Aspects of Reproduction and Development in the Prairie Vole Part 2

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 s.h.i.+fting for themselves at this age.

In confinement, however, young voles of greater age continued to suckle and remained closely a.s.sociated 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.

EARLY DEVELOPMENT OF YOUNG

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

Newborn: The skin is pinkish gray dorsally and pink ventrally. In profile, spa.r.s.e 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).

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 compet.i.tion 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 compet.i.tion 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.

GROWTH FROM WEANING TO MATURITY

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 s.e.xes.

It is only after s.e.xual 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 s.e.xes in the oldest voles, as evident in Fig. 2.

[Ill.u.s.tration: 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.]

Table 5. Average Growth (in Over-all Length) in Young Voles of Several Sizes. ([M] = Male; [F] = Female)

==================+==============+===========+=========================== Average lengths Average Average in mm. at length, increment Total, and beginning and in days, per day number of each end of growth of growth in mm. s.e.x in sample period periods ------------------+--------------+-----------+--------------------------- 97.0 to 126.6 in 16.8 1.76 5 (1 [M], 4 [F] [F]) 103.3 to 127.3 in 14.9 1.61 9 (3 [M] [M], 6 [F] [F]) 107.5 to 123.4 in 11.0 1.44 8 (5 [M] [M], 3 [F] [F]) 114.0 to 132.3 in 17.5 1.05 6 (5 [M] [M], 1 [F]) 118.5 to 136.0 in 19.7 .88 6 (3 [M] [M], 3 [F] [F]) 122.1 to 135.8 in 16.2 .85 15 (5 [M] [M], 10 [F] [F]) 129.3 to 145.5 in 22.8 .71 4 (all [M] [M]) 130.6 to 146.1 in 19.8 .78 12 (all [F] [F]) 139.8 to 147.5 in 29.5 .26 10 (all [M] [M]) 141.2 to 148.8 in 26.2 .29 23 (all [F] [F]) ------------------+--------------+-----------+---------------------------

[Ill.u.s.tration: 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.]

[Ill.u.s.tration: FIG. 4. Weight in free-living prairie voles in a year-around sample from juveniles to large adults (grouped in length-cla.s.ses of 6 mm. range, separate for each s.e.x). In each sample mean, standard error, standard deviation, and extremes are shown. Note that mean weight is proportional to length, that in each size cla.s.s 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 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.

[Ill.u.s.tration: 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.]

SIZE AND AGE AT s.e.xUAL MATURITY

Greenwald (1956: 220) found that in females of _Microtus californicus_ some individuals are extremely precocious s.e.xually, 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 pa.s.sed through earlier seemed to represent a "tuning-up" stage before establishment of the pituitary-gonad relations.h.i.+p.

[Ill.u.s.tration: 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 p.u.b.erty, they may become perforate well before impregnation can occur, and seem to pa.s.s 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:

March 19, 1956 Born in captivity.

April 7, 1956 (19 days old) Released on study area at site of mother's capture; length 102 mm., weight 11.1 gms.

April 15, 1956 (27 days old) Recaptured; perforate with a copulatory plug; length 113 mm., weight 13.4 gms.

April 27, 1956 (39 days old) Recaptured; imperforate; length 131 mm., weight 24.3 gms.

May 12, 1956 (54 days old) Recaptured; perforate and in late pregnancy; length 146 mm.

May 25, 1956 (67 days old) Recaptured; imperforate, in an advanced state of lactation; length 150 mm., weight 33 gms.

[Ill.u.s.tration: 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.]

[Ill.u.s.tration: 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 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.