Natal dispersal and philopatry in prairie voles (Microtus ochrogaster ...

Ethology Ecology & Evolution 6: 267-284, 1994

Natal dispersal and philopatry in prairie voles (Microtus ochrogaster): settlement, survival, and potential reproductive success

L.L. GETZ, B. MCGUIRE 1, J.E. HOFMANN 2, T. PIZZUTO

3

and B. FRASE

4

Department of Ecology, Ethology, and Evolution, University of Illinois, 515 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801-3799, U.S.A.

Received 14 March 1992, accepted 22 July 1993

We analyzed the costs and benefits of natal dispersal and philopatry in a free-living population of the prairie vole, Microtus ochrogaster, in which 70% of the males and 75% of the females were philopatric. Rather than settling into a nest, 40% of male dispersers continued to wander throughout the study area, while only 13% of female dispersers did so. Whereas males were more likely to wander in spring-early autumn during low density periods, females were more likely to wander during spring-early autumn, irrespective of population density. Of those animals that settled into a nest, females were more likely than males to settle as single individuals. Same-sex siblings that dispersed commonly joined the same social group. Although often settling within 5 m of each other, opposite-sex siblings that dispersed never joined the same social group or formed a male-female pair. Total length of life was longer for males and females that dispersed than for those that remained at the natal nest. Animals survived longer after dispersal if they settled > 30 m from the natal nest than if they settled < 30 m from the natal nest. Length of survival following dispersal was not correlated with age at time of dispersal. Fitness of female dispersers was 2.5 times that of philopatric females, estimated by comparison of the percent becoming reproductive, survival time after becoming reproductive, and the estimated number of female offspring per litter that survive to adult age. The success of dispersers may be related to the high food resource habitat in which the study was conducted. KEY WORDS:

natal dispersal, philopatry, voles, survival, settlement, reproductive potential.

1 Present address: Department of Psychology, University of Massachusetts, Amherst, MA 01003, U.S.A. 2 Present address: Illinois Natural History Survey, Champaign, IL 61820, U.S.A. 3 Present address: Department of Entomology, Clemson University, Clemson, SC 29634, U.S.A. 4 Present address: Department of Biology, Bradley University, Peoria, IL 61625, U.S.A.

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L.L. Getz et alii Introduction . . . . . . . . . Methods . . . . . . . . . . Results . . . . . . . . . . Fate of dispersers and philopatric young Settlement . . . . . . . . Survival . . . . . . . . . Reproductive potential of philopatric females Discussion . . . . . . . . . Acknowledgments . . . . . . . References . . . . . . . . .

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268 268 272 272 272 275 277 278 283 283

INTRODUCTION

The costs and benefits of philopatry and dispersal may be categorized as either genetic or somatic (SHIELDS 1987). Genetic aspects include two opposing forces, reduction of inbreeding effects and conservation of successful parental genomes. Somatic considerations, on the other hand, involve survival, successful acquisition of essential resources, and reproductive success. Although consideration of both genetic and somatic costs and benefits is necessary for a complete understanding of the selective advantages of natal dispersal and philopatry (SHIELDS 1987), our focus in this paper is on somatic aspects only. Potential somatic benefits associated with philopatry include increased survivorship and fecundity as a result of the reduced risk and energy expenditure associated with familiarity with the local physical and social environment (SHIELDS 1982). In some cases, philopatric young may benefit through the acquisition of parental resources (e.g., JONES 1986). Such advantages, however, may be balanced by costs associated with competition with relatives for food, nest sites, or mates (e.g., CLUTTON-BROCK et al. 1982). Individuals that disperse, while potentially facing high energy costs and predation as a result of increased movement and lack of familiarity with the area (e.g., AMBROSE 1972, METZGAR 1967), may benefit through increased access to resources by avoiding locally crowded conditions at the natal nest. In the present study we assessed the somatic costs and benefits associated with natal dispersal and philopatry in the prairie vole (Microtus ochrogaster), a species in which individuals live in communal groups comprised largely of family members plus a few apparently unrelated animals (GETZ et al. 1990, 1993). In an earlier paper (MCGUIRE et al. 1993), we detailed patterns of natal dispersal and philopatry in our study population. The majority of prairie voles remained at their natal nest until death; only 30% of males and 25% of females dispersed from their place of birth. Males and females that dispersed moved similar distances and left home at approximately the same age. Dispersal in prairie voles is consistent with the view that some young animals leave the natal nest in search of mates as a result of the typical failure of familiar individuals to breed with one another.

METHODS Study sites and field procedures These data were collected during a 7 year live-trapping study of the social organization of prairie voles living in two adjacent 1 ha (75 × 135 m and 100 × 100 m) alfalfa fields at the

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University of Illinois Biological Research Area near Urbana, Illinois. The first field was trapped from October, 1980 through July, 1984, and the second from June, 1983 through May, 1987. The study site and trapping protocols have been described in detail elsewhere (GETZ et al. 1990, 1993); we provide only brief descriptions here. We assessed philopatry and patterns of dispersal and settlement within the population by live-trapping (1) at 10 m grid intervals twice a month (GETZ et al. 1987), (2) directly at the nests of social groups twice a week (e.g., GETZ et al. 1993), and (3) at the outskirts of home ranges of selected social groups 3 times a month (from March, 1986 through April, 1987 only; MCGUIRE et al. 1990). For all three trapping protocols we used multiple capture livetraps baited with cracked corn. At each capture we recorded location, animal number (from toe clip), weight (at first capture and periodically afterwards), and reproductive condition (reproductive males had scrotal testes; reproductive females had a perforate vagina, or were pregnant or lactating). Each month, the entire grid was trapped for 3 days, and 2 weeks later, selected grid traps (those > 15 m from nests of known social groups) were set for another 3 day period. In both cases, we set grid traps on Tuesday afternoon and checked them daily through Friday afternoon at 21:30, 08:00, and 15:00 hr. We trapped directly at the nests of social groups (4-5 traps placed at the openings to burrows leading to the underground nests or in runways within a radius of 0.25 m of surface nests) for two 28-hr periods each week. We set nest traps at 06:30 on Monday and checked them at 2-4 hr intervals until midnight. On Tuesday morning, traps were checked twice, opened, and left in place. The same schedule was repeated Thursday through Friday morning of each week, except for the week when the entire grid was trapped. During the week of grid trapping, nest traps were set only Monday through Tuesday. In order to monitor animals at the outskirts of home ranges of social groups, we encircled (at about 5 m) the nests of selected groups with from five to eight traps. These traps were set on Tuesday, after the nest traps were unset, and checked at 15:00 and 21:00 hr, and then on Wednesday, at 07:00, 15:00, and 21:00 hr. Trapping at the periphery of home ranges was conducted for 3 weeks each month; traps were not set during the week in which the entire grid was trapped.

Types of social groups Patterns of association (not genetic analyses) were used to classify animals as related or unrelated. When an animal was captured primarily at one nest for at least 10 days, we considered that animal to be a resident. Animals < 20 g when first captured at a nest were considered to be offspring of a resident female at the nest. Our method of assigning maternity seemed reasonable given that animals < 20 g were never captured at adjacent nests, even when nests of adjacent groups were < 5 m apart. During the period of highest population density (624/ha) there were 74 social groups in the study area; the mean distance between nests at this time was 8.6 + 0.1 m, range 3-20 m, variance 2.8 m. Further, animals < 20 g rarely visited the outskirts of the home range of adjacent social groups (MCGUIRE et al. 1990). Home ranges of social groups, as determined by radiotracking (GETZ & HOFMANN 1986), encompassed an area of approximately 10 × 15 m. Only adults were observed to make forays into the home ranges of adjacent social groups. If a single adult male was living at the nest at the time of conception, we considered him to be the father of the offspring. Preliminary results from DNA fingerprinting suggest that this assumption is generally accurate. Analysis of embryos from three male-female pairs indicated only one instance of extrapair copulation among the 12 embryos in the three females. We assumed that wandering adults and animals from different social groups were unrelated if they had never been captured as young animals with any of the residents of the focal group. Most prairie voles at our study sites lived in three types of social units; male-female pairs, single female units, and communal groups (GETZ et al. 1990). Whereas pairs consisted

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of one adult male and one adult female, single female units were comprised of an adult female and no resident adult male. Pairs and single females often had young at their nests; if young remained at the natal nest until 30 days of age (the age at which prairie voles can become reproductive and thus considered to be adult), the group was classified as communal. Communal groups included two or more adults of the same sex. Most (78.7%) formed as extended families by the addition of philopatric offspring to male-female pairs or single female breeding units. In addition to members of an extended family, most communal groups also contained one or two apparently unrelated adults (animals previously recorded as wanderers or residents of another social group) that began nesting with the family once at least two resident offspring reached adult age. The remaining 22.3% of the communal groups formed by the joining together of two or more unrelated adults at a nest. In addition to pairs, single females, and communal groups, a number of single males were identified as residents in the population. Although some lived alone at a nest, others lived with their juvenile offspring following loss of the adult female (again, if these offspring lived to 30 days of age, the group was then classified as communal). Most unpaired males did not qualify as residents because, rather than settling into a nest, they wandered throughout the study areas; approximately 45% of the total adult males in the population were wanderers (GETZ et al. 1993).

Determination of philopatry and dispersal Animals were classified as philopatric if they remained at their natal nest until death. Individuals that permanently left the natal nest, even though remaining within the study site, were classified as natal dispersers. When calculating the proportion of philopatric animals, we considered only those individuals that lived at least 30 days; animals that died before 30 days may not have had sufficient opportunity to disperse, given that weaning in prairie voles does not occur until approximately 20 days of age (MCGUIRE & NOVAK 1984). Animals were considered to have dispersed from their natal site if they (1) were captured at least 20 m (two home range radii) from the natal nest and not again at the nest or anywhere else, (2) formed a pair or joined another established social group, or (3) left the natal nest, and rather than settling into a nest, wandered throughout the study areas until they died or emigrated from the study site. We arbitrarily designated capture of an animal twice the distance from the nest to the furthest boundary point of the longest axis of an average group home range (GETZ & HOFMANN 1986) as an indication that an individual had actually dispersed from the natal nest. If such animals did not return to the natal nest and were not captured again, we assumed they had dispersed and either succumbed before being captured again, or had emigrated from the study site. Approximately 49% (n = 165) of the animals that formed or joined another social group, did so within 20 m of their natal nest; thus, given a home range radius of 10 m, the home range boundaries of the new and original social groups may be contiguous. However, even when group nests were < 20 m apart, residents of one group rarely visited the nest of the adjacent group (GETZ & HOFMANN 1986). Such social groups represented distinct entities and those animals taking up residence in a new group were no longer considered to be associated with their natal social unit. We examined our assumption that mortality for those animals that disappeared from the nest and were not captured elsewhere actually occurred while such animals were still residents of the nest and not during or after they had dispersed by comparing known dispersal (1) immediately before and after a grid trapping session was conducted, (2) during periods when trapping was and was not conducted at the periphery of the home range of a large number of social groups, and (3) when very few nests were trapped, as compared to when a large number of nests were trapped (GETZ et al. 1992a). Before and after grid trapping. One week each month the study areas were trapped at a 10-m grid interval the Tuesday-Friday, immediately following a Monday-Tuesday nest monitoring session. If animals that disappeared from the nest had actually dispersed rather than died at the nest, one would anticipate catching more animals elsewhere after they had disap-


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peared from the nest the Monday-Tuesday prior to a Tuesday-Friday grid-trapping (because grid traps were evenly distributed throughout the area to intercept dispersing animals) than when a Monday-Tuesday nest monitoring session was followed by a Thursday-Friday nest monitoring. Thus, if apparent nest mortality resulted from an inability to intercept dispersing animals before they succumbed to mortality outside the natal home range, we would expect to record more natal dispersal during Monday-Tuesday of the week of the grid trapping than during other weeks. Dispersal of young that were last captured at their natal nest Monday-Tuesday prior to the Tuesday-Friday grid trapping was therefore compared with that of animals last caught the following Monday-Tuesday trapping, which was followed by Thursday-Friday trapping at the nests. There was no significant difference between dispersal values for these 2 weeks of each month (week prior to grid trapping, 29.9%, n = 137; week prior to nest trapping, 27.6%, n = 116; χ2 = 0.073, df = 1, P = 0.787). Peripheral trapping. If residents repulsed unfamiliar dispersing animals from the traps at the nest, we would expect higher known dispersal when traps were set at the periphery of the home range than when such traps were not set. Of a total of 95 young that disappeared from natal nests, only 5 (5.3%) were subsequently captured in peripheral traps, well below the 27.8% recorded as natal dispersers from the main data set. Small vs large number of nests being trapped. If we underestimated natal dispersal, then we would expect to have captured more dispersing animals when population density was high and a large number of closely spaced nests were trapped than when population density was low and fewer, more widely dispersed nests were trapped. During the summer most social groups formed one or more surface nests within their home ranges. Although surface nests normally did not constitute the main nest of the social group, all nests were trapped until the group disappeared. At low densities it was easier to determine the actual nest of a social group; few secondary surface nests were trapped at these times. Further, we continued to trap a given nest for 2 weeks after the residents seemed to have disappeared from the nest. Thus, at high densities not only was the distance between nests small, but a large number (frequently at least 50%) of those nests being trapped at any given time were not inhabited. At low densities very few uninhabited nests were trapped. Comparisons of known dispersal when a large number of nests (> 100) were trapped and when a few nests (< 25) were trapped should indicate greater dispersal during the former periods, if our protocol underestimated natal dispersal. Although not statistically significant, known dispersal was actually slightly higher (33.3%; n = 39) when few nests were trapped than when large numbers of nests were trapped (20.6%; n = 92; χ2 = 1.75, df = 1, P > 0.15). Microtus habitat adjacent to the two study sites was live-trapped monthly as part of an ongoing study of the demography of prairie vole and meadow vole (M. pennsylvanicus) populations (GETZ et al. 1987). Only 5.0% of all young born in the two study areas and known to have survived to at least trappable age (about 12 days) were captured in the surrounding fields, and 1.7% had been recorded as dispersers before they moved to the other fields. We obviously did not intercept all long-range dispersers (only those moving through the adjacent site while we were trapping or those that had settled there); however, these data suggest relatively few individuals dispersed outside the study areas. VERNER & GETZ (1985) reported that only 16.7% of the total population, all age classes combined, of prairie voles inhabiting a bluegrass habitat eventually dispersed from the study site.

Data analysis We analyzed seasonal effects by dividing the year into late autumn-winter (16 October15 March) and spring-early autumn (16 March-15 October). When the data were analyzed on the basis of population density, we considered low and high population densities to be < 100/ha and ≥ 100/ha, respectively. We used log linear analyses to evaluate relationships between patterns of settlement of dispersers and factors such as sex, reproductive condition, type of natal social group, season,

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and population density. Log linear analyses were also used to examine the proportion of autumn-born young that survived to the following spring in relation to sex and whether or not individuals dispersed. When significant associations were detected, we compared proportions using confidence intervals. A χ2 test of association was used to examine the relationship between dispersal and reproductive activation in females. Data pertaining to total length of life, number of days survived after dispersal, number of days survived after attainment of reproductive status, and distance dispersed were analyzed with ANOVA. When variances were unequal among groups, we weighted each case by the inverse of its variance. Welch’s t-tests were used for posthoc comparisons.

RESULTS

Fate of dispersers and philopatric young Settlement. The relationship between season, population density and whether an animal settled into a nest or wandered following dispersal differed for males and females (Table 1; χ2 = 4.91, df = 1, P < 0.05). A larger proportion of males wandered during low density periods in spring-early autumn than at other times and densities. In contrast, more females wandered during both low and high density periods in spring-early autumn than during high density periods in late autumnwinter. The proportion of females wandering during high density periods in springearly autumn was also greater than the proportion wandering during low density periods in late autumn-winter. Overall, 40% (46/115) of male dispersers and 13% (13/100) of female dispersers wandered rather than settled after leaving their natal nests. We examined type of natal group, reproductive condition at time of dispersal, and age at time of dispersal, in order to determine whether animals that settled into a nest after dispersal differed in some way from those that wandered following departure from the natal nest. Whether an animal settled or wandered was not associated with type of natal group (Table 2; χ2 = 1.95, df = 2, P > 0.35). Animals that settled or wandered after dispersal also did not differ with respect to reproduc-

Table 1. Proportion of natal dispersers (n = 215) of Microtus ochrogaster that either settled into a new nest or wandered following departure from the natal nest. Data are grouped by sex, season, and population density; n in parentheses. Sex

Season

Population density

Fate Settle

Male

Late autumn-winter Spring-early autumn

Female

Late autumn-winter Spring-early autumn

Low High Low High Low High Low High

76.5 63.8 30.8 78.6 89.5 94.4 81.5 77.8

(13) (37) (8) (11) (17) (34) (22) (14)

Wander 23.5 36.2 69.2 21.4 10.5 5.6 18.5 22.2

(4) (21) (18) (3) (2) (2) (5) (4)


273 Table 2.

Proportion of natal dispersers (n = 102) of Microtus ochrogaster that either settled into a nest or wandered after dispersal as a function of type of natal social group; n in parentheses. Fate

Natal social group Male-female pair

Settle Wander

Communal group

77.4 (24) 22.6 (7)

68.5 (37) 31.5 (17)

Single female 64.7 (11) 35.3 (6)

tive condition at the time of dispersal; whereas 58.3% (n = 72) of those that settled were reproductive when they left the natal nest, 53.3% (n = 30) of those that wandered were reproductive when they left home (χ2 = 0.09, df = 1, P > 0.75). Finally, age at time of dispersal did not differ significantly between animals that settled into a nest (50.1 ± 3.3 days, n = 71) and those that wandered (38.9 ± 3.3 days, n = 30; F = 1.59, df = 1, 97, P > 0.20). Animals that settled into a nest after dispersing either formed a male-female pair, joined a communal group, or settled as a single individual. We examined whether type of social group joined or formed was associated with sex of disperser, population density, or season. Log linear analysis revealed no significant third or fourth order interactions. However, two significant second order effects were found. First, males and females differed in their pattern of settlement following dispersal in that more females than males settled as single individuals (Table 3; χ2 = 8.29, df = 2, P < 0.05). Second, pattern of settlement after dispersal was associated with season (Table 3; χ2 = 14.96, df = 2, P < 0.001). Specifically, more animals joined communal groups and fewer settled as single individuals in late autumn-winter than in spring-early autumn. The association between type of social group joined or formed and population density was not significant (Table 3; χ2 = 2.71, df = 2, P > 0.25). We examined whether distance dispersed varied as a function of sex, season, population density, or type of social group joined or formed. Few animals settled as single individuals, and thus we considered only those individuals that either formed Table 3. Proportion of natal dispersers (n = 156) of Microtus ochrogaster that either settled as single individuals, formed a monogamous pair, or joined a communal group. Data are grouped by sex, season, and population density; n in parentheses. Social group Factor

Male-female pair

Communal group

Single individual

Sex Male Female

37.7 (26) 29.9 (26)

58.0 (40) 48.3 (42)

4.3 (3) 21.8 (19)

Season Late autumn-winter Spring-early autumn

30.7 (31) 38.2 (21)

63.4 (64) 32.7 (18)

5.9 (6) 29.1 (16)

Population density Low High

40.0 (24) 29.2 (28)

40.0 (24) 60.4 (58)

20.0 (12) 10.4 (10)

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pairs or joined communal groups in the ANOVA. There were no significant second, third, or fourth order interactions; means (± SEM) for each group are given in Table 4. We did, however, detect main effects for population density and type of social group joined or formed. Individuals dispersed shorter distances at high population density (21.1 ± 2.4 m, n = 51) than at low population density (39.6 ± 3.1 m, n = 105; F = 11.69, df = 1, 122, P < 0.001). Dispersers that joined communal groups moved shorter distances (26.8 ± 2.8 m, n = 77) than did those that formed pairs (39.7 ± 3.9 m, n = 61; F = 4.25, df = 1, 122, P < 0.05). Likewise, more dispersers settled within 20 m (the average home range diameter) of the natal nest if they joined a communal group (59.1%, n = 88), than if they formed a pair (37.7%, n = 77) or settled as a single individual (34.8%, n = 23; χ2 = 9.22, df = 2, P < 0.01). During the 7 years of the study, only 74 (5.1%) of the young animals that survived to at least trappable age (12 days of age) were known to have eventually emigrated into study sites adjacent to the alfalfa fields. Owing to the small sample size and annual variation in monthly reproductive success, analysis of seasonal and density effects on emigration out of the study site was not feasible. However, 28 (37.8%) emigrated May-July, the period of lowest annual juvenile survival and population density (GETZ et al. 1990), and only 13 (17.6%) dispersed during SeptemberNovember, the period of highest juvenile survival and highest overall population density. These data suggest that long range natal dispersal, i.e., emigration, may be highest during late spring-early summer in our study population. When both male and female littermates dispersed from the natal nest, 72.2% (26 of 36 litters involving dispersal of at least two littermates) left within 3 days of each other. In 17 of the 36 pairs (47.2%), male and female littermates settled within 5 m of each other; none of the littermates, however, formed a breeding unit or joined the same communal group. Of 45 natal dispersers that formed a male-female pair, 35 (77.8%) did so with a wandering adult. Only 22.2% paired with another natal disperser; all such pairings were with natal dispersers from distant (> 2 home range diameters away from natal nest) and nonadjacent breeding units. In six of the 11 instances (54.5%) when two male littermates dispersed from the natal nest, the individuals left within 3 days of each other. In three of the 11 pairs (27.3%), the male littermates joined the same communal group; in the remaining eight pairs, the littermates settled at least Table 4. Distance dispersed (m) by Microtus ochrogaster as a function of sex, season, population density, and type of social group joined or formed. Values represent mean ± SEM; n in parentheses. Sex

Social group

Late autumn-winter Low

Male

Pair Communal Single*

Female Pair Communal Single*

Spring-early autumn

High

Low

High

41.8 ± 8.6 (5) 35.8 ± 6.2 (12) 44.0 ± 25.0 (2)

24.5 ± 9.5 (2) 22.9 ± 6.7 (10) 16.0 (1)

50.6 ± 8.7 (17) 37.8 ± 15.5 (8) 64.0 ± 40.0 (2)

28.5 ± 11.7 (4) 14.9 ± 4.9 (10) ——-

44.2 ± 19.2 (5) 24.2 ± 5.8 (9) 18.7 ± 7.5 (3)

34.3 ± 8.9 (6) 28.2 ± 9.5 (4) ——-

40.9 ± 8.4 (16) 33.1 ± 6.0 (17) 47.6 ± 13.7 (9)

18.0 ± 2.4 (6) 8.6 ± 2.0 (7) 30.0 (1)

*Excluded from ANOVA due to small sample sizes in several groups.


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5 m apart. In four of 14 cases (28.6%) in which two female littermates dispersed from the natal nest, the individuals left within 3 days of one another. Finally, in five of the 14 pairs of female littermates (35.7%), the littermates settled into the same communal group; in the remaining nine pairs, the littermates settled at least 5 m apart. We conducted a simple test to determine if such observations deviated from a random pattern. The azimuth of dispersal of a total of 110 hypothetical paired dispersers from a focal nest was determined by use of a random numbers table. The animals were presumed to have settled 38 m from the natal nest (the mean distance from the natal nest dispersers settled in our study). Only two of the 110 “pairs” of dispersers settled within 5 m of each other. Although we cannot apply statistical analysis to these comparisons, it appears that the observed proportion of paired natal dispersers, whether of the same or opposite sex, settling within 5 m of each other did so more frequently than by chance. Survival. We examined whether total length of life varied as a function of sex, season, population density, or whether an animal dispersed or remained at the natal nest. There were no significant second, third, or fourth order interactions; means (± SEM) for each group are shown in Table 5. We did, however, detect main effects for population density and for whether or not an animal dispersed. Individuals survived longer at high population density (74.1 ± 2.1 days, n = 507) than at low population density (59.5 ± 4.2 days, n = 177; F = 4.89, df = 1, 668, P < 0.05). Total length of life was longer for dispersers (108.9 ± 5.1 days, n = 159) than for philopatric young (58.6 ± 1.6 days, n = 525; F = 76.13, df = 1, 668, P < 0.0001). Animals survived longer after dispersal (i.e., after becoming settled into a nest) if they settled > 30 m from the natal nest (87.5 ± 8.8 days, n = 58) than if they settled < 30 m from the natal nest (66.8 ± 6.3 days, n = 93; F = 4.45, df = 1, 147, P < 0.05). There was no correlation between length of survival following dispersal and age at time of dispersal (R2 = 0.02, P > 0.10, n = 158). Most of the individuals that formed spring breeding pairs each year were born the previous autumn (GETZ et al. 1993). The association between dispersal and percent survival of autumn-born young (those born between 1 September and 30 November) differed between the sexes (χ2 = 11.29, df = 1, P < 0.001). Whereas more autumn-born males that dispersed from the natal nest survived until spring (at least 15 March; 29.2%, n = 65) than did those males that remained at home

Table 5. Total length of life (days) of Microtus ochrogaster as a function of sex, season, population density, and whether individuals dispersed or remained at the natal nest. Values represent mean ± SEM; n in parentheses. Sex

Status


Male

Dispersed Philopatric

Female Dispersed Philopatric

High

Spring-early autumn Low

High

89.2 ± 20.2 (9) 121.8 ± 12.8 (35) 54.4 ± 9.6 (20) 60.0 ± 2.2 (137)

110.7 ± 15.1 (27) 29.6 ± 1.8 (59)

92.7 ± 7.1 (26) 54.4 ± 3.2 (75)

90.0 ± 20.6 (4) 43.4 ± 4.7 (17)

120.9 ± 20.2 (13) 44.1 ± 8.4 (28)

118.0 ± 14.4 (25) 68.7 ± 4.7 (96)

98.6 ± 7.2 (20) 75.8 ± 4.6 (93)

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(2.1%, n = 141), survival of autumn-born females was not associated with whether or not they dispersed (dispersed, 27.3%, n = 33; philopatric, 18.0%, n = 122). For the measure “total length of life”, the interaction between sex and whether or not an autumn-born animal dispersed did not reach statistical significance (F = 2.86, df = 1, 362, P < 0.10). Overall, however, total length of life was longer for autumn-born animals if they dispersed (males, 111.1 ± 8.6 days, n = 61; females, 107.0 ± 9.5 days, n = 34) than if they remained at the natal nest (males, 62.6 ± 2.5 days, n = 143; females, 78.1 ± 4.2 days, n = 128; F = 44.97, df = 1, 362, P < 0.001). The average age of dispersal of autumn-born males and females was 52.9 ± 3.4 (n = 65) and 54.8 ± 4.5 days (n = 34), respectively. The relationship between age at reproductive activation and whether or not an individual dispersed differed for males and females (F = 7.44, df = 1, 192, P < 0.01). Among females, those that dispersed became reproductive at an earlier age (43.9 ± 2.9 days, n = 44) than did those that remained at the natal nest (61.5 ± 5.0 days, n = 59). In contrast, male dispersers and nondispersers attained reproductive status at about the same age (dispersers, 46.6 ± 4.4 days, n = 64; nondispersers, 39.0 ± 2.6 days, n = 29). These calculations include animals that became reproductively activated before dispersing and those that became reproductive after dispersing. Even though becoming activated at the natal nest, those reproductive offspring that eventually dispersed were considered to be natal dispersers. Indicators of reproductive activation of females included evidence of an open vulva (31.8%) and pregnancy (61.5%); only 6.7% were lactating when first observed to be reproductive. Of the 85 females first recorded as having open vulvas or pregnant at the natal nest, 67% dispersed before giving birth. The remainder had their first litter at the natal nest; their subsequent litters were born after they had dispersed. For those animals that became reproductive prior to leaving the natal nest, the interval between reproductive activation and dispersal was similar for males (17.6 ± 4.0 days, n = 45) and females (22.9 ± 4.7 days, n = 32; F = 0.74, df = 1, 75, P > 0.35). Survival after attainment of reproductive status was longer for dispersers (males, 70.6 ± 8.3 days, n = 60; females, 76.7 ± 9.6 days, n = 44) than for philopatric animals (males, 17.8 ± 2.4 days, n = 88; females, 42.6 ± 4.5 days, n = 73; F = 53.66, df = 1, 261, P < 0.0001). For philopatric animals, the relationship between reproductive condition and total length of life varied as a function of gender (F = 46.49, df = 1, 517, P < 0.0001). Philopatric females that became reproductive at the natal nest lived longer (102.3 ± 6.4 days, n = 73) than did philopatric females that remained nonreproductive (52.6 ± 2.5 days, n = 159). In contrast, total length of life of philopatric males that became reproductive at the natal nest (55.2 ± 3.0 days, n = 84) did not differ from that of philopatric males that remained nonreproductive (49.9 ± 1.8 days, n = 207). We examined whether survival of male dispersers (time from departure from natal nest to disappearance) varied with season, population density, or whether an individual settled into a nest after dispersal or continued to wander throughout the study site. Data pertaining to female dispersers was not included in the ANOVA due to small sample sizes in several groups. Means (± SEM) for both males and females are shown in Table 6. Survival of male dispersers varied as a function of season and population density (F = 5.04, df = 1, 86, P < 0.05). Specifically, whereas individuals in late autumn-winter survived for similar lengths of time during periods of low (57.3 ± 24.0 days, n = 9) and high population density (69.9 ± 12.2 days, n = 34), animals in spring-early autumn survived longer at low population density (76.9


277 Table 6.

Survival (days) after dispersal of Microtus ochrogaster as a function of sex, season, population density, and whether individuals settled into a nest or continued to wander throughout the study site. Values represent mean ± SEM; n in parentheses. Sex

Fate


High

Spring-early autumn Low

High

Male

Settle Wander

19.0 ± 4.2 (3) 76.5 ± 34.0 (6)

66.1 ± 13.6 (26) 82.2 ± 27.8 (8)

81.5 ± 17.5 (15) 69.1 ± 31.2 (9)

50.5 ± 8.6 (18) 19.8 ± 6.3 (9)

Female*

Settle Wander

31.5 ± 8.5 (2) 8.0 (1)

44.9 ± 6.8 (16) 14.2 ± 4.0 (4)

86.6 ± 19.3 (11) 101.5 ± 96.5 (2)**

75.8 ± 16.6 (17) 12.3 ± 9.3 (3)

* Excluded from ANOVA due to small sample sizes in several groups. ** One female survived 5 days after dispersal and the other 198 days.

± 15.7 days, n = 24) than at high population density (40.3 ± 6.6 days, n = 27). Although it was not always possible to tell exactly when a disperser joined or formed a social group, existing data indicate no significant difference in time from last capture at the natal nest to first capture after settlement into communal groups (8.6 ± 1.2 days, n = 36), male-female pairs (6.4 ± 1.5 days, n = 21), or as single individuals (3.5 ± 1.0 days, n = 4; F = 1.38, df = 2, 58, P < 0.27).

Reproductive potential of philopatric females and females that dispersed Owing to an inability to estimate reproductive success of males, we limited our comparison of reproductive success (fitness) of natal dispersers and philopatric animals to females. In this analysis, we considered only those females that were born before 15 October of each year; females born after mid October would reach adulthood during the nonbreeding period. A larger proportion of females that dispersed from the natal nest became reproductive (82.5%, n = 40) as compared to those that remained at home (42.3%, n = 111; χ2 = 17.457, df = 1, P < 0.0001). Without genetic analyses of maternity, we could not accurately assign young in communal groups to particular adult females in those groups. Specifically, we could not differentiate the young of a philopatric female from those of her mother or sisters, and we could not differentiate the young of a female that dispersed and joined a communal group from those of other adult females in that group. As a result of relying on patterns of association and not genetic analyses to assess kinship, a direct calculation of reproductive success of females as a function of whether or not they dispersed from the natal nest was not possible. Estimates were made, however, on the overall potential reproductive success of such females. Included in the calculations were comparisons of philopatric animals with dispersers in regard to: (1) proportion becoming reproductive, (2) longevity after becoming reproductive, and (3) the potential number of litters produced (prairie voles display postpartum estrus; thus we calculated potential number of litters by dividing the number of days survived after becoming reproductive by the gestation period of 22 days). We calculated directly from our data the proportion becoming reproductively activated and the length of time reproductive. Because we were unable to

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L.L. Getz et alii Table 7.

Potential fitness of philopatric and natal disperser female Microtus ochrogaster. See text for details. Components of fitness Percent reproductive Survival time after becoming reproductive (days)* Mean number of potential litters Potential total females/litter surviving to ≥ 30 days per female (0.32/litter) Mean number of potential total young

Dispersed

Philopatric

82.5 55.4 ± 8.9

42.3 42.6 ± 4.5

2.5 0.80

1.9 0.61

0.66

0.26

*Calculated from time of dispersal, if became reproductive before dispersing.

assign young animals to a specific female, the number of potential litters could only be estimated. In our study region, females once having achieved reproductive condition, remain reproductive until the end of the usual breeding period, normally early December; there is no midsummer decline in reproduction. In addition, breeding activity remains high throughout the winter every 3-4 years. We limited our calculations to animals born prior to 15 October to ensure a realistic estimate of the proportion of females becoming reproductively activated. However, since we are estimating potential fitness, the primary objective was to determine the proportion becoming reproductive and the average amount of time such females would have to produce litters, regardless of when they were born. For dispersers, we included only the amount of time they were reproductive after dispersal; 70.4% (n = 27) of the dispersers became reproductively activated at the natal nest. Of those females activated at the natal nest, approximately 36% may have had a litter before dispersing. This litter was not included in the fitness estimates, only those litters produced after dispersal were included since we were estimating fitness after dispersal. The mean number of female offspring surviving to adult age per litter produced (0.32 individuals; L.L. GETZ unpublished) was used to estimate the number of daughters contributed to the population by females that either dispersed or remained philopatric. A female had the potential to produce 2.5 times as many females that survive to adult age if she successfully dispersed as compared to if she remained at her natal nest (0.66 and 0.26, respectively; Table 7).

DISCUSSION

Pattern of settlement after dispersal differed between male and female prairie voles. It was more common for male dispersers (40%) than for female dispersers (13%) to wander throughout the study area instead of settling into a nest. Furthermore, males were more likely to wander during periods of low population density in spring-early autumn than at other times and densities. Females were also more likely to wander in spring-early autumn than in late autumn-winter, but level of density did not matter. Given the demands of lactation and the need for a stable nest site, an unsettled state would not be conducive to high reproductive rates (fit-


279

ness) among females. Wandering males, on the other hand, could retain a high degree of fitness by mating with females encountered during their visits to social groups. Although nonresident males visit all types of social groups in our population, visits to single female units are most common (GETZ & HOFMANN 1986, MCGUIRE et al. 1990). The general pattern that animals were more likely to wander during springearly autumn than during late autumn-winter may be related to the ease with which surface nests can be constructed and serve as adequate shelter during these months. Our finding that wandering by males was particularly common during low density periods in spring-early autumn may reflect the scarcity of social groups to join at such times and the tendency for males to wander rather than settle as single individuals. Of those dispersers that settled into a nest in late autumn-winter, few settled as single individuals and most joined a communal group. Although joining a communal group during periods of low temperatures could be related to reduction of energy expenditures, such behavior most likely represents a greater opportunity to join communal groups during this period. Communal groups are the most prevalent type of social group during late autumn-winter (GETZ et al. 1993). Dispersing animals at this time therefore had a higher probability of finding an established communal group to join than during spring-early autumn. During the spring-early autumn, there simply may not be communal groups which they can join, thus more continue to wander, form a pair, or settle as single animals. That neither formation nor maintenance of communal groups is a response to low temperature stresses (GETZ et al. 1993) supports the conclusions that the greater proportion of dispersers settling into a group, particularly to communal groups, is opportunistic rather than an adaptation for avoidance of low temperature stresses. Other than gender, we were unable to identify factors that differentiated animals that wandered after departure from the natal nest from those that settled into a nest. Animals that wandered did not differ from those that settled in terms of type of natal group, reproductive condition at time of dispersal, or age at time of dispersal. Whether or not an individual disperses, however, may be related more to factors in the early social environment that influence behavioral development than to factors present at the time of dispersal (e.g., within litters, individuals that display low levels of social interaction may be more likely than some of their more interactive littermates to disperse from the natal site; BEKOFF 1977). Individual differences in patterns of behavior following dispersal also may be shaped more by characteristics of the early social environment than by conditions at the time of departure from the natal nest. It was not uncommon for same-sex littermates that dispersed to join the same communal group; in approximately 27% of the instances involving male littermates and 36% of the cases involving female littermates, individuals settled in the same communal group. That related same-sex individuals settle together, or at least close to one another, following dispersal has been reported for other species of microtine rodents. In the common vole (Microtus arvalis), a species in which the majority of young females mature, mate, and then disperse from the natal nest, female littermates, as well as related females from consecutive litters, settle near each other in the same habitat patch (BOYCE & BOYCE 1988). LEUZE (1976) reported similar findings for related male water voles (Arvicola terrestris) that disperse. Such patterns of settlement may reflect benefits of being surrounded by relatives rather than nonrelatives (BOYCE & BOYCE 1988).

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In our study population, male and female littermates often left home at about the same time, and in almost half of these cases, settled within 5 m of each other. Despite settling close to one another, male and female littermates never formed a breeding pair, and unlike the situation for same-sex littermates, opposite-sex littermates never joined the same communal group. The vast majority of natal dispersers that formed male-female pairs, did so with a wandering adult. Only 22% paired with another natal disperser, and such pairings were always between individuals from distant or nonadjacent social groups. These field data are consistent with laboratory evidence demonstrating that familiarity between young male and female prairie voles is associated with absence of reproductive activity (GAVISH et al. 1984). Estrus in virgin females is induced by direct contact with a chemosignal in the urine of an unfamiliar male (CARTER et al. 1980). The estrus-inducing chemosignal is present in the urine of male family members, but because females rarely sniff the genital area of familiar males (e.g., MCGUIRE & GETZ 1991), they do not pick up the chemosignal and thus remain reproductively quiescent. The failure of young females to sniff the genital area of their father or brothers is thought to form the basis of a behavioral block to reproduction within family groups. Offspring retain the ability to recognize familiar animals for up to 15 days following separation (GAVISH et al. 1984). Natal dispersers that formed a pair did so an average of 6.4 days following departure from the natal nest, and thus dispersers would probably recognize siblings as familiar animals. The behavioral barrier to breeding among family members appears to extend beyond the time of reproductive activation. When females living in family groups were induced into estrus through interactions with unfamiliar males, they were observed to mate exclusively with nonresidents and to repel the small number of mating attempts made by male family members (MCGUIRE & GETZ 1991). In the present study, most dispersers (77.8%) that formed a male-female pair did so with a wandering adult. The remaining individuals (22.2%) paired with natal dispersers from distant and nonadjacent social groups. These data suggest that the association between familiarity and lack of reproductive activity may extend beyond the immediate family group and include individuals living in adjacent social groups. Typically, small mammals that disperse are assumed to experience high mortality. Reduced survival of dispersers relative to philopatric animals is thought to result from factors such as high predation rates due to increased movement and lack of familiarity with the area (AMBROSE 1972, METZGAR 1967) and difficulties associated with establishing residence in an existing population (e.g. JOULE & CAMERON 1975). In our study, however, total length of life was longer for males and females that dispersed than for males and females that remained at the natal nest. Although the success of dispersers might be explained by the fairly short time that most spent in the transient stage (on average, from 3.5 to 8.6 days elapsed between last capture at the natal nest and first capture after dispersal and settlement into a nest), our data on the survival of individuals that persistently wandered also fail to indicate increased mortality associated with transiency. Survival following dispersal from the natal nest did not differ for those males that continued to wander throughout the study site and those that settled into a new nest soon after leaving home (females were not included in the analysis due to small samples sizes). Thus, unsettled animals in our population did not appear especially susceptible to predation. Indeed, the lower survival of philopatric animals suggests that predators at our study site may have been particularly attracted to established nests occupied by large social groups.


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Most dispersers in our population settled close to their natal nest. Median dispersal distances for both males and females approximated the diameter of only one home range (MCGUIRE et al. 1993). Although moving through and settling in a familiar physical and social environment would seem to reduce risks associated with dispersal, animals that settled close to the natal nest experienced reduced survival relative to those that settled far from the natal nest. Although we lack information about the hunting strategies of predators on our population, individuals that live in closely spaced social groups may have been more susceptible to predation than individuals living in social groups that are more widely spaced. If predators key in on clumped social groups, then this may offset any survival benefits associated with familiarity with the local physical and social setting. Finally, there was no correlation between age of dispersal and subsequent survival following dispersal. Thus, possible experience gained by remaining at the natal nest did not increase survival after dispersal. JOHNSON & GAINES (1987) reported higher fitness for female prairie voles that dispersed than for either those that remained at their natal site or those prevented from dispersing. The dispersers in that study were placed in optimal habitats from which all residents had been removed. The greater fitness of dispersers involved increased survival and reproduction. The same authors obtained similar results in another study (JOHNSON & GAINES 1985). However, in both of these studies the dispersers were removed to a different habitat patch. Thus, their conclusions are not directly equivalent to those derived here. We estimated potential fitness of female prairie voles as a function of whether or not they dispersed from the natal nest. Our results suggest that females that disperse, but remain within the same habitat patch, have the potential to produce more than twice as many female offspring that survive to adult age as compared to females that remain at the natal nest. According to our estimate, the greater reproductive potential of females that disperse results largely from two factors. First, females that disperse are much more likely than are philopatric females to become reproductive (82.5% versus 42.3%, respectively). Second, survival following attainment of reproductive status was longer for females that dispersed than for females that remained at the natal nest, 55.4 and 42.6 days, respectively. Our estimate of reproductive success, however, is fairly crude. For example, we used the average value of 0.32 females per litter surviving to adulthood for both philopatric females and females that disperse. The value 0.32 represents mean survival of offspring of all reproductive females throughout the entire 7 years of the study. Possibly, the survival of young differs between females that remain at home and those that leave. We also assumed that philopatric females and females that dispersed produced litters every 22 days. In the laboratory, interlitter interval in prairie voles varies as a function of litter size and presence of an older litter at the natal nest (e.g., SOLOMON 1991), and thus time between litters could differ between the two groups of females. More accurate determination of the fitness of female prairie voles that disperse or remain at the natal nest requires genetic analyses of all members of social groups. Furthermore, given that prairie vole young may gain indirect fitness benefits from helping to rear younger siblings (SOLOMON 1991), a consideration of inclusive fitness, rather than simply individual fitness, may also be necessary. The results of the present study indicate that prairie voles that disperse survive longer, and at least in the case of females, probably produce more female offspring that survive to adult age, than do animals that remain at the natal nest.

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Despite the apparent success of the dispersal strategy, however, the majority of male and female prairie voles in our population (70% and 75%, respectively) remained at the natal nest until they died (MCGUIRE et al. 1993). If dispersal is successful, then why do most prairie voles remain at the natal nest? Our current hypothesis focuses on the fact that all of our information on dispersal has been collected from populations living in alfalfa fields, an extremely food rich habitat for prairie voles (COLE & BATZLI 1979). Animals that leave the natal nest are not faced with the problem of finding a new nest site with a suitable food supply. The prairie vole evolved in low food tallgrass prairie habitat, in which survival of dispersers may be very low owing to scarcity of food. Dispersers may have to traverse extensive areas to locate suitable sites in which to settle. Under such conditions, we propose there may have been selection for remaining at the natal nest. We further predict that philopatry is retained in populations that occupy habitats with high food availability. In such habitats, owing to high food, reproductive success may be greater for those few females that do disperse than for philopatric females. GETZ et al. (1992b) reported similar proportions of natal dispersal and philopatry and a communal social organization of the prairie vole in bluegrass (medium to low food availability) and alfalfa habitats in September-November. Their results were similar to those recorded during the same months in the present study. Further, social organization in tallgrass prairie habitat in January-February was similar to that observed during the same months in this study. Anecdotal evidence from prairie habitats in Kansas (FITCH 1957), the original low food resource habitat of the species, indicates a similar social organization to that observed in our study. If our hypothesis is valid, it would imply that there has not been sufficient selection for natal dispersal among individuals occupying high food habitats to produce a change in patterns of natal dispersal and social organization. We can only estimate how long prairie voles have had an opportunity to occupy high food habitats. Clover (also a high quality food) was a major crop plant in central Illinois as early as 1850, while alfalfa became a prominent forage crop by 1920. Thus, prairie voles have had an opportunity to occupy high food habitats in this region for approximately 140 years. Estimation of the normal annual reproductive period obtained from a long term demographic study in the region of the study sites (April-midDecember; GETZ et al. 1987) indicates potential for approximately five generations per year. Thus, there has been potential for selection of natal dispersal in high food resource habitats for approximately 700 generations in east-central Illinois. However, the vegetation in the majority of the high food sites (alfalfa and clover fields) is harvested at frequent intervals; as such, these sites do not provide adequate cover to be suitable vole habitat. Most of the suitable vole habitats in east-central Illinois consist of grasses. These habitats provide low to medium food for voles. In spite of the difference in potential reproductive success of philopatric and dispersing females, it would appear the species still retains the basic social behavior that evolved for existence in the original low food habitat. Comparative studies of philopatry, natal dispersal, and fitness in prairie vole populations in food-rich and food-poor habitats will be necessary to assess the costs and benefits of dispersal in relation to food availability. In addition, we need to determine rate of predation in relation to size and distribution of social groups, and whether suites of predators differ between our study site and the original tallgrass habitat occupied by prairie voles.`


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ACKNOWLEDGMENTS This research was supported by grants to L.L. Getz from the National Science Foundation (DEB 78-25864), National Institutes of Health (HD 09328), and the University of Illinois Research Board. The following individuals contributed greatly to the success of the study: Bob Berk, Sandra Edwards, Leah Gavish, Sherri Gruder-Adams, Kathryn Gubista, Wendy Holmgren, Brian Klatt, Patti Malmborg, Phil Mankin, Connie Rinaldo, Pamela Sutherland, Cindy Triebold, Sheila Vanthournout, and Margaret Welke. We are especially appreciative of the enthusiastic assistance of Maria Snarski throughout the study. Finally, we thank Dr John Buonaccorsi for statistical advice.

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LEUZE C.C.K. 1976. Social behaviour and dispersion in the water vole, Arvicola terrestris (Lacépède). Unpublished Ph.D. Thesis, University of Aberdeen. MCGUIRE B. & GETZ L.L. 1991. Response of young female prairie voles (Microtus ochrogaster) to nonresident males: implications for population regulation. Canadian Journal of Zoology 69: 1348-1355. MCGUIRE B., GETZ L.L., HOFMANN J.E., PIZZUTO T. & FRASE B. 1993. Natal dispersal and philopatry in prairie voles (Microtus ochrogaster) in relation to population density, season, and natal social environment. Behavioral Ecology and Sociobiology 32: 293-302. MCGUIRE B. & NOVAK M. 1984. A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Animal Behaviour 32: 1132-1141. MCGUIRE B., PIZZUTO T. & GETZ L.L. 1990. Potential for social interaction in a natural population of prairie voles (Microtus ochrogaster). Canadian Journal of Zoology 68: 391-398. METZGAR L.H. 1967. An experimental comparison of screech owl predation on resident and transient white-footed mice (Peromyscus leucopus). Journal of Mammalogy 48: 387-391. SHIELDS W.M. 1982. Philopatry, inbreeding, and the evolution of sex. Albany: State University of New York Press. SHIELDS W.M. 1987. Dispersal and mating systems: investigating their causal connections, pp. 3-24. In: Chepko-Sade B.D. & Halpin Z.T., Edits. Mammalian dispersal patterns. Chicago: University of Chicago Press. SOLOMON N.G. 1991. Current indirect fitness benefits associated with philopatry in juvenile prairie voles. Behavioral Ecology and Sociobiology 29: 277-282. VERNER L. & GETZ L.L. 1985. Significance of dispersal in fluctuating populations of Microtus ochrogaster and M. pennsylvanicus. Journal of Mammalogy 66: 338-347.