[Pg 129]

University of Kansas Publications

Museum of Natural History

Volume 10, No. 4, pp. 129-161, 8 figs. in text,
6 tables

  December 19, 1957  

Aspects of Reproduction and Development

in the Prairie Vole (Microtus ochrogaster)

BY

HENRY S. FITCH

University of Kansas

Lawrence

1957

[Pg 130]

University of Kansas Publications, Museum of Natural History



Editors: E. Raymond Hall, Chairman, Henry S. Fitch,

Harrison B. Tordoff









Volume 10, No. 4, pp. 129-161, 8 figs. in text,
6 tables



Published December 19, 1957















University of Kansas

Lawrence, Kansas

PRINTED IN

THE STATE PRINTING PLANT

TOPEKA, KANSAS

1957



29-5936

[Pg 131]

The prairie vole is by far the most abundant mammal on the
University of Kansas Natural History Reservation and on grassland
areas throughout northeastern Kansas. This vole therefore affects
the vegetation, perhaps more than any other native vertebrate, and
it is an important food source for most of the vertebrate predators.
Since the Reservation was established, in 1948, more data have been
accumulated concerning this vole than for any other species of
animal there. From February, 1950, to February, 1954, a grid of
live-traps at 50-foot intervals was set for several days each month
in a three-acre field inhabited by voles, and the population of
marked individuals was studied throughout the four-year period. From
November, 1953, to June, 1956, a half-acre trap grid with 20-foot
interval was used on an area adjoining the three-acre field. Other
trap lines in somewhat different habitats were maintained for
shorter periods as a basis for comparison. By June, 1956, a total of
some 3550 voles had been caught and recorded 14,750 times in all.
The present report is a preliminary attempt to analyze, in part,
these extensive data, and is concerned with certain phases of the
species' reproduction and growth that have bearing on the observed
population changes from month to month and from year to year on the
Reservation.

Through the studies of Jameson (1947) and Martin (1956), both made
in the same general area as my own, and several earlier studies, the
life history and ecology of the prairie vole are already well known.
The present report, with much larger amounts of data, further
clarifies certain phases of the ecology; and by using types of data
not available to Jameson and Martin I have dealt with some topics
not included in their reports.

Previous studies of growth in Microtus have been based almost
entirely on weights. However, the weight of an individual vole may
fluctuate widely over a short period, depending on pregnancy and
parturition, length of time in a trap without food, availability of
moisture, and other factors. In the course of my study, in 1954
[Pg 132]
and 1955, and parts of 1953 and 1956, measurements of total length, in
addition to weights, were recorded for most of the voles
live-trapped.

To test the accuracy of measurements, successive readings were
compared in individual voles that were already of large adult size
and that presumably either had stopped growing or were growing so
slowly that the gain was scarcely detectable in the relatively short
periods involved. For 200 such readings 33 per cent were just the
same as previous records for the same animals, 24 per cent deviated
by 1 mm., 22 per cent deviated by 2 mm., 15 per cent by 3 mm., 4.5
per cent by 4 mm., .5 per cent by 5 mm., 1 per cent by 6 mm., and .5
per cent by 7 mm. On the average, successive measurements varied by
1.43 mm., somewhat less than one per cent of the adult vole's total
length. Occasional errors of two to four per cent were easily
eliminated because for the voles used for growth records, series of
measurements were available, with clearly defined trends. The
occasional readings that deviated from the general trend for the
individual were discarded.

Measurements were recorded along with other data in the field at the
point of capture. Obtaining a reasonably accurate measurement on a
live and struggling vole required patience and practice. With the
thumb and forefinger of the left hand, I grasped the vole by loose
skin of the nape, and simultaneously grasped the tail at a point
approximately three-fourths of the distance to the tip. Then, with
gentle but steady pressure, I stretched the vole out to its full
length, meanwhile manipulating a millimeter ruler with the free
fingers, so that the vole was pressed against it, with the nose pad
at the end of the ruler.

The total length measurement is considered the best index to
over-all size. The relative tail-length varies slightly between
individuals, averaging approximately 22 per cent of the total
length. Individuals having broken tails, or having the distal parts
of their tails missing, were not included. The total length can be
measured with greater accuracy than can either the head-and-body
length or the tail-length separately.

As compared with other mammals, voles are tolerant and somewhat
social. That individuals are not mutually exclusive (territorially)
in areas occupied was demonstrated on many occasions when more than
one individual was caught simultaneously in the same live-trap.
Injury of a vole by a trap-mate was a rare occurrence.

[Pg 133]
Multiple captures often involved a female in oestrus and one or more males,
or a female and her young, but other instances involved various
combinations of sex and age groups. As many as five adults have been
caught in a trap simultaneously at times when the population density
was high. At such times, the meadow habitat is crossed by a maze of
interconnecting surface runways and one runway may be traced
continuously for 100 yards or more. Because each individual vole
normally confines its activity to a small area, only a fraction of
an acre, it is evident that individuals living at different places
overlap in their home ranges, and also in the trailways followed in
foraging. A high degree of tolerance is indicated. Where population
is so sparse that the systems of surface runways comprise separate
and isolated units, trapping experience has shown that one such
system may harbor several or many individuals.

As direct observations on voles under natural conditions are rarely
feasible, because of the animals' timidity, their utilization of
concealing cover, and tendency to crepuscular habits, best evidence
of social habits and underground life is based upon behavior of
captive individuals. Many voles were kept in confinement for varying
lengths of times, either singly or in association with others. Under
such conditions there was sometimes sporadic fighting, but it was
mainly defensive and serious injuries were rare. Two or more voles
caught at a given spot regardless of whether they were found in the
same trap simultaneously, or trapped separately within a short time,
usually were completely tolerant of each other. When at rest in
their container, such voles would huddle together in a corner or in
a nest, if materials were provided, so that collectively they
presented the minimum exposed surface. The intimacy and lack of
antagonism displayed on such occasions, suggested that the voles
were accustomed to living together amicably in the same nest
chamber. In live-trapping, "double" captures in a single trap often
involved the same two individuals. Such trap-mates were often male
and female, and in many instances the female was not in breeding
condition. That the voles are not monogamous in habits was
demonstrated when the same female was often trapped in association
with either of two males. Other trap associates taken together
repeatedly often were two males, or two females. Voles that are nest
mates or "neighbors" may tend to move about together in their
foraging, or one confined in a trap may attract the other
sufficiently to cause it to force an entrance by lifting the heavy
door of a trap.

[Pg 134]
When a new vole, caught at a different location, is added to a
container in which one or more are already confined, there is mutual
circumspection between the original occupants and the newcomer. At
first, each vole is intimidated by movements of the other, and as a
result, the original occupants huddle in their established corner
while the newcomer cowers in the most remote part of the container.
Gradually the voles become less timid and one may approach another
slowly and cautiously, to sniff at it. The vole approached may react
with a show of hostility which is largely defensive. In the
characteristic posture of threat for defense, the vole crouches, or
rears back on its haunches, with snout elevated and incisors
prominently displayed. If the warning posture is unheeded, or if the
vole is made unusually aggressive by having young to defend, or for
some other reason, it attacks with a sudden forward lunge, striking
the adversary simultaneously with both forefeet and with the
incisors. The lunge is so rapid that when I have observed it, I have
been unable to discern whether the attacker bit its opponent. The
attack serves to force back the other animal, throwing it off
balance and intimidating it. The attacked animal may dodge nimbly to
avoid the lunge, but whether or not it is actually struck, it
usually retreats, avoiding or postponing further hostilities. Voles
that have been kept in containers for periods of hours or days tend
to be more hostile and aggressive toward a newcomer than are those
newly introduced. After series of meetings resulting from the
exploratory behavior of the newcomer and the curiosity or normal
activity of those longer confined, hostility gradually subsides.
Within a few hours a newcomer is usually accepted, and thenceforth
he huddles with other members of the group when at rest, and
hostility is rarely evident.

This ready acceptance on short acquaintance of strange voles into
the family or social group suggests that lack of territoriality
extends even to the use of the nest burrows, and that groups of
voles may share the same nest, huddling together and deriving mutual
benefit from the association, such as warmth in cold weather.
Schmidt (1931: 113), studying this vole in Clark County, Wisconsin,
noted its colonial habits. He found isolated small mounds that were
riddled with burrows, and little sign in intervening areas. At one
mound he trapped two adult males, one adult female, and two young;
at another mound, two adult males, two adult females, and four young
were trapped. My individuals that were released from live-traps were
on many occasions trailed by means of a stiff wire collar with spool
of thread attached, to holes that presumably
[Pg 135]
were their home burrows. Data obtained in this manner indicated that
ordinarily several or many individuals use the same burrow system.
The histories of individual voles on the study area at the
Reservation indicate shift of home base from time to time, usually
for short distances within the area already included in the home
range, but occasionally to new areas relatively remote from the
original home range.

Severe fighting between adult prairie voles occurs at times.
Occasionally, sharp squeaks accompanied by brisk rustling in the
grass suggesting pursuit or conflict, are heard in their habitat. An
unusually large adult male, long resident on a study area, suddenly
lost weight and deteriorated in condition over a period of several
days, then was found dead in a nest-box attached to a trap.
Dissection revealed numerous punctures in the skin and flesh of the
neck and back, probably made by the incisors of another vole.
Extensive hemorrhage and swelling had occurred, and obviously these
injuries were the cause of death.

Although it was not feasible to study the home life of the voles
underground, clues were gained from those uncovered in runways and
nests beneath large boards and strips of tarpaper, previously
distributed for this purpose. Nests were constructed by the voles
beneath several such pieces of tarpaper and runways appeared beneath
all the pieces that were placed in habitat favorable to the voles.
In summer, however, the high daytime temperatures beneath these
shelters made them uninhabitable to the voles, and they were used
mainly in spring. From February 15 to May 1, 1953, 14 voles were
caught 19 times beneath five of the tarpaper strips, and many other
voles that were seen beneath them escaped. Upon turning one of the
strips I often discovered voles in close proximity. Sometimes two or
more darted from the same nest. The disturbance of repeatedly
raising the strips and exposing the voles' shelters soon caused them
to desert the sites; consequently the information obtained by this
means was limited.

There is sexual activity in every month of the year, but its
incidence varies greatly from one season to another. As has been
indicated by various authors, male voles reach sexual maturity later
than females. It seems that ordinarily the availability of sexually
active males is not a limiting factor, however. While males that are
still well below average adult size produce mature spermatozoa, and
are probably capable of breeding (Jameson, 1947: 145), certain
[Pg 136]
large old males may sire a disproportionately large percentage of the
litters produced. Observations on males in confinement indicated
that sexual activity tended to be directly proportional to the size
of the testes. Occasional individuals, having much enlarged scrotal
testes were more readily stimulated to sexual activity and more
aggressive toward females than were those in which the testes were
of more nearly typical size or abdominal or were smaller than
normal. The combination of factors controlling size of testes is not
well understood, but males having unusually large testes were caught
most often when food supply was optimum, for instance after a period
of heavy precipitation when an abundant supply of new grass provided
succulent and nutritious food.

In confinement sexual activity was largely inhibited and attempts to
establish a laboratory colony met with failure. Sexual activity was
observed mainly in recently captured males, and their interest was
aroused chiefly by females that had given birth to litters within a
few hours previously. Oestrus is known to follow closely after
parturition. Females found in live-traps with newborn young often
were brought to the laboratory for observation. An apparent instance
of hostility between rival males competing for an oestrus female was
observed on September 2, 1950. The female was found in a trap with
four newborn young, and since the young had not yet attached to her
teats, she was temporarily returned to the trap after recording, to
prevent desertion of the litter. Returning twenty minutes later I
found another adult vole at this trap. It would suddenly emerge from
dense grass nearby, and would move over the trap or around it, with
jerky, halting movements, then would dart back under cover. The
female emerged from the nest box into the trap runway, and sniffed
at the other, and both pressed against the intervening wire barrier.
There was gnawing on the wire by one or both. A third adult vole
appeared. As it moved toward the trap, all three suddenly took alarm
and darted back under cover, the female hiding in the trap nest box.
In a few seconds they again appeared. The two outsiders, presumably
both males, were not individually recognizable, but several times
one was seen to dart at the other, chasing it away momentarily. They
were seldom both in sight at once.

Males confined with post-partum females usually evinced sexual
interest, following them about persistently and nuzzling their
genitalia. The females, however, were often unreceptive perhaps
because they were disturbed by strange surroundings and by the
presence of their litters, so that they usually attempted to escape,
[Pg 137]
or to rebuff the male's attention. At first the female might flee,
squeaking in protest at the male's pursuit. If he still continued to
follow, she would turn on him, rearing back in the characteristic
threatening pose, and would lunge at him, striking him sharply or
driving him back. After such rebuff, males were usually intimidated
or discouraged so that they temporarily or permanently abandoned
their advances, and small males were more easily rebuffed than were
larger individuals. On several occasions large males having enlarged
testes were not readily rebuffed by females but continued to follow
them. When the female turned upon him, such a male might lunge
against her, throwing her off balance, and causing her to attempt to
escape, and then continuing the pursuit until it ended in copulation
or in more severe fighting. Although not accepted sexually, a
rebuffed male might be readily accepted as a nest-mate, huddling
along with the female and perhaps other individuals of both sexes.
In huddling voles, the most frequently observed type of social
behavior was grooming; one individual would slide its chin or muzzle
through the other's fur with a stroking movement consisting of a
series of rapid forward jerks and the stroking movements might
continue for periods of minutes. The recipient of the grooming
usually made no evident response indicative of either pleasure or
displeasure. Often it seemed to be sleeping while the grooming was
performed. Individuals of both sexes performed this grooming and the
recipient might be of either the same sex or the opposite sex. This
grooming may have some significance as a search for ectoparasites
such as fleas, or mites that often infest the voles. However, after
prolonged grooming by a companion, a vole's fur was of mussed and
disarranged appearance. Although the grooming that occurs between
voles that are resting in nests seems to have no direct significance
as sexual behavior, somewhat similar actions constitute part of the
mating pattern. A sexually aroused male overtaking a receptive
female, slides his chin forward along her back with jerky, stroking
movements. In some observed instances this behavior continued
intermittently for several minutes before actual copulation. In some
other instances it was almost lacking.

In female voles that are sexually quiescent, both those that have
not yet attained breeding maturity, and those that have undergone
regression after attainment of sexual maturity, the vaginal orifice
is not evident. The canal is sealed externally by a membranous
[Pg 138]
layer of epithelium. Presence of a vaginal orifice indicates that the
individual is in some active stage of the breeding cycle.
The appearance of the orifice varies between different females, and
it changes in the same female from day to day or even from hour to
hour. Presumably these changes in the vaginal orifice are cyclical
and are closely correlated with oestrus, but attempts to trace them
were unsuccessful largely because the normal cycle was rapidly
suppressed in captive voles, which soon became sexually quiescent.
Individual voles living under natural conditions were not trapped
with sufficient regularity to permit tracing the details of changes
in their genitalia.

In those females having the vaginal orifice most developed, the
margins are turgid and slightly inflamed. The circular opening gapes
1.0 to 1.5 mm. in diameter when the tail is raised. A female may
remain in this condition for two days or more. Vaginal smears at
this stage often showed nucleated cells characteristic of oestrus.
Subsequently the margins of the orifice become less prominent and
the opening becomes smaller. The dorsal and ventral walls adhere
until an opening is no longer evident unless the adjacent skin is
stretched.

In pregnancy the orifice is occasionally sealed, but usually is
evident. It is, however, less prominent than in oestrus, and does
not gape. The margins are less turgid than in oestrus, and the
opening is in the form of a transverse slit through which the
purplish epithelial lining of the dorsal wall of the vagina can be
seen. After parturition, placentae and bloody discharge often are in
evidence in the vaginal canal. Females that have not given birth to
young recently may also have bloody mucous discharge. Its
significance has not been determined. In females that are undergoing
sexual regression, the margins of the vaginal orifice become
shrunken and pale, and the orifice becomes partly or wholly sealed.

Bodenheimer and Sulman (1946:255) concluded from their study of
Microtus guentheri that in this species, as in "the cat," "the
rabbit," "the ferret," and a few other mammals, ovulation is induced
by copulation, and that there is no regular vaginal cycle. Hoyte
(1955:412) disagreed with these conclusions for other species of
Microtus, as he trapped individuals of M. oeconomus that had
recently ovulated without copulation (at least no sperm were found
in the genital tracts). In M. ochrogaster oestrus seems to be
controlled largely by the food supply, at least the incidence of
perforate females was found to fluctuate irregularly tending to
follow the trend of rainfall, and, probably in more direct
correlation, the amount
[Pg 139]
of new grass present (see Table 1, and Martin, 1956:383-384). It
therefore seems unlikely that in this species ovulation is dependent
on copulation.

In females that have not yet produced young the teats are minute and
well concealed in the fur, so that they are difficult to find, but
in lactation they become conspicuous. In early lactation the teats
are typically about 1 mm. in diameter and 2.5 mm. in length. As
lactation progresses, they become thickened to nearly twice the
original diameter. After lactation, as inversion occurs, they shrink
to scabrous low prominences, 2 mm. to 3 mm. in diameter, surrounded
by bare skin. There are three pairs of mammae, one pair pectoral and
the other two abdominal. As mentioned by Jameson (1947:146), the
pectoral mammae show little evidence of use in lactating prairie
voles. Probably they are not used at all except in females with more
than the four young in a litter accommodated by the abdominal
mammae. As in various other rodents, the suckling young may cling to
the female's teats and may be dragged over the ground as she moves
about. When the female forages near the nest, she may drag the young
with her instead of leaving them, but she can detach them instantly
if she so desires. On many occasions females found in live-traps had
young that were several days old clinging to their teats. In some
instances young that had their eyes open may have followed the
female into the trap and attached afterward.

In the region of my study the prairie vole breeds the year round,
but the rate of breeding changes continually. There is no regularity
in the trend of the breeding season from year to year. It is obvious
that the species is responsive to environmental changes and is so
well attuned that its breeding is speedily initiated or inhibited by
changes to favorable or unfavorable weather. The incidence of
breeding is highest when temperature is moderate and both water and
foods of preferred sorts are plentiful.

Tables 1 and 2 and Fig. 1, based on 11,109 records representing each
month over a four-year period, show the changing trends from month
to month. The perforate condition recorded in Table 1 may represent
any of several stages in oestrus or pregnancy, but is regarded as a
crude index of rate of breeding, since voles in the anoestrus stage
lack the vaginal orifice. Highest percentages of perforate females
occurred in the months of February, March, April, May, and June,
while by far the lowest percentages were recorded in the drought
summers of 1952 and 1953. Even in mid-winter a substantial
proportion of the females trapped were perforate.

[Pg 140]

Fig. 1. Average catch per day in a three-acre field, in a grid of 100 live-traps,
over a four-year period. For each year, solid line represents total and dashed
line represents number of young up to 30 grams in weight. Numbers caught
are roughly indicative of population density, but many variables distort this
relationship. Young are never represented in the catch in their true ratio to
adults, since on the average they are less vagile and less attracted to traps.

[Pg 141]

Usually pregnancy can be recognized only in the last week before
birth of the litter, when the female's abdomen is noticeably
distended by the enlarged fetuses. Palpating to detect embryos
was not attempted because of the danger of injuring them or the
female. Because gestation is of approximately three weeks duration,
the figures in Table 2 represent roughly perhaps one-third,
or a little less, of the adult females actually pregnant. At most
times of year a substantial proportion of adult females (sometimes
nearly all) are pregnant. Only in the winter (including March
in 1951) were samples taken in which no recognizably pregnant
females were found. Incidence of pregnancy was notably high in
July, August, September, and October of 1950, May, 1951, May,
1952, and April and May, 1953. A high rate of breeding was not
necessarily followed by an increase in the population. A relatively
low rate of breeding was adequate to maintain the population
level, provided that environmental factors remained favorable.
Fig. 1 shows the average catch per day (with approximately 100
live-traps) over the four-year period, 1950 through 1953. The
young (including all those weighing 30 grams or less, and corresponding
roughly with the part of the population less than two
months old) are shown separately. It is noteworthy that throughout
[Pg 142]
the entire period the ratio of young to adults tended to be
fairly stable—usually fluctuating between ten and thirty per cent
of the total catch. Ratios of young to adults were notably high
in March and May, 1950; April, June and July, 1952; and April,
May and June, 1953. Ratios of young were notably low in June and
December, 1950; January, February, March, and June through
October, 1951; January, February, and March, 1952; and November,
1953.

In Fig. 1 the catch per day of voles, varying from month to
month, reflects chiefly the changing population density. However,
other factors also have important effects on the catch. For example,
bait acceptance is better in the winter when natural foods, especially
greens, are scarce, with the result that a higher catch can be made
with the same population density. Interference with the trap line
by other animals also affected the catch of voles. In warm weather
the traps were checked in both morning and evening, and the
catch was correspondingly greater than it was in cool weather
when the traps were checked only once daily. The ratios obtained
of young to adult voles cannot be accepted at face value as the
true ratios in the population, either. For the first several days of
each trapping period, the voles caught were mostly adults previously
marked and, presumably, conditioned to the grain bait.
Later, young voles not previously recorded, came to the traps in
increasing numbers. The young, being at first not conditioned to
the bait, and also having relatively small home ranges, would
generally be less well represented in the catch than would the
adults.

In other species of Microtus, so far as known, a 21-day gestation
period seems to be the rule (Bailey, 1924:528; Hamilton, 1941:13;
Hatfield, 1935:264). M. ochrogaster seems to conform to this
pattern, but the data obtained were meager, because breeding
activity was usually inhibited in voles kept in confinement.

A female live-trapped on July 23, 1951, appeared to be in
breeding condition. When trapped two days later, she had a
copulatory plug, and 21 days after this she was found with a newborn
litter in a trap. A female thought to have given birth to a
litter between successive captures on July 20, and July 21, 1951
(on the basis of appearance of genitalia, and reduction in weight
from 53 to 46 grams), appeared to have just completed parturition
[Pg 143]
when she was examined on August 10. A female that gave birth to
a litter in confinement on May 18, 1954, bred and was released the
same day. She was recorded as pregnant in the first week of June,
but on June 7 was no longer pregnant. If this pregnancy terminated
normally, a gestation of 20 days or less is indicated.

Greenwald (1956:221) suggested that in M. californicus, oestrus
might occur in the period of lactation, because he found recently
formed corpora lutea in lactating females. In the course of my
field work on M. ochrogaster, I obtained precise or approximate
dates of successive litters born at intervals of somewhat more than
21 days apart. In different females, intervals of 23, 23, 24, 26,
and approximately 27 (between 26 and 28) days were recorded
between successive litters. In four other females intervals between
litters were known only approximately because one of two records
was based on a capture in late pregnancy judged to be within
two or three days of parturition. For these females, intervals of
23, 24, 24, and 26 days were recorded. From the trend of these
records, it seems that females often became pregnant within a
few days after birth of a litter. Pregnancy from post-partum
oestrus would seem to be less frequent than pregnancies beginning
a few days after birth of the previous litter, and within the period
of lactation.

Jameson (1947:146) found an average of 3.4 young per litter
in 58 litters of M. ochrogaster from northeastern Kansas, mostly
from Douglas County. Martin (1956:386) recorded a somewhat
lower mean of 3.18 ± 0.24 in 65 litters on the Reservation in 1950,
1951, and 1952. For a total of 82 litters recorded from 1950 through
1956, inclusive, I obtained an average of 3.37 ± .075 young per
litter. Several litters that were recorded were excluded from this
computation as in each instance there was reason to suspect that
they were incomplete. These included instances of females found
in traps with young several days old, females that may not have
completed parturition when they were released with newborn
young, and those litters that might have sustained losses through
cannibalism by the mother or her trap-mates.

Mean numbers of young per litter were found to vary from year
to year and from month to month, as shown by the following lists:
1950, 3.0 (13 litters); 1951, 3.5 (23 litters); 1952, 3.5 (11 litters);
1953, 3.4 (5 litters); 1954, 3.4 (15 litters); 1955, 4.1 (7 litters);
1956, 3.8 (5 litters); January 2.0 (1 litter); February 3.5 (4 litters);
[Pg 144]
March 4.5 (4 litters); April 3.9 (12 litters); May 3.3 (25 litters);
June 3.0 (9 litters); July 2.7 (4 litters); August 2.9 (7 litters); September
2.8 (6 litters); October 3.4 (7 litters); November 5.0 (2 litters);
December 4.0 (1 litter).

These differences can be logically explained on the basis of
changes in the average age of the breeding females in the population.
On the average, with greater length, weight and age, females
produced progressively larger litters, although individuals
did not necessarily conform to this general trend. For 24 females
recorded in 1954-1956 and measured within a few days of birth of
their litters, average length was correlated with number of young as
follows: 6 young, 163.5 mm.; 5 young, 158.0 mm.; 4 young, 157.7 mm.;
3 young, 154.6 mm.; 2 young, 160.5 mm.

For 48 other females, recorded in 1950-1953, that were not measured,
but that were mostly assignable to broad age groups on the
basis of their individual histories in the trapping records, the following
well defined trend was demonstrated.

It seems that the exceptionally high average numbers of young
per litter in March and April result from the breeding females in
those months being nearly all fully mature survivors of the previous
year. In summer, when many females that are only a few weeks
old become pregnant, the average litter declines to less than three
young. The small average litter of 3.0 young for 1950 probably
resulted from the fact that the population on the Reservation was
then expanding rapidly in the newly favorable habitat created by
one year's crop of vegetation after discontinuance of grazing, and
had an unusually high percentage of breeding females that were
not fully adult.

[Pg 145]

In four newborn young, total lengths, in mm., were 47, 45, 45,
and 42. From the length-weight relationships shown in Fig. 2, it
seems that a length of approximately 47 mm. is typical of newborn
young of average weight. Martin (1956:388) found a mean
weight of 2.8 ± 0.36 grams in sixteen newborn prairie voles from
the Reservation. For a series of 67 other newborn voles representing
27 different litters in seven different years, I found an average
of 2.9 ± .05 grams. Young ranged in weight from 3.8 to 2.0 grams.
Weights of the newborn voles could not be correlated with season,
size, age of females, or food conditions. However, a distinct trend
toward larger size in those litters that contained fewer young was
evident, as shown in Table 4.

Voles less than 100 mm. in total length were seldom captured,
because those less than this size are dependent on the female,
and rarely venture far enough from the nest to be caught in a trap.
A further difficulty in obtaining growth records on the smallest
young is that of making accurate measurements. During their
first few days they partially retain the fetal posture, usually lying
on one side, with the head, body and tail flexed in an arc almost
completed by the tail approximating the muzzle. Straightening
the animal by stretching it and holding it with sufficient firmness
to obtain a measurement might have involved injury to it. Therefore,
in most instances the newborn voles examined were merely
weighed or an approximate measurement was estimated without
stretching the young to its full length.

Newborn voles were obtained when females that were caught
in live-traps produced their litters before they were found and released.
[Pg 146]
In some instances, females caught while in late pregnancy
were retained in the laboratory for a day or more until parturition
occurred. Many of the newborn voles were marked by toe-clipping,
according to the same system used for adults. Early growth
was measured in some instances by keeping the female with her
litter in confinement, measuring and weighing the young at intervals.
In most instances, the female was released at the point of
capture (presumably near her nest burrow) with the young clinging
to her teats. For the young so released, the incidence of recovery
was remarkably low, seeming to indicate that they were
subject to decimating losses. Perhaps such losses are normal,
at least on the study area where voles are live-trapped regularly.
Holding of adults and partly grown young in live-traps ordinarily
has no harmful effects on them, but the resultant separation of females
from newly born litters may often result in death of the
young either from hunger and exposure, or from attack by other
voles and natural enemies.

During the first ten days the increase in length from an original
47 mm. is from three to four mm. per day. Figs. 2,
5, and 8 show
length and weights of voles whose ages in days were definitely
known because they were born in the laboratory, or in a live-trap
after the female was caught there. Young voles marked at birth
and released with the female were rarely recovered in the period
of suckling, as they ordinarily remain in the nest burrow when
the female ventures out to forage. Litters retained in the laboratory
therefore have provided most of the records of growth in suckling
young. Growth varied greatly between litters. It was not
clearly correlated with size of female, size of young at birth, or
number of young in litter, but probably was influenced by attentiveness
of the female, her adjustment to captivity, and her productivity
of milk. Within each litter there were usually persistent differences
in development, but these were minor (except for those of occasional
runts) compared with the differences between litters. In
several litters of five young, one was usually smaller than the others
at birth and therefore could not compete successfully with its
litter mates, so that it never gained possession of a teat other than
one of the pectoral pair, and always succumbed within a few days,
after failing to gain weight as its litter mates did. The relatively
few voles marked at birth and recovered after developing under
natural conditions, did not deviate from the trend of those in confinement.

[Pg 147]

Females in confinement were attentive to young, and, soon after
parturition, licked them clean and huddled over them protectively.
Ordinarily, the newborn young soon attached to a teat, and spent a
large part of its time attached during its early development. Females
found in live-traps with their litters of young less than a day
old, often had some or all of the young clinging to their teats. Females
with newborn litters, when released from live-traps, always
left without attempting to retrieve any young that were unattached.
Such young usually were permanently deserted, but in some instances
disappeared within an hour or less, perhaps rescued by
the female returning for them.

Females with newborn young were made far more aggressive
than most other voles by their tendency to protect their young
from possible danger. In captivity such females usually took the
offensive in attacking or rebuffing any other voles confined with
them. Post-partum females obviously in oestrus were prevented
from being fully receptive by their hostility toward males whose
presence might endanger the young. Such a female has been seen
to turn on a pursuing male and attack him viciously, several times
within a few minutes, before copulation occurred. In captivity,
at least, such attacks would soon discourage a male so that unless
he was exceptionally active sexually, mating was prevented.

Cannibalism, involving destruction of the newborn, is probably
an important factor in the population dynamics of the prairie vole.
Only a small percentage of the young known to have been born
on an area ever survived to be live-trapped; this small percentage
was indirect evidence of decimating losses in the young. Under
unfavorable conditions each of several females killed and ate her
own litter, but the degree of provocation varied greatly among
individuals. Females that gave birth to young in live-traps occasionally
ate one or more of their newborn young, as evidenced
by discarded remnants. Perhaps other instances passed unnoticed
because no remnants were found. That need for food or moisture
as well as psychological stress often motivated such cannibalism
was suggested by the fact that surviving litter mates might be
accepted and cared for by a female that had already eaten one or
more of her young. Although cannibalism is most likely to occur
within a few hours after birth of the young, they may be killed
and eaten at any stage of development. One female that had probably
[Pg 148]
eaten one or more of her litter, soon after parturition, nursed
the two survivors. When these were two weeks old, all were
"pastured out" in a wire mesh cage in tall brome grass. When
the supply of grass had become scarce (though some was still available),
the female killed and partly ate both her remaining young.

One female was captured with three young attached that were
several days old. The young were detached from the female's teats
with great difficulty. When these young were returned to the female
a few minutes later, after they had been measured, weighed
and marked, she attacked them viciously, and within a few seconds
had killed all of them by biting their heads. In this instance the
dead young were not eaten, although they were temporarily left
with the female.

Females with young have ample cause for their circumspective
demeanor toward adult males, which are especially inclined to eat
the newborn. A male engaged in sexual pursuit has been observed
to grasp a young dangling behind the female, pull it from her teat,
and pausing momentarily, nibble its head off, before continuing
to follow the female. Like the genitalia of the post-partum female,
the newborn young seem to have an odor that attracts and excites
the male.

To a lesser degree, adult females also display marked interest in
the newborn young of other individuals, which is liable to result
in cannibalism. The incidence of cannibalism is affected by the
condition, collectively, of the population of voles, and the availability
of nutritious food and moisture. In periods of summer
drought the grass becomes coarse and fibrous, and its protein
content declines. Under such conditions many voles appear to be
undernourished, and some are actually emaciated. Dehydration
may be an important factor at times when dew is unavailable for
drinking and the green vegetation remaining is exceptionally low in
moisture content. Voles caught at such times and brought to the
laboratory, drank avidly, and gained several grams soon after being
offered water or succulence. Cannibalism by adults on newborn
young in times of drought may be motivated by the acute
need for moisture and nutritious food. In times of drought the
birth rate is at low ebb.

Adult males have never been observed to display paternal solicitude
toward young, but some individuals, kept with females and
their litters, did not molest the young and were accepted by the
females as members of the family group.

[Pg 149]
Other things being equal, cannibalism involving the young might
be expected to be greater at times of high population density. Then,
young left in the nest by a female in the course of her foraging
would more often encounter adults and partly grown young, both
those that lived in the same burrow system and exploring intruders
from other areas.

The eyes open at an age of nine or ten days. Then the young
enter upon an exploratory period, when each wanders out of the
nest, emerges from the burrow, and wanders through the adjacent
surface runways in frequent short forays, sometimes following the
female and sometimes alone. Such forays usually cover only a
few inches at first, but as the young vole grows, becomes familiar
with its surroundings, and takes more plant food, its sphere of
activity gradually widens, and family ties are dissolved. Voles
reared to an age of three weeks in the laboratory and then released,
survived just as well if the female was not released with
them demonstrating that they were fully capable of shifting for
themselves at this age. In confinement, however, young voles of
greater age continued to suckle and remained closely associated
with the female. Females in confinement evinced much uneasiness
because of their inability to evade the young when the latter were
old enough to walk. The young then followed the female continually
and suckled whenever she stopped or even while she
moved about, unless she paused to remove them from her teats,
but they would not remain detached for more than a few seconds.
When a young followed the female away from the nest and then attached
to a teat, the female after pulling the young from her teat,
would usually carry it, grasped between her incisors, back to the
nest and deposit it there. On one occasion a young vole caught in
a live-trap was partly plucked and eventually killed by the female
on the outside trying to pull it through the wire mesh.

On several occasions, young were successfully transferred from
the mother to another lactating female in confinement, which accepted
them as part of her own litter. Young, up to the time of
weaning, appeared not to differentiate between the mother and
other adult voles. They would follow any larger individual indiscriminately,
and would huddle against it or nuzzle its undersurface
searching for a teat.

The following notes are based upon many different litters, and
give some idea of the sequence of events in their early development.

[Pg 150]
Newborn: The skin is pinkish gray dorsally and pink ventrally.
In profile, sparse and exceedingly fine hairs less than 1 mm. in length
are discernible. The vibrissae are approximately 2 mm. long. The
skin is thin and partly transparent, much wrinkled, with some
deeper folds, notably one between the knee and the heel. The
young lie on their sides making violent convulsive respiratory
movements. When not attached to the female's teats, they may
make faint squeaking sounds.

One day old: Little changed in appearance or behavior except
that the dorsal surface has become darker because of growth of
hair.

Two days old: Covering of fine brown hair readily discernible
on dorsal surface; lower incisors protruding about .5 mm. from the
gum; upper incisors have barely pierced the gum.

Four days old: Pale brown hair averaging about 1 mm. in length
over the dorsal surface gives the young a sleek, seallike appearance.
The young have gained greatly in muscular co-ordination.
Part of the time they may still lie on their sides, but they are able
also to gain an upright sprawling posture. In crawling, they are
unsteady and often topple over on their sides after taking a few
halting steps. They make frequent jerky lateral flexions of the
body, probably to search for a teat. Their eyes and ears still are
sealed shut.

Five days old: Young have changed but little in appearance
since the preceding day, but they have become notably more active,
with movements better co-ordinated. When placed on a level
surface they can crawl briskly.

Eight days old: Young are able to stand erect, with bodies held
clear of the ground, and they can even run, but the gait is slow
and clumsy, and the forequarters and hind quarters are poorly co-ordinated,
so that the voles tend to fall on their sides. The fur
averages approximately 3 mm. in length.

Nine days old: At this stage all young have their eyes open or
beginning to open.

Ten days old: All young of this age have their eyes open, but
not to their fullest extent, and the eyes are still slitlike in appearance.
The young have become rather gopherlike in appearance and gait.
They walk briskly but unsteadily, with bodies held high off the
ground. When handled, they struggle vigorously, and try to bite.
These young are similar in size and appearance to the smallest
voles caught in live-traps apart from their mothers.

Thirteen days old: Hair on back has grown to an average length
of 8 mm. (shorter on ventral surface, head, and limbs).

[Pg 151]
Seventeen days old: The young have become alert, and almost
as quick in their movements as adults. They have molariform teeth,
and are taking plant food. When a family group was examined,
the young instantly detached from the female's teats and scattered.
The hair on the back averages 10 mm. long and the vibrissae average
20 mm. long.

There is intense competition among the young of a litter, especially
if the litter has more than the average number of young. In
litters with more than four young, there is competition for the
inguinal teats, since, in most females at least, the pectoral teats
seem to have an inadequate milk supply. As a result, it is doubtful
whether more than four young to a litter are ever able to survive.
From the time their eyes open, the young compete actively.
When litters in confinement were fed with fresh greens, there was
nearly always quarrelsome squeaking and scuffling, as the young
competed for food. At such times, they have been seen to chase
and attack each other.

No individual vole was recaptured with sufficient regularity,
from birth to maturity, to provide a complete growth curve. The
curve in Fig. 7 is a composite based on all available records of
voles that were recorded as making growth in length and were recaptured
before they were fully grown, so that growth rates could
be computed. The figure shows that growth is extremely rapid
for the first three weeks, and thereafter slows gradually but steadily,
until in individuals of adult size, the increment per day is much
less than that in the small young.

Since rate of growth changes rapidly, with a slowing trend,
only those young voles that were recaptured within a few weeks
showed the approximate growth rate for any specific portion of
the ontogenetic curve. Table 5 summarizes the records of 98 such
young sorted into size groups representative of several stages in
development. The slowing trend of growth in voles that are nearing
subadult size is well shown by these records. Throughout
the greater part of the growth curve no difference could be found
in rate between the sexes. It is only after sexual maturity has
been attained and growth has become relatively slow that males
become noticeably larger than females. This tendency for continued
growth in the adult males results in a much more marked
disparity in size between the sexes in the oldest voles, as evident
in Fig. 2.

[Pg 152]

Fig. 2. Size distribution of prairie voles in a year-around sample, including
all the measurements of voles taken over a three-year period. Young are not
represented in their actual ratio to the total population in this sample, because
they are less attracted to the bait, and range less widely than adults. The
higher ratios of males than of females in the three largest size groups is well
shown, as is the higher ratio of females among those voles of small adult size.

[Pg 153]

Click on graph to view larger version.

Fig. 3. Changing numbers and composition (according to size of individual)
in a population of voles on an area of approximately one half an acre that
was intensively sampled with live-traps over periods of months. The population
as a whole and the ratio of young to adults tended to be higher in spring
and summer, but with little regularity from one year to the next. Weather was
far more important than season in determining the population trend. Many of
the voles recorded on the half-acre area ranged more or less beyond its
boundaries.

[Pg 154]

Fig. 4. Weight in free-living prairie voles in a year-around sample from juveniles
to large adults (grouped in length-classes of 6 mm. range, separate for
each sex). In each sample mean, standard error, standard deviation, and extremes
are shown. Note that mean weight is proportional to length, that in
each size class females average heavier (because of pregnancy in some) and
have a much wider range of variation in weight.

Martin (1956:389) stated that growth in young prairie voles
was, in general, most rapid in the period April-May-June and
least rapid in mid-winter. However, his data were based entirely
on weights. The high incidence of pregnancy in the larger young
females in spring and early summer may have caused the trend.
Measurements taken by me of lengths do not bear out the idea of
more rapid growth in the spring and summer, but, indeed, show the
opposite. In most instances, voles of comparable sizes made significantly
more rapid growth in the colder half of the year (mid-October
to mid-March) than in the warmer half. Dividing the
young voles in eight size groups and separating each group into
comparable summer and winter samples, I found more rapid average
growth in the summer sample in only two instances. These
[Pg 155]
deviations from the general trend probably resulted from inadequately
small sizes of some samples. On the average, the
growth rate in summer was 92 per cent of that in winter.

Fig. 5. Over-all length plotted against weight in young prairie voles, from
newborn to the minimum size at breeding maturity. The range of variation increases
as development proceeds, especially after the age of weaning is attained.

[Pg 156]

Greenwald (1956: 220) found that in females of Microtus californicus
some individuals are extremely precocious sexually, and
might, at an age of as little as two weeks, produce corpora lutea and
have sperm in the uterus. Greenwald mentioned one perforate
female which weighed only 10 grams, but most reached a weight
of at least 30 grams before their first pregnancies. The sterile
cycles passed through earlier seemed to represent a "tuning-up"
stage before establishment of the pituitary-gonad relationship.

Fig. 6. Weight plotted against age in young voles, from birth up to 25
days. The range is wide at the start and increases as development proceeds.

Although females of M. ochrogaster are much less precocious
in their manifestations of puberty, they may become perforate
[Pg 157]
well before impregnation can occur, and seem to pass through
sterile cycles before becoming pregnant. The 18 smallest females
recognized as being pregnant were of the following over-all lengths,
in mm.: 149, 149, 149, 148, 148, 148, 147, 146, 145, 145, 144, 144,
143, 143, 143, 142, 135, and 134. As pregnancy is ordinarily recognized
only in the last four days the females must have been impregnated
from 20 to 17 days earlier—when they were in most instances
7 to 11 weeks old and 135 to 145 mm. in length. The two smallest individuals,
recorded as pregnant at 135 and 134 mm., must, if they
were of typical size for their age, have become pregnant at an
age of approximately one month, when they were only 119 and
122 mm. in length. The smallest lactating females (some of them
pregnant also) were recorded at lengths of 149, 148, 148, 147, 147,
146, 144, 144, 143, 143, and 142 mm. Occasionally females of less
than 120 mm. were found to be perforate, and seemingly had begun
oestral cycles. Records of a female of definitely known age,
typical of many of the same size in her development, are cited
below:

Fig. 7. Growth curve in the prairie vole; dots are based on means of
series of definitely known age (born in captivity); circles are based on mean
lengths of recaptured marked young whose ages were not precisely known.

Fig. 8. Over-all length in young prairie voles of definitely known ages,
up to 40 days. All were born in captivity. Some were released with the
female and developed under natural conditions, but their growth rate did
not differ discernibly from that of those kept in the laboratory. Dots indicate
individual records; circles are means for ages at which four or more records were
obtained.

When captured on May 12, at an age of 54 days, this female
appeared to be within two or three days of parturition, and hence
[Pg 159]
must have become pregnant at an age of approximately 35 or 36
days. Pregnancy in the more precocious females probably occurs
at a length of approximately 130 mm. and an age of a little
less than 40 days. Such females are still growing so rapidly that
by the time their litters are born, they have grown to more than
140 mm.

Table 6 is a summarization of 73 records of individuals that made
substantial growth as adults, after they were marked and measured.
These records show the slowing trend of growth with advanced age.
Also, they show the wide range of individual variation in growth
rate, and difference between the sexes. With advanced age, growth
in females lags behind that in males to an increasing extent. Exceptionally
large individuals, of either sex, are many months old,
but some individuals live to be a year old or more without growing
much beyond average adult size. The average growth rate of
more than 1 mm. per day in young has slowed to less than .1 mm.
per day, on the average, in adults exceeding 160 mm., and has
slowed to less than .05 mm. per day, on the average, in those exceeding
165 mm.

[Pg 160]

The prairie vole is non-territorial and somewhat social. Several
or many individuals of both sexes and various sizes may use the
same system of surface runways and burrows and even the same
nest. In general, members of such a group are mutually tolerant.
A strange vole may provoke some hostility at first, but may soon
be accepted as a member of a new group. Consequently, there
are frequent shifts from one home base to another. Sexual relations
are probably more or less promiscuous, although a male and
female may rest and travel together in a semi-permanent association.
In confinement only those males having markedly enlarged
scrotal testes showed interest in females that were in oestrus.
Post-partum females especially were eagerly pursued by such males.
Anoestrus females are imperforate, and a vaginal orifice is present
only during an active oestral cycle or in pregnancy. The perforate
condition therefore, is a crude index of breeding activity in the
population. In adult females the ratio of those that were perforate
usually fluctuated between one-fourth and three-fourths
of the total. Only in severe summer drought did the numbers
decline below 24 per cent. Normally, breeding continues the
year around, but it is temporarily inhibited in unusually cold
weather or drought. The highest incidence of pregnancy normally
is in late spring and early summer. The ratio of juveniles in the
population from month to month and year to year is far more stable
than the actual population density.

Gestation is 21 days or a little less. The mean litter is 3.37 ± .075
young. Three is the most frequent number per litter, with four,
two, and five in that order of frequency. Larger and older females
have more young per litter, on the average. Average size is greater
in those litters having fewer young. At birth, young are between
40 and 50 mm. in length (typically, 47 mm.), and weigh 2.9 ± .05
grams.

At an age of nine days the young have their eyes open, and
they may be weaned at an age of approximately three weeks.
Young suckle chiefly from the four abdominal teats. The pectoral
mammae seem to be inadequately developed, with the result that
in exceptionally large litters of five, six or seven young, usually
no more than four survive. Until weaning the young spend much
of their time attached to the female's teats. She may even drag
them behind as she forages. Females that have suckling young
[Pg 161]
become much less tolerant of other voles. Attacks on young, and
cannibalism, are common. Adult males, especially, are liable to
eat the newborn young. The acquisition of cannibalistic habits
by individuals, and seasonal lack of adequately nutritious plant
foods may result in the killing off of young in such numbers that
the population level is held down.

In young females sterile oestral cycles often begin at about the
time of weaning. Earliest pregnancies occur when females are
approximately one month old, but most are several weeks older
before they become pregnant. Rate of growth declines steadily
from a length increment of approximately 2 mm. per day in voles
less than two weeks old to an increment of approximately one-fourth
mm. per day in subadults. Growth rate is highly variable
among individuals at all stages, and especially in those that have
attained adult size. Even adults tend to gain in length, slowly,
as well as in weight, and the largest individuals are all many months
old.

26-7561

[Pg i]

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