A Population Study of the Prairie Vole (Microtus ochrogaster) in Northeastern Part 2

One female was captured 22 times in the seven-month period of October, 1950, to April, 1951. She used an area of 0.83 of an acre, but this actually comprised two separate ranges. From October, 1950, through December, 1950, she was taken 17 times within an area of 0.12 of an acre; and from January, 1951, to April, 1951, she was taken five times within an area of 0.15 of an acre. The largest area a.s.sumed to represent one range of a female was 0.38 of an acre, recorded on the basis of six captures in three months. The largest area encompa.s.sed by the record of an individual male was 0.41 of an acre. He, too, s.h.i.+fted his range, being taken five times on an area of 0.07 of an acre and twice, two months later, on an area of 0.09 of an acre. Presumably, the remainder of his calculated total range was used but little, or not at all. The largest single range of a male was 0.36 of an acre, calculated on the basis of 18 captures in seven months. The smallest total range for both s.e.xes was 0.02 of an acre.

Many voles s.h.i.+fted their home range and a few did so abruptly. The large range of a female vole, described above and plotted in Fig. 6, indicated an abrupt s.h.i.+ft from one home range to another. More common is a gradual s.h.i.+ft as indicated by the range of the male shown in Fig. 7. Large parts of each monthly range of this vole overlapped the area used in other months but his center of activity s.h.i.+fted from month to month.

[Ill.u.s.tration: FIG. 6. Map with cross-hatched areas showing the range of vole #20 (female). Dots show actual points of capture at permanent trap stations 30 feet apart. Vertical lines mark area in which vole was taken 17 times in October and November, 1950. Horizontal lines mark area in which vole was taken five times in March and April, 1951. This vole was not captured in December and January.]

[Ill.u.s.tration: FIG. 7. Map showing range of vole #52 (male) with seeming s.h.i.+fts in its center of activity. Dots show actual points of capture at permanent trap stations 30 feet apart. Solid line encloses points of six captures in October and November, 1950. Broken line encloses points of five captures in February and March, 1951. Dotted line encloses points of nine captures in April, May and June, 1951.]

That home ranges overlapped was demonstrated by frequent capture of two or more individuals together in the same trap. No territoriality has been reported in any species of _Microtus_, to my knowledge, and my voles showed no objection to sharing their range. Voles taken from the field into the laboratory lived together in pairs or larger groups without much friction.

Definable systems of runways and home ranges were not coextensive.

Runway systems tended to merge, as described later in this report, and relations.h.i.+ps between them and home range were not apparent. Home ranges had no characteristic shape.

LIFE HISTORY

Reproduction

Reproductive activity might have been measured in a number of ways.

Three indicators were tested: the percentage of females gravid or lactating, the percentage of juveniles in the month following the sampling period, and the percentage of females with a v.a.g.i.n.al orifice in the sampling period. The condition of v.a.g.i.n.a proved to be most useful.

Whether or not there is a v.a.g.i.n.al cycle in _Microtus_ is uncertain.

Bodenheimer and Sulman (1946:255-256) found no evidence of such a cycle, nor did I in my work with laboratory animals at Lawrence. How much the artificial environment of the laboratory affected these findings is unknown. The presence of an orifice seemed to indicate s.e.xual activity (Hamilton, 1941:9). The percentage of gravid females in the population could not be determined accurately by a live-trapping study and was not useful in this investigation. The percentage of juveniles trapped in the month following the sampling period tended to follow the curve of the percentage of adult females with a v.a.g.i.n.al orifice. The ratio of trapped juveniles to adults trapped was a poor indicator of reproductive activity. Juveniles were caught in relatively small numbers because of their restricted movements, and no way to determine prenatal and juvenal mortality was available.

Reproductive activity continues throughout the year. Within the thirty-month period for which data were obtained, December and January showed the lowest percentages of females with v.a.g.i.n.al orifices (Fig. 8).

The other months all showed higher levels of reproductive activity with a slight peak in the August-September-October period in both 1950 and 1951. In the species of _Microtus_ that are found in the United States, such summer peaks of breeding seem to be the rule (Blair, 1940:151; Gunderson, 1950:17; Hamilton, 1937b:785). Jameson (1947:147) worked in the same county where my field study was made and found that the high point of reproduction was in March, although his samples were too small to be reliable. The peak of reproductive activity slightly preceded the highest level of population density in each year (Fig. 8).

[Ill.u.s.tration: FIG. 8. Variations in density and reproductive rate of voles, with variation in monthly precipitation. Abnormally low rainfall in 1952 caused a decrease in breeding activity and eventually in the numbers of voles. The solid line indicates the number of voles per acre, the broken line the percentage of females with a v.a.g.i.n.al orifice and the dotted line the inches of rainfall.]

A marked reduction in the percentage of females having v.a.g.i.n.al orifices was observed in the unusually dry summer of 1952. The rate of reproduction was found to be positively correlated with rainfall (Fig.

9). Correlation coefficients were higher in each case when the amount of rainfall in the month preceding each sampling period was used instead of that in the month of the sample. This suggested that the rainfall exerted its influence indirectly through its effect on plant growth.

Bailey (1924:530) reported that a reduction in either the quant.i.ty or quality of food had a depressing effect on reproduction. Drought, such as occurred in 1952, would certainly have a depressing effect on both.

The critical factor seems to be the supply of new, actively growing shoots available to the voles for food rather than the total amount of vegetation. As far as could be determined from the small sample of males examined, their fecundity was not affected by rainfall. Some decrease in the percentage of males that were fecund was noted in the winter and was reported also by Jameson (1947:145) but most of the males in any sample were fecund. Thus any depression in the reproductive rate was due to loss of fecundity by females. This was in agreement with reports in the literature on the subject (Baker and Ransom, 1932a:320; 1932b:43).

The correlation coefficient between rainfall and the percentage of adult females with a v.a.g.i.n.al orifice was 0.53. This was considered to be surprisingly high in view of the expected effects on the breeding rate of temperature, seasonal diet variations and whatever rhythms were inherent in the voles. When only the summer months were considered the correlation coefficient between rainfall and the percentage of adult females with a v.a.g.i.n.al orifice was 0.84. This indicated that, during the season when breeding was at its height, rainfall was a factor in determining the rate of reproduction and when rainfall was scarce, as in the summer of 1952, it seemed to be a limiting factor (Fig. 9).

[Ill.u.s.tration: FIG. 9. Comparison between monthly rainfall and reproductive rate of voles in summer. The dry summer of 1952 caused a notable decrease in reproductive activity. The correlation coefficient between rainfall and the percentage of females with a v.a.g.i.n.al orifice was 0.84.]

Of the total captures 20.6 per cent involved more than one individual.

When the distribution of these multiple captures was graphed for the period of study, a high correlation between the percentage of captures that were multiple and the percentage of females with a v.a.g.i.n.al orifice (r = 0.70) was found. An even higher correlation (r = 0.76) was observed between the percentage of captures that were multiple and the population density. The higher percentage of multiple captures may have been largely a result of fewer available traps per individual on the area and thus only indirectly related to the rate of reproduction.

Of the multiple captures, 66 per cent involved both s.e.xes. The correlation coefficient between the percentage of captures involving both s.e.xes and the level of reproductive activity was 0.58. Among those pairs of individuals caught together more than once, 61 per cent were composed of both s.e.xes. Among those pairs taken together three or more times 76 per cent were male and female and among those pairs taken together four or more times 80 per cent were male and female. When adult voles stayed together any length of time their relations.h.i.+p usually appeared to be connected with s.e.x. Family groups were also noted, as pairs were often trapped which seemed to be mother and offspring. A lactating female would sometimes enter a trap even after it had been sprung by a juvenile, presumably her offspring, or a juvenal vole would enter a trap after its mother had been captured. Such family groups persisted only until the young voles had been weaned.

The youngest female known to be gravid was 26 days old and weighed 28 grams. During summer most of the females were gravid before they were six weeks old, although females born in October and after were often more than 15 weeks old before they became gravid. The youngest male known to be fecund was approximately six weeks old. Male fecundity was determined as described by Jameson (1950). Difference in the age of attainment of s.e.xual maturity serves to reduce the mating of litter mates (Hamilton, 1941:7) and has been noticed in various species of the genus _Microtus_ by several authors (Bailey, 1924:529; Hatfield, 1935:264; Hamilton, _loc. cit._; Leslie and Ransom, 1940:32).

For 35 females, each of which was caught at least once each month for ten consecutive months or longer, the mean number of litters per year was 4.07. Certain of the more productive members of the group produced 11 litters in 16 months. _M. ochrogaster_ seems to be less prolific than _M. pennsylvanicus_. Bailey (1924:528) reported that one female meadow vole delivered 17 litters in 12 months. Hamilton (1941:14) considered 17 litters per year to be the maximum and stated that in years when the vole population was low the females produced an average of five to six litters per year. In "mouse years" the average rose to eight to ten litters per year. During this study several females delivered two or more litters in rapid succession. This was noted more frequently in spring and early summer than in other parts of the year. Those females which produced two or three litters in rapid succession in spring and early summer often did not litter again until fall. Post-parous copulation has been observed in _M. pennsylvanicus_ by Bailey (1924:528) and Hamilton (1940:429; 1949:259) and probably occurs also in _M.

ochrogaster_.

The gestation period was approximately 21 days, the same as reported for _M. pennsylvanicus_ (Bailey, _loc. cit._; Hamilton, 1941:13) and _M.

californicus_ (Hatfield, 1935:264). A more precise study of the breeding habits of _M. ochrogaster_ failed to materialize when the voles refused to breed in captivity. Fisher (1945:437) also reported that _M.

ochrogaster_ failed to breed in captivity although _M. pennsylvanicus_ (Bailey, 1924) and _M. californicus_ (Hatfield, 1935) reproduced readily in the laboratory.

Litter Size and Weight

In the course of this study 65 litters were observed. The mean number of young per litter was 3.18 0.24 and the median was three (Fig. 10).

Three litters contained but one individual and the largest litter contained six individuals. Other investigators have reported the number of young per litter in _M. ochrogaster_ as three or four (Lantz, 1907:18) and 3.4 (1-7) (Jameson, 1947:146). _M. pennsylvanicus_ seems to have larger litters. Although Poiley (1949:317) found the mean size of 416 litters to be only 3.72 0.18, both Bailey (1924:528) and Hamilton (1941:15) found five to be the commonest number of young per litter in that species. Leslie and Ransom (1940:29) reported the average number of live births per litter to be 3.61 in the British vole, _M. agrestis_.

Selle (1928:96) reported the average size of five litters of _M.

californicus_ to be 4.8. Hatfield (1935:265), working with the same species, found that litter size varied directly with the age of the female producing the litter. He reported litters of young females as two to four young per litter and of older females as five to seven young per litter. In the litters of _M. ochrogaster_ that I examined, young females did not have more than three young and usually had but two.

However, older females had litters of one, two and three often enough so that no relations.h.i.+p, as described above, was indicated clearly.

[Ill.u.s.tration: FIG. 10. Distribution of litter size among 65 litters of voles.]

No seasonal variation in litter size was noted. The mean size of the litters in 1950, 2.68 0.30, was significantly lower than that found in 1951 (3.76 0.20) but neither differed significantly from the mean size of litters in 1952 (3.35 0.66). The lower mean size of litters was in part coincidental with a high population level and the higher mean of the two later years was in part coincidental with a low population level. Since a sharp break in the curve for population density occurred after the flood in July, 1951, the litters were arranged in pre-flood and post-flood categories for study. Pre-flood litters averaged 3.07 0.28 young per litter whereas post-flood litters averaged 3.34 0.48.

This difference was not significant. Increase in litter size, if it had actually occurred, might have been a response to the increasing food supply and lower population density after the flood.

A difference in the mean number of young per litter was noted for those litters delivered in traps as compared with those delivered in captivity and the numbers of embryos examined in the uterus. The mean number of embryos per female was higher than the mean number of young per litter delivered in captivity and the mean number of young per litter delivered in traps was lower than in those delivered in captivity. The differences were not statistically significant. In some instances females that delivered young voles in traps may have delivered others prior to entering the trap or the mother or her trapmates may have eaten some of the newborn voles before they were discovered.

The mean weight of 16 newborn (less than one day old) individuals was 2.8 0.36 grams. No other data on the weight of newborn _M.

ochrogaster_ were found in the literature but this mean was close to the 3.0 grams (Bailey, 1924:530) and 2.07 grams (Hamilton, 1937a:504; 1941:10) reported for _M. pennsylvanicus_ and to the 2.7 grams (Selle, 1928:97) and 2.8 grams (Hatfield, 1935:268) reported for _M.

californicus_. No correlation between the weight of the individual newborn vole and the number of voles per litter was observed.

Although the ratio of the average weight of newborn voles to the average weight of an adult female was approximately equal for _M.

pennsylvanicus_ and _M. ochrogaster_, the ratio of the weight of a litter to the average weight of an adult female was larger in the eastern meadow vole because the mean litter size was larger. Perhaps this is related to the more productive habitat in which the eastern meadow vole is ordinarily found.

Size, Growth Rates and Life Spans

The mean weight of adult voles during the period of study was 43.78 grams. The females averaged slightly heavier than the males but the overlapping of weights was so extensive that s.e.xual difference in weight could not be affirmed. The difference observed was less in December and January when gravid females were rare, suggesting that the difference was due, at least in part, to pregnancy. Jameson (1947:128) found, for a sample of 50 voles, a mean weight of 44 grams and a range of 38 to 58 grams. The range in the adult voles I studied was much greater, from 25 to 73 grams. In part, this increase in the range of adult weights was due to a much larger sample.

[Ill.u.s.tration: FIG. 11. Relations.h.i.+p between rainfall and the mean weight of adult males in summer. The abnormally low rainfall in the summer of 1952 was accompanied by a decrease in mean weight. The solid line represents mean weight and the broken line rainfall. The correlation coefficient between the two was 0.68.]

During the unusually dry summer of 1952, a notable reduction in the mean weight of adults was recorded (Fig. 11). The correlation coefficient between the mean weight of adults and the amount of rainfall for the summer months was 0.68. It seems reasonable to attribute the drop in mean weight to an alteration of plant growth due to decreased rainfall.

Some of the reduction in mean weight was due to the loss of weight in older individuals but most of it was due to the failure of voles born in the spring to continue growing.

No data on the growth rate of _M. ochrogaster_ were found in the literature. According to the somewhat scanty data from my study, secured from observations of individuals born in the laboratory, young voles gained approximately 0.6 of a gram per day for the first ten days, approximately one gram per day up to an age of one month, and approximately 0.5 of a gram per day from an age of one month until growth ceases. This growth rate was especially variable after the voles reached an age of thirty days. The growth rate approximates those described for _M. pennsylvanicus_ (Hamilton, 1941:12) and for _M.

californicus_ (Hatfield, 1935:269; Selle, 1928:97). Although the data were inadequate for a definite statement, I gained the impression that there was no difference between the s.e.xes in growth rate. In general, young voles grow most rapidly in the April-May-June period and least rapidly in mid-winter. Several voles, born in late autumn, stopped growing while still far short of adult size and lived through the winter without gaining weight, then gained as much as 30 per cent after spring arrived (Fig. 12).

[Ill.u.s.tration: FIG. 12. Growth rates of two voles selected to show typical growth pattern of voles born late in the year. Growth nearly stops in winter and is resumed in spring.]

The recorded life spans of most voles studied were less than one year.

No accurate mean life span could be determined. Leslie and Ransom (1940:46), Hamilton (1937a:506) and Fisher (1945:436) also found that most voles lived less than one year. Leslie and Ransom (_op. cit._: 47) reported a mean life span of 237.59 10.884 days in voles of a laboratory population. In the present study one female was trapped 624 days after first being captured; another female was trapped 617 days after first being captured; and a male was trapped 611 days after first being captured. The two females were subadults when first captured. The male was already an adult when first captured; consequently its life span must have exceeded 650 days. No evidence of any decrease in vigor or fertility was observed to accompany old age.

Of the 45 marked voles snap-trapped in August of 1952, 21 had been captured first as juveniles. The ages of these voles could be estimated within a few days, and the series presented a unique opportunity for studying individual and age variation. Only individuals weighing less than 18 grams when first captured were used, and their ages were estimated according to the growth rate described above. Howell (1924) reported an a.n.a.lysis of individual and age variation in a series of specimens of _Microtus monta.n.u.s_, and Hall (1926) studied the changes due to growth in skulls of _Otospermophilus grammarus beecheyi_. The series of specimens described here differs from those of Hall and Howell, and from any other collection known to me, in the fact that the specimens are of approximately known age and drawn from a wild population.

Unfortunately, this sample was small, and the distribution of the specimens among age groups left much to be desired. No specimens less than one and one-half months old were taken and only a few individuals older than four and one-half months. Table 3 shows the age distribution.

The small size of the sample and the absence of juveniles were due, partly, to the unusually dry weather in the summer of 1952. The reduction in the rate of reproduction, caused by drought (as described elsewhere in this paper), reduced the populations and the percentage of juveniles to low levels.