie-vole mating comes from laboratory observations. A combination of laboratory studies and field work provides a general understanding of mating in prairie voles.
A chemical signal, or pheromone, in a male prairie vole’s urine stimulates the first period of estrus, or heat, in a virgin female. This pheromone does not travel through the air, so it’s transmission depends on a female sniffing a male’s genital area. A female usually acquires this pheromone from an unfamiliar male, because she does not sniff the genitals of familiar males. Within 48 hours of sniffing this substance, and if a female stays in the presence of a male (not necessarily the one she sniffed), she achieves estrus and mates. Her pregnancy lasts about 21 days. Within a day of giving birth, the female enters postpartum estrus and will usually mate immediately if a reproductive male (usually her mate) is nearby.
If a female practices philopatry–living with her extended family-reproductive activation becomes more complicated. Reproductively active females in a group produce another urine-based pheromone that suppresses the reproductive activation of young females. So a single bout of male-genital sniffing will not activate a virgin female. Instead, she requires multiple exposures, about a dozen, to the male-urine pheromone over three or four days to achieve estrus.
For the most part, philopatric females do not mate with family members or even familiar males. Laboratory studies indicate that a reproductive, philopatric female will not mate with her brothers or her father if unfamiliar males are present. Without the presence of an unfamiliar male, on the other hand, these females occasionally mate with familiar males, including family members. The presence of a female’s mother, however, inhibits a daughter from mating with her father. In any case, matings between philopatric females and their brothers or father rarely lead to pregnancy. As already mentioned, such a female usually becomes reproductive only through frequent visits from unfamiliar males, with which she could mate in the wild.
In addition, philopatric males do not become reproductive in family groups unless they interact with unfamiliar animals, males or females. Moreover, males reared with family members display less than average reproductive behavior when they encounter reproductive females. These behaviors should also reduce matings between related animals in a social group.
Given the social structure of a prairie-vole population, opportunities for mating with various partners might exist. Frequent group living, for instance, could provide several potential mating partners for any individual. Moreover, an unfamiliar partner could come from the wandering voles, which include nearly half of the males and one-quarter of the females in a population. The likelihood of a vole mating with more than one partner, however, depends on its type of social group.
In male-female pairs, several factors support monogamy. In such a pair, the male rejects overtures from unfamiliar, virgin females by not allowing them to sniff his genital area. In addition, a male excludes unfamiliar males from the vicinity of his nest, as well as from the periphery of his home range. This mate-guarding behavior works best, as expected, during low-population periods. During high-population periods, unfamiliar males may enter the home range of a male-female pair, which produces an opportunity for the female to mate with another male.
Laboratory observations indicate that a paired, estrous female might mate with unfamiliar males. Nevertheless, DNA fingerprinting of embryos from females of free-living, male-female pairs revealed that the females had mated exclusively with their partners, even at a high population density. It appears that males of such pairs also remain loyal to their mates, because they are rarely found visiting nearby nests.
Single females, on the other hand, receive numerous visits from males, suggesting that litters may be fathered by more than one male. Field evidence reveals that single females could potentially mate with wandering males or neighboring paired males. Nonetheless, wandering males make up more than 90 percent of the male visitors at single-female nests, regardless of the population density. So single females probably mate with wandering males most of the time.
In communal groups, resident males defend the outskirts of their home range against unfamiliar males. At low population densities, unfamiliar males can be excluded, and only 17 percent of the philopatric females become reproductive in a communal group, probably because they are not exposed to unfamiliar males. At high population densities, on the other hand, resident males may fail to exclude all of the wandering males, and 77 percent of the philopatric females become reproductive. Such intending males may also mate with these females. In fact, we have evidence for multiple paternity in some litters from females that lived in communal groups in high-density populations. The resident males were not mating with multiple partners, so the wandering males must have been mating with a groups’ females.
The largely restricted mating interactions in a population of prairie voles bring up a fundamental question: How do prairie voles maintain genetic variability? Populations that undergo periods of low density–so-called population bottlenecks–may experience reduced genetic variability simply because of a reduced number of individuals. Likewise, populations that form genetically distinct subunits, called demes, risk even higher losses of variability during a population bottleneck. If a population crashes and an entire deme dies out, unique genes may be lost.
At first, we predicted that prairie voles would be susceptible to a loss of genetic variability. Their social organization includes communal groups formed largely from family members, and every two to five years this species experiences extreme population bottlenecks of 5 to 15 generations. Although this combination could favor reduced genetic variability, prairie voles apparently avoid that problem. First, hormonal and behavioral mechanisms reduce the probability of mating between related voles. Second, a breeding population of voles gets mixed completely at the beginning of each annual breeding period. Finally, voles that do disperse from their natal nest travel far enough away that they are not likely to mate with a family member. So most voles mate with unrelated partners, which facilitates gene flow and genetic variability in a population, even during bottlenecks.
The preceding information suggests an evolutionary answer to an earlier question: Why do prairie voles form communal groups? This animal evolved in tallgrass prairies, which are very low in food. Although these habitats include forbs–broad-leaved herbs with succulent stems and leaves–that are the essential food for prairie voles, these plants provide food only during spring, and even then they are scattered. By early summer, the growth of tall surrounding grasses shades a forb’s base, causing the lower leaves to wither and die. At the same time, a forb’s stem turns dry. During the winter, little green vegetation of any sort exists in a tallgrass prairie. This low level of food leads to low population densities and widely dispersed females.
We believe that the social organization and mating system of prairie voles might have evolved as an adaptation to low-food habitats. If a low-food habitat induces a low population density among voles and widely dispersed females, then a male might do better by forming a pair with a female. That pair-forming behavior would assure a male of a suitable mate and prevent him from continually expending energy on searching for other females. Once a male selects a mate, he might increase his fitness by guarding her from other males and by providing care for his offspring. Then all of the young produced by the female would be his and more would survive, because of receiving additional parental care.
In a low-food habitat, any voles leaving their natal nest would face little chance of finding a mate and locating a home range that would provide enough food for successful reproduction. So offspring would do better by staying home. In addition, reproductive activation of philopatric offspring would be selected against, because the habitat would not offer enough food for a mother and her daughters to raise litters on the same home range. Few of the offspring that did leave their natal nest would survive, because of limited food. That would lead to very few wandering males. So a male of a male-female pair could adequately guard his mate and prevent reproductive activation of his daughters. The offspring that remained at their natal nest could increase their own reproductive success, or fitness, by caring for younger siblings, which share common genes with their extended family. That helping, instead of reproducing, would further limit the size of a prairie-vole population.
Although the social organization of prairie voles apparently evolved in response to limited food, several field studies reveal that the present social organization does not vary with food availability. Perhaps the basic behaviors associated with communal nesting in a low-food habitat–behavioral monogamy and philopatry–remain stable even in high-food habitats. Nevertheless, some behaviors, such as mate guarding and reproductive suppression of philopatric females, may not maintain the original mating system in high-food habitats. In fact, we predict that ample amounts of food lead to increased survival for voles that leave their natal nest. That would induce more breeding groups, more wandering males and, in turn, more potential visitors to social groups than in low-food situations. At some point, a male of a male-female pair could not fend off all of the wandering males, and most of the philopatric females would become reproductive. With a high level of food, however, those females could raise successful litters in their natal nest. Nevertheless, such a disruption of the normal mating system would lead to higher population densities, especially in late autumn, when more nestlings survive. Overall, this change in prairie-vole mating would lead to large-amplitude swings in population in high-food habitats. Therefore, we conclude that there is a clear relationship between the social organization and mating system of prairie voles and the variations in population demography that are observed in different habitats. These conclusions should be tested by comparing the social organization and mating system in high- and low-food habitats across a range of population densities.