Res. Popul. Ecol. (1964) VI, 54--66

POPULATION DYNAMICS OF THE SMITH'S RED-BACKED

VOLE IN HIGHLANDS OF SHIKOKU

Ryo TANAKA

Zoological Laboratory, Kochi Women's University, Kochi

INTRODUCTION

The Smith's red-backed vole, Eothenornys smithi(TtIoMAs, 1905)% is very commonly

distributed in highlands of Shikoku among other districts of Japan except Hokkaido,

and the only vole in Shikoku is dominant in small-mammal communities over the

range. Thus upland afforestation is all the times subjected to damage by the pest,

and it is very important to elucidate its population dynamics from the view-point

of forest protection as well as population ecology.

A population fluctuation of the vole during the last decade beginning in the

outbreak year 1955 (TANAKA, 1956) has been disclosed on the basis of my data taken

from the same two plots set consecutively over the term on Mt. Turugi located in

the east of the highlands. On the other hand, since the fall of 1958, an abundance

of samples and data has been accumulated by Mr. ITo to devise a program of pest

control for forest protection. His samples and data, serving enough to know a

general population trend, either yearly or seasonal, throughout Shikoku, could be

partly made available to reinforce proofs for the present study through his courtesy;

a portion of his materials was utilized in the previous paper (TANAKA, 1962).

I am deeply grateful to Mr. Takeo ITO, Shikoku Branch of Government Forest

Experiment Station, and also to Mr. R. WATANABE, chief of the Station Branch, who

afforded every facility for my recent field surveys at Mt. Turugi.

ENVIRONMENTS AND METHODS

The environment on the Turugi plots in 1955 was already explained (TANAKA,

1956). Here we need to make a further note. The plots are located in the almost

natural-wooded area, 1500~1600m high, being a transition from the deciduous

latifoliate (temperate) to the coniferous (subalpine) forest zone. Soon after the drastic

destruction of habitat due to the widespread decay of dense cover of Sasa on one

The view of genus of the vole is still keenly opposed to between Japanese taxonomists; one insists on Eothenomys while another on Anteliomys, but Hoor~l~ & HART (1962) claim that both genera may well rank as subgenera of Clethrionomys. I am inclined to adopt the last until its world-wide, comprehensive research is completed, and yet for the present Eothenomys is used conventionally.

55

plot (A) in the outbreak year, the descendant plants generated, growing larger year

after year, and got back to the previous level of thriving in 1964 or so, while the

cover on another (B) kept invariable through the period.

ITo's specimens, however, were all taken from afforested areas, 700 to 1300m

high, equivalent to the lower half of the temperate forest zone.

On Turugi, the trapping was made for 4-6 days once a year in mid-summer(mid-

July to early August), but in 1957 and 1961 it was discontinued ; the trap-effective

area (the area covered by traps plus that of boundary strip computed from the

average size of home range, 0. 14 acres, of the vole) was 1-1.5 acres in the earlier

two years and about 2 acres at the other times. At each of the stations arranged

mostly in a 10 m or less grid on the plots, a single-catch live-trap was set f rom

1955 to 1960 (mark-and-release method), whereas three snap traps were laid out from

1962 to 1964 (removal method), for I became aware of intricate effect of multiple

collisions incidental to the former method (TANAKA, 1963). ITO'S samples were taken

only by the removal method from a lot of plots slightly smaller than 1 acre in trap-

effective area.

These plot sizes are as small as likely to cause overestimation, due to ingress

of animals from surroundings, in censusing, but it was in practice difficult to use

large enough plots in our study areas of complicated topography. To avoid the wrong

rating, therefore, special precaution was taken in analysis of data for the estimation

of population, in which the formula C~,~= (N-S~, 1) P was as a rule applied to trapping

records, so far as those were suitable to it (TANnKn, 1963). In most cases, aside

from Turugi data, it was applied to a set of pooled daily catches from more than

one plots of the same date in the same locality, and the population density per ha

is shown as an average of those obtained from various number of different localities

at the same season.

ITo's specimens were all re-examined in respect to female breeding features and

his measurements of body weight were revised into true values after the same

criterion as described in the preceding paper (TANAKA, 1962). Adrenal weights of

his specimens were measured in our laboratory.

The level of population fertility was discussed by the use of adult females alone,

for as a whole males ran parallel with females in breeding activity. The female

activity was measured by pregnancy rate (PrR), active reproductivity rate (ARR),

litter size and incidence of pregnancy (I1). ARR is ratio of adult females in any

stage of operating oestrous cycle; to say concretely, the active adults consist of

those having placental scars (parous) or swelled uteri ready to contract (post partum),

or in visible pregnancy, or holding well developed ovaries and uteri indicating near

oestrus (nulli-parous).

The level of adrenal weight in populations was expressed by an average of

relative adrenal weight (RAW) of subadult and adult males, i.e., paired adrenal weight

in mg per unit of the gross body weight in g (BW). Further, it was corrected to be

56

ad jus t ed to m e a n B W of each s amp le by the s ame r eg re s s ion coefficient as g iven in

1962.

T h e convenien t , bu t bas i ca l ly just i f iable , d e t e r m i n a t i o n of subadu l t s and adu l t s

fo l lowed the r a n g e s of B W ( s u b a d u l t 16 g o r more , a d u l t 19 g o r m o r e ) c o m m o n to

bo th sexes in l ikewise w i th before .

ANNUAL CHANGES IN TURUGI

T h e s m a l l - m a m m a l c o m m u n i t y in the s t u d y a r e a is c o m p o s e d of the vole, two

species of Apodemus (argenteus, speciosus) and three species of insec t ivores (Urotrichus talpoides, Dymecodon pilirostris, Sorex shinto). The long- t a i l ed mice (A. argenteus) r a n k s nex t to the vole in abundance , the o the r m e m b e r s be ing f a r less. CALIaOUN

(1959) is a p p r e h e n s i v e of an i n h i b i t o r y effect which d o m i n a n t species m a y in some

w a y exh ib i t upon some second and thus s u b o r d i n a t e species fo r e a r l i e r d a y s wi th in

a s n a p - t r a p p i n g per iod. T h e influence was t hough t den iab le in our field works , some

p roof s be ing shown in T a b l e 1. T h e z2- tes t p roves tha t the d e p a r t u r e of expec ted

f r o m o b s e r v e d n u m b e r s is qui te ins igni f icant . W e m a y say , thus, t ha t the r e l a t ive

a b u n d a n c e of these c o m p o n e n t s in the c o m m u n i t y was well ref lected in the r e l a t ive

ca tches t h r o u g h the t r a p p i n g pe r iod ( 4 ~ 5 d a y s ) .

Table 1. Es:Eothenomys smithi, Aa : Apodemus argenteus Daily catches in Turugi, the very rare mouse, A. speciosus, being omitted.

I 1964 CA) 1962 (Plots A, B) 1963 (A, B)

Days I, II III IV V Total I II III IV ! Total i I II III IV I Total i

24 13 7 3 7 3

E s

As Insectivores

16 7 6 10 39 13 5 1 2 21 6 4 4 1 15

Total 35 16 11 13 75 38

0.10~P~0.20

9 6 52 20 5 2 4 31 3 1 14 4 2 3 2 ~ 11 3 4 17 3 1 2 2 8

. . . . . . . . . I . . . . .

19 15 11 83 ~27 8 7 8 50

0.50~P~0.80 0.50~P~0.80

In the s t u d y area , a p a t t e r n of s ea sona l popu la t i on change of the vole has no t

been exp lored . I t is, however , supposed t ha t the peak wil l u s u a l l y come in la te

s u m m e r o r e a r l y fall , because no d rop of b r e e d i n g r a t e was rea l ized in m i d - s u m m e r

as seen f r o m the A R R - v a l u e s (0 .50~0 . 60, T a b l e 2) in the y e a r s 1959~64, w he re a s

ITo 's s a m p l e s r evea led v e r y low va lues a t the c o r r e s p o n d i n g season. T h e p r o b l e m

wil l be d i scussed a g a i n l a t e r on.

Here is a d d e d a n o t h e r proof . In e a r l y O c tobe r when the census was execu ted

in 1955, the p o p u l a t i o n s were dec l in ing a f t e r the supposed peak in mid- o r la te s u m m e r

(TANAKA, 1956), and the i r b r e e d i n g had u t t e r l y ceased by then (ARR, 0 or 0.02).

T h e p h e n o m e n a m a y in p a r t be t r a c e d back to the s ea sona l t r e n d of a b u n d a n c e in

t4sual yea r s , bu t the p recoc ious peak in the m i d - s t l m m e r and the dep re s sed b reed ing

Table 2. Populat ion densi ty per ha (PD) on the two plots (A, B) in Turugi for two species (Es, Aa), and p regnancy ra te (PrR) , act ive reproduct iv i ty ra te (ARR) and relat ive adrenal weight (RAW) for the vole. n = n u m b e r of specimens examined, B = b e g i n n i n g , M=midd le , E = e n d

57

1955 Oct. B

A Es 170 0 - - 15 33 43 - - 28

plot Aa . . . . . . . . . . . . . . . PD _ 1 5 30 - 3 1 1 - ,5

175 10 - - 25 98 88 - - 28

plot l Aa 5 5 - - 15 13 23 - - 20 I

f n 41 PrR

n ARR

I

n RAW

3 or 0. 02

41

D.02 ~ .08

'56 '57 '58 '59 '60 '62 '63 '64 July M Aug. B July E July E '61 July E July E July E

50 48

18 30

38

8

- - 1 19 18 - - 17 21 15

- - - - 0.05• 0.28i.10 - - 0.12A=.10 0.19• 0.13=~.11

- - 1 19 18 - - 17 21 15

- - - - 0.47:~.11 0.61~.12 - - 0.59• 0.52=k_.11 0.60=~.13

- - - - 17 27 - - 14 26 13

- - - - 0 . 4 7 0 . 2 8 - - 0 . 3 5 0 . 2 3 0 . 28

Fig. 1.

200

150

I00

50

X ARR •

xo

�9 .

�9 ~ A W ,

1 I I I 1 I I I I

1955 '56 '57 '58 '59 '60 '61 '62 '63 '64

0.60

0.40

0. 20

0

Yearly changes in densi ty of the Turug i populations, a t tended by shifts in b reed ing aci t ivi ty and adrenal weight of the vole; re fer to Tables 1 and 2 about abbrevia t ions . (plot A : Q, plot B : /~, Es: - - , Aa - - ) .

i n t h e e a r l y f a l l m a y l a r g e l y be r e d u c e d to r a p i d p r o p a g a t i o n a n d i n t e n s i f i e d s o c i a l

s t r e s s l i k e l y to o c c u r a t o u t b r e a k (CHRISTIAN, 1957). T o m y r e g r e t , a t t h a t t i m e

a n y a d r e n a l a n a l y s i s w a s n o t c a r r i e d o u t of t h e m . N e x t y e a r t h e r e t o o k p l a c e a

s t r i k i n g d e c r e a s e of n u m b e r s (F ig . 1) e n o u g h to s u g g e s t ' p o p u l a t i o n c r a s h ' , w e l l

e x p l i c a b l e b y CHmSTIAN'S t h e o r y (TANAKA, 1960).

T h u s t h e m i d - s u m m e r d e n s i t y i n n o n - o u t b r e a k i n g y e a r s m a y we l l b e s u p p o s e d

as t h e m e d i u m o r n e a r t h e m a x i m u m in t h e s e a s o n a l t r e n d .

T h e p o p u l a t i o n f l u c t u a t i o n s of t h e vo l e a n d t h e l o n g - t a i l e d m o u s e a r e d r a w n i n

F ig . 1. T h e r e a r e t w o m i s s i n g l i n k s in 1957 a n d 1961 f o r t he c h a i n of d a t a , b u t

t h e y a r e u n i m p o r t a n t b e c a u s e t h e f o r m e r w a s p e r h a p s a c o n t i n u a t i o n of t h e s c a r c e t y

p h a s e ( C m T T y & CmTTY, 1961) d u e to t h e c r a s h a n d t he l a t t e r is s u p p o s e d to h a v e

58

been the same low density as in 1962 judging from ITo's data.

The second and third milder peaks of the vole in numbers appeared in 1959~60

and 1963~64, the cyclic interval 3-4 years being that widely known about microtine

rodents. The population trends on both plots ran almost in phase, and furthermore

ITo's samples evidenced that the overall density level throughout Shikoku uplands

showed roughly the same trend as this since 1959 onwards at least. The 1955-outbreak

also seems to have been so much widespread, but little was known about its precise

range.

We can see, therefore, that the vole populations in every locality of Shikoku

tend to have a cyclic trend keeping pace with one another. It seems to make a sharp

contrast to the adjacent vole populations at Lake Vyrnwy which ran mostly out of

phase or in opposite phase (CHITTY & CHITTY, 1962).

Nevertheless, two or three times as many voles were found on one plot (B) as

on another (A) at the second peak time when the Sasa-thicket had been poorly

recovered on A. Thus the difference in density should mainly be assigned to that

in habitat, for the A density was not inferior to the B's in 1963 when both cover

conditions were almost alike.

In contrast with the vole, the subordinate mouse on both plots expressed far

minor fluctuation in numbers, with indistinct cyclic phases generally indifferent to

the vole's or opposite to each other.

Although a second outbreak has not come into being, the violent change in

abundance of the vole will assure that it has a great population potential based on

its prolific feature. During the study period, no appreciable environmental changes,

other than the plentiful supply of Sasa.seeds and the attendant events in partial

areas about 1955 and the unusually low temperature in January of 1963, have been

encountered throughout the district. Already I argued that the food supply was not

the ultimate motive of the outbreak in 1955 (TANAKA, 1957). In view of the observed

values of ARR and PD in the winter of the year III (Table 3, Figs. 2 and 3), it is

unlikely that the severe weather had some influence on the vole populations. The

heavy haunting of predators in 1955 (TANAKA, 1956) was only a temporary event

incidental to the overpopulation. Hence we are led to postulate that the depressed

number of the vole in 1956~58 as well as in 1961~62 hardly derived from either

predator pressure or adverse weather. Thus, this kind of cyclic population-trend is

readily accounted for by the theory (TANAKA, 1960) that a cyclic oscillation in

numbers at regular intervals of 3 or 4 years, apt to be started in a collapse at

outbreak, is attributable to the intrinsic mechanism of a vole-population provided

with some prolific potential. The theory is never of imaginary but of practical content.

SEASONAL CHANGES

Seasonal changes in population and breeding could be in some degree brought

59

to l i gh t w i t h ITo ' s v o l e - p o p u l a t i o n s . T h e t h r e e - y e a r d a t a w e r e e x a m i n e d by a r r a n g i n g

t h e m by the b i o l o g i c a l yea r , t he d u r a t i o n f r o m A p r i l to the n e x t M a r c h ; t he y e a r s

1959~60, 1961~62 a n d 1962~63 a r e he re f o r s i m p l i c i t y d e s i g n a t e d as I, I I and I I I

r e s p e c t i v e l y ( T a b l e 3, F igs . 2 a n d 3).

Table 3. Seasonal mean values of the vole in the lower temperate zone for density (PD), breeding (PrR, ARR, I~), body weight ( B W ) a n d adrenal weight (RAW) in three years. I~=incidence of pregnancy. Refer to the foregoing

-- ~ - - -

Years ~ Months

1959 i Apr.} !May i 19

July ] !1 11 Aug. I

I Oct . ) i Nov. J 41

Dec. 79

19601 Jan. 10

Average

1961 i June

A u g .

O c t .

[Nov.

19621 Feb.

tables about other abbreviations.

PrR ARR

n : n

0. 58-k. 10

0• 13

!0. 22• 07

O. 19• 05

0• 13

O. 219• 033

32 O. 09• 07

9 ! o•

50 ~0. 20• 02 i [ 49 0 . 5 3 •

19 i0.26• 10

3 0. 33• 24

19 0.68 !:. 11

11 0.09~. 15

38 0.74•

79 0.52L.06

10 0.40 •

O. 554• 039

32 O. 38• 09 53

9 0 L . 1 4 25

50 0.62• 02 51

49 O. 88• 02 57

19 0.84• 28

3 0.67• 28J Mar.

Average 0. 278• 033 0. 642=0. 039 - - - T . . . . . . . T . . . . . . . . .

1962 May ~ 47

June 20

Aug, 4

Sept. I

i Oct. 15 i Nov. 41 i

!Dec. ! 36

19631 Feb. 18

Average

0. 43• 06 47 0.68•

0~ .09 20 0.25!:.11

0 ~.21 4 0 L.25

10. 33• 15 0.87:= 13/ 0.24• 41 0.51-{:.08

0.08L.07 36 0.64~:.08

0 .11• 18 0.44 !:.12

0.220• 0.565 J:0.037 i

BW (g) R A w PD I [ n n

8 19.9 8 0.52 174

19 25.5 19 0.26 55

28 29.3 28 O. 27 87 8.5

67 25. 8 67 O. 24 78

15 23.9 15 0.25 39

25.6 !:0.39 0 .27t0 .012

23.9 53 0.43 30

23.7 25 0.23 11

26.1 51 0.20 - - 9.3 29.4 57 0.18 28

24 24.1 28 0.24

25. 9 0. 26

44 26.0 44 0.43 27

22 26.4 22 0.50 21

12 25.2 12 0.21 7

21 28.0 21 0.20 8.4 46

48 29.0 48 0.18 16

41 29.0 41 0.20 40

21 27.9 21 0.15 39

27.6 0.27

B e f o r e g o i n g f u r t h e r , the i n c i d e n c e of p r e g n a n c y is e x p l a i n e d . I t w a s w o r k e d

o u t a f t e r t h e f o r m u l a , Ii=pT/t.,r, of fe red f o r t he b r o w n r a t by CALrlOUN (1962),

w h e r e p w a s e x p r e s s e d by a n n u a l m e a n s of P rR , bu t t hose of A R R w e r e s u b s t i t u t e d

f o r r b e i n g def ined by h i m as r a t i o of adu l t f e m a l e s v i s i b l y pa rous , f o r I t h o u g h t

i t r a t h e r s u i t a b l e to do so. T h e d u r a t i o n of v i s ib l e p r e g n a n c y t~ w a s e s t i m a t e d a t

15 o r 16 d a y s f o r o t h e r vo les (KALELA, 1957; HOFFMA.NN, 1958), but , i n s t ead , t.~=17

a n d T = 3 6 5 w e r e u s e d as w a s done w i t h the ra t , s ince the g e s t a t i o n p e r i o d of vo l e s

a n d r a t s is c o n s i d e r e d a l ike .

60

As seen f rom Fig. 2, in consonance wi th the year ly t r ends in Tu r ug i , the vole

popula t ion is twice or more as high in the year I as in II and III f rom May to

December. The very high densi ty in May of I was a s ingle value, except ional ly

ob ta ined f rom only a plot, ins tead of an average f rom mul t ip le plots in others.

Thus , it would fail to represen t an average dens i ty level in the month. Accord ing

to the genera l knowledge of seasorial t r ends for vole popula t ions in t empera te

cl imates, a much lower density, possibly 50 or so, should have been given.

200

150

100

56

A Fig. 2.

I

RAW 3o

-0.10

M J J A S O N D J F M Seasonal trends in population (PD) and adrenal weight (RAW) of the vole in the lower temperate zone in three years. (--@-- : 1959~'60, ... x... : '61~ '62, - - ~ - - : '62~'63

If we view, keeping in mind this assumpt ion , the three-year seasonal f luctuat ions

in dens i ty f rom a low in spr ing to a high in fall, they are reducible to the n o r t h e r n

pa t t e rn (STmKEL & WARBACH, 1960). The peak was reached in October and near ly

m a i n t a i n e d to December.

The breeding t rends (Fig. 3) are co inc ident wi th those of Peromyscus s tudied

Fig. 3.

o.=o -----?1

0. 207 ~ ~//~/~/~/~/~/~/~/~Y~' "~Y-'~l_

80 r

O. 50 . . . . . " - - ~ t ~ - -

A M J J A S O N D J F M Seasonal breeding trends of the vole in the lower temperate zone in three years, each ratio being attended by upper and lower ranges of its standard error.

61

by Bm~T (194-0) in that the breeding level reached the first peak in late spring and

then declined sharply in July-August but dissimilar in that a second peak appeared

in October-November rather than in September-October. Then the peak-like populaton

must have been kept as lares as Decemper with our voles. Another dispari ty is that

the fecundity was kept relatively high, instead of the complete fall in Peromyscus, through winter, the winter level being rather higher than that of mid-summer.

But, to our general knowledge, the observed values for fecundity in mid-summer

seem to have been too small for the temperate vole. Be that as it may, these values

obtained in July-August f rom Turugi samples were compared with those f rom ITo's

samples, just discussed, as follows:

ITo's Turug i Diff . /SE P

PrR 0/24-=0 14/91 =0.154 1.60 )>0.05

ARR 1/24=0. 042 51/91-0. 560 4. 58 < 0 . 0 i

Although a significant difference can be found only in ARR, both values in Turugi

are large enough to teli that the breedgin may begin in spring and continue in mid-

summer. Thence we may infer, as referred to foregoingly, that the peak comes in

late summer or ear ly fall in ordinary years. Supposing it is true, the seasonal cycle

in Turugi may be at tr ibuted to the typical northern pat tern such as found with

Peromyscus in New Brunswick (MorRis, 1955). A more northern type having a

breeding peak in June has been discovered with the same vole on the subalpine

forest zone, 1900~2400 m high, in Honshu (MIYAO et al., 1964).

I shall speak of visible pregnancy rate (PrR) commonly available as a measure

of reproductivity. In the above comparison, the difference in PrR failed to reach a

significant level. The fact can be a proof that PrR is not pert inent to the measure.

Considerable discrepancy and non-parallelism between the trends of PrR and ARR

is expressed also in Fig. 3. A presumable reason is that PrR is liable to decline by

dint of a density-controlling factor, copulation pressure; it is demonstrated with

exper imental populations that the factor may be operative even in those of high

fecundity in terms of the rate of ovum production (SouT~WTCK, 1955).

PROBLEM OF SOCIAL STRESS

According to the theory of CHRISTIAN', adrenal increase is a reflection of stress

induced by increasing density and some environmental fac tors mediated through

the single pa thway of social interaction. Nevertheless, with our materials sampled

f rom usual-year populations, adrenal analysis failed to afford any affirmative evidence

for the theory.

In the study (1962), I have clarified that relative adrenal weights may augment

in females while decrease in males with rise of fecundity as well as with progress

of age, the rate of change being much greater in voles than in rats. Thus it has

62

turned out nearly meaningless if one comments on the theory from a result of his

work, done in utter disregard or ignorance of these sources of error, about voles

at least. My method seems to have been enough appropriate in this respect.

As for Turugi data (Fig. 1), the overall levels of ARR and RAW are kept almost

constant inspire of the apparent change of PD over the period 1960~64, nevertheless

in one (1959) of peak years ARW lies above but ARR below the respective levels.

Only what happened to RAW in 1959 looks to accord with the theory, but it might

have derived from the fact that RAW in males changes inversely with fecundity

independently of social stress.

As for I ro ' s data (Table 3, Fig. 2), no difference in average of RAW through

the seasons concerned was found between the year I of high density and the years

II and III of low. The slight tendency for the peak-year values in fall and winter

to surpass the corresponding ones in II and III is likely to be due to the general

decline of fecundity in I.

It is worth noting that RAW in May and June was decidedly larger than in other

months through the three years. A maximum in seasonal trend of adrenal weight

was found in June also for the vole at Lake Vyrnwy (CHITTY, 1961). As is the case

with this, the above discussion of our vole naturally leads to consider that the adrenal

peak in May and June should be unrelated to breeding and, needless to say, to PD.

Then would it be related to stress due to some social derangement peculiar to the

months? Altogether the discrepancy between ARR and PrR was much smaller in

spring than in fall and winter. If we presume the discrepancy to be induced mainly

by copulation pressure which is in turn likely to derive from social derangement,

the social stress should have been decreased to a minimum, whereas in practice the

adrenal level was highest, in spring. The greatest discrepancy ratio (PrR/ARR)

was shown in October-November, when the seasonal trend of PD was at peak, in

the year I of high density, but no corresponding peak value of RAW was manifested.

Therefore, apart from what is expressed in terms of stress, the presumption of

intensified copulation pressure will be valid for the months.

REPRODUCTIVITY REGULATED BY POPULATION DENSITY

For the vole populations in the three years, above treated, it has proved that

some breeding items are on the overall average inversely related to the density level

of the year. Meanwhile no extrinsic agents are considered to have been effectively

at work, so the phenomenon can be regarded as the self-regulation of fecundity by

density within a population. Up to date, not a few examples for this have been

known of natural populations in small mammals. But the kinds of breeding items

concerned in the phenomenon seem to be fairly divergent from case to case even

with microtine rodents. For instance, HOFFMANN (1958) recognized, in two species

of Microtus, a generally inverse relation to density about ovulation rate, litter size

63

and p r e g n a n c y r a t e bu t denied i t abou t age of m a t u r i t y and inc idence of p o s t - p a r t u m

p r e g n a n c y , and bes ides he d isc losed t ha t the l e n g t h of b r e e d i n g season was i nva r i a b l e

f r o m y e a r to y e a r fo r one vole (montanus) at least . T h e n he c l a imed that, s ince

the obse rved v a r i a t i o n in n a t a l i t y was r e l a t i ve ly minor , the i m m e d i a t e cause of

popu l a t i on cycles in these spec ies m u s t lie wi th in o ther half of the n a t a l i t y - m o r t a l i t y

equa t ion . In con t r a s t , the inverse dens i t y -de pe nde nc e wi th a vole of Clethrionomys (KALELA, 1957) was revea led c l ea r ly in ra te of m a t u r a t i o n of f i r s t -yea r y o u n g s and

length of b r eed ing season, hence inc idence of p r e g n a n c y , bu t s ca rce ly in p r e g n a n c y

r a t e and l i t t e r size.

In the p r e s e n t work , as to the overa l l m e a n s of P rR and A R R t h r o u g h the y e a r

( T a b l e 3), no s ign i f ican t difference was obse rved be tween the y e a r I of h igh de ns i t y

and the y e a r s II and III of low, bu t m a x i m u m s were seen in II. A n d ye t the mean

of A R R of II coun ted f r o m the fa l l and w i n t e r d a t a was l a r g e r enough to be s ign i f ican t

t han the c o r r e s p o n d i n g one of I. A c c o r d i n g l y the inc idence of p r e g n a n c y (I1),

d e p e n d e n t on these values , w o r k e d out to be g r e a t e r in II t han in I. T h e r e was on ly

l i t t le difference be tween I and III abou t these values .

Table 4. Frequency of viable litter size, counted from ITO'S samples combined with Turugi samples, in three years.

Litter size . . . . . . . . . . . . . . . . . . . . 1 2 3 4 5 : Total Mean (5?~fiducial limits)

Years ._ ! : i J i

I (1959~'60) i 6 16 12 1 0 35 2. 23-:. 13 (1.97~2. 49) 1[ (1961~'62) ] 3 19 15 6 1 44 2. 61:5.13 (2. 35~2. 87)

(1962~'63) 1 14 21 3 2 41 2. 78:1=. 13 (2. 52--3.04)

Fig . 3 sugges t s t ha t the b r e e d i n g season in the lower t e m p e r a t e zone m a y las t

a l m o s t al l the year , f o r A R R kep t i ts h igh va lue 0 .62-0 .88 f r o m Oc tobe r to M a r c h

in the y e a r II. F r o m these da ta , we would be unable to pos tu l a t e tha t the b reed ing

season was l onge r in the low-dens i ty y e a r s t han in the p e a k year , because the va lue

of A R R w a s st i l l as much as 0.40 in J a n u a r y , none of those in the subsequen t m o n t h s

be ing ava i l ab le to us.

A more m a r k e d v a r i a t i o n of dens i t y - r egu la t i on , however , a p p e a r e d in l i t t e r size

( T a b l e 4). T h e annua l mean of the v iab le l i t t e r size, n e a r l y iden t i ca l w i th the g r o s s

size inc lud ing n u m b e r of qui te few r e s o r b i n g e m b r y o s , was a p p r e c i a b l y sma l l e r in

the peak y e a r than in the low-dens i ty years , but a s ign i f ican t difference was obse rved

on ly abou t the y e a r III.

PROBLEM OF PROLIFIC POTENTIAL

I r r e spec t ive of the pro l i f ic po t en t i a l in the vole popu l a t i on supposed f r o m the

v io len t annua l t rend, the mean l i t t e r size as smal l as 2 .23-2 .78 in the g r o s s and 2. 00

a t t e r m was obse rved c o n t r a r y to our expec ta t ion . MIYAO et al. a lso ob ta ined 2. 3

64

from the same vole. Those known from many microtine rodents appear to be in

the order of 5-6. To make full compensation for the few embryos, a high rate of

litter production and survival in pre- and post-natal development can be expected.

In this paper, however, I could not touch upon any of what was related to the

postnatal survival or mortali ty rate.

The incidence of pregnancy counted by means of CALHOUN'S formula was 8. 4-9.3

on the assumption of the breeding season lasting a year. The corresponding values

by HOFFMANN were 9. 3-11.2 for californicus and 6. 7-7.4 for montanus, but his count

was based on the equation of EMLEN ~ DAVIS (1948) which is slightly different from

CALHOUN'S in lack of r so as to cause some underestimate. Despite the fact, the

value of californicws was larger, but that of montanus smaller, than our vole's.

From the breeding data of his vole presented by KALELA, I could calculate times

of litter production per year at about 4 5; the value was smaller than those, above

given, probably on account of a shorter breeding season in the subarctic vole, but

it is not comparable precisely to the L-value.

The intra-uterine mortali ty was estimated by the same means as in KALELA, i.e., the developmental stage of embryos during visible pregnancy was discriminated

by length of uterine swellings and the sample was grouped into three categories of

earlier, middle and later stages. The mean litter size for each stage was as follows:

earlier 2. 5020. 09, middle 2.66~0.13, later (at term) 2. 0020.18

There was a significant difference between the second and the third, then the intra-

uterine mortali ty during visible pregnancy working out at 0. 25 (0.66 loss per litter).

KALI~LA thought nothing of the role of this mortali ty in population dynanmics from

his result of his vole showing so small a difference in mean litter size among those.

HOFFMANN assessed the overall prenatal mortality of montanus at 0. 02-0.25 and the

post-implantation prenatal mortality of caIifornicus at 0-0. 11.

Consequently, I have been able to detect no affirmative evidence that our vole

is ahead of other voles either in incidence of pregnancy or in prenatal survival rate.

Further researches on the postnatal mortality of our vole are required to solve this

problem.

SUMMARY AND CONCLUSION

Population dynamics of the SMITH'S red-backed vole predominantly common

through uplands of Shikoku have been in some degree disclosed by the use of my

own and Government Forest Station's samples collected since 1955 onward.

It has proved that the upper-range population reaches its density peak possibly

in late summer or early fall, but the lower-range one does probably in October-

November, as the seasonal trend in usual years. The upper one produced a peak

three times at 3-4 year intervals, the first peak being an outbreak followed by a

crash, during the last decade. It seems likely that all the populations through the

65

range have, in the gross, f luctuated in phase af ter 1959 at least. The cyclic f luctuat ion

m a y readi ly be expla ined by the theory of in t r ins ic mechanism, because no ex te rna l

fac tors are considered to have exer ted a conclusive effect.

Except what was concerned in the outbreak, the role of the social s tress could

be set a t naught .

The regu la t ion of fecundiy by densi ty was expressed more marked ly in l i t ter

size and less in active reproduc t iv i ty rate and incidence of p regnancy .

The mean l i t ter size at te rm as small as 2.00 is c o n t r a r y to our expecta t ion in

view of the supposed prolific potent ia l , never the less the observed f requency of l i t ter

poduct ion and in t r a -u te r ine surv iva l ra te has proved not to be so high as to make

up for the small l i t ter size. The p rob lem in the pos tna ta l mor ta l i t y has r ema ined to

be solved.

LITERATURE

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Michigan. Mis. Pub. Mus. Zool. Univ. Mich., 40: 1~58.

CALHOUn, J.B. (1959) Revised sampling procedure for the North American census of small mammals,

Popul. Dynam. Vert., EeL 10: 1~12.

CALI~OIIN, J.B. (1962) The ecology and sociology of the Norway rat. Bethesda.

Cmrrr, D. & H. CUlTT~: (1962) Population trends among the voles at Lake Vyrnwy, 1932~60.

Symposium theriologicum, Brno, 1960: 67~76.

CmTwr, H. (i961)Variations in the weight of the adrenal glands of the field vole, Microtus

agrestis. J. Endocrin., 22: 387~393.

C~glSrIAN, J.J. (1957) A review of the endocrine responses in rats and mice to population size

including delayed effects on offspring. Nay. Med. Res. Inst., Lect. & Rev., SeT. 57-2 : 443~

462.

EZCLEN, J.T. & D.E. DAVIS (1948) Determination of reproductive rates in rat populations by

examining of carcasses. Physiol. ZooL, 21: 59~65.

HOFFMANN, R.S. (1958) The role of reproduction and mortality in population fluctuations of voles

(Microtus). Ecol. Monogr., 28: 79~109.

HooPEl~, E.T. & B.S. HART (1962) A synopsis of recent North American microtine rodents.

Mis. Pub. lY[us. ZooL Univ. Mic[z., 120: I~68.

KALEZA, O. (1957) Regulation of reproduction rate in subarctic populations of the vole Clethrionomys

rufocanus. Ann. Acad. Sci. Fennicae, A, 4: 1~60.

Mi~AO, T., T. Mo~oztr_~i & H. HA~A~WRA (1964)Small mammals on Mt. Yatsugatake in Honshu

IIL Smith's red-backed vole in the subalpine forest zone. Zool. Mag. Japan. 73: 189~195.

MORRIS, R.F. (1955)Population studies on some small forest mammals in eastern Canada.

J. Mature., 36 : 21-35. SOVT~W~eK, C.H. (1955) The population dynamics of confined house mice supplied with unlimited

food. Ecology, 36: 212~225. STICKE~, L.F. & O. WAa~.BACI~ (1960) Small-mammal populations of a Maryland woodlot, 1949~54.

Ecology, 41: 269~286. TANAKa, R. (1956) Fluctuations in vole-populations following the wide spread synchronous flowering

66

of bamboo-grasses on Mt. Turugi. Bull. Kochi Worn. Coll., 4 : 61~68.

TaNAKa, R. (1957) An ecological review of small-mammal outbreaks with special reference to

their association with the flowering of bamboo-grasses. Bull. Kochi Worn. Univ, Ser. Nat.

Sci., 5 : 20~30.

TaNAICA, R. (1980) Some ~eatures in population dynamics of simultaneous vole-outbreaks over

the wide range of Japan in 1959. Bull. Kochi Wom. Univ., Ser. Nat. Sci., 8 : 11~17.

TANAKA, R. (1962) Adrenal analysis for critique of the social s tress theory in natural populations

of a montane vole. Res. Popul. Ecol., 4 : 8~16.

TANAKA, R. (1963) Examination of the routine census equation by considering multiple collisions

with a single-catch t rap in small mammals. Jap. J. Ecol., la : 16~2t.

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