Winter Breeding in Woodland Mice, Apodemus Sylvaticus, and Voles, Clethrionomys Glareolus and...

Winter Breeding in Woodland Mice, Apodemus Sylvaticus, and Voles, Clethrionomys Glareolusand Microtus Agrestis, Near OxfordAuthor(s): Michael SmythSource: Journal of Animal Ecology, Vol. 35, No. 3 (Oct., 1966), pp. 471-485Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/2486 .

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471

WINTER BREEDING IN WOODLAND MICE, APODEMUS SYLVATICUS, AND VOLES, CLETHRIONOMYS GLAREOLUS

AND MICROTUS AGRESTIS, NEAR OXFORD

BY MICHAEL SMYTH*

Bureau of Animal Population, Department of Zoological Field Studies, Oxford University

Bank voles Clethrionomys glareolus and wood mice Apodemus sylvaticus will readily eat acorns and beech mast (Gorecki & Gebczyn'ska 1962; Holi'sova 1960), yet in English woodland both species usually stop breeding in October, when most of the seed crop falls. Now in some years acorns and beech mast are very much more abundant than in others (Jones 1959; Matthews 1955); in some years, too, bank voles and wood mice breed into and even through the winter (Baker 1930). Further, it has sometimes been observed, both in England and on the Continent, that the winter breeding has followed the heavy seed crop (Kulicke 1960; Newson 1963; Zejda 1962); the nature of the relationship between them, however, is not clear.

In this paper the relation between acorn crops and winter breeding in small woodland rodents is examined by means of two correlations, one between acorn crops and winter breeding in one part of Wytham Woods, near Oxford, over the last 16 years, the other between acorn crops and winter breeding in different parts of this same wood in December 1962.

STUDY AREAS

The data were collected in two parts of Wytham Woods known as Great Wood and Marley Wood. Great Wood is mostly mixed deciduous woodland; some parts are dominated by sycamore Acer pseudoplatanus L. and ash Fraxinus excelsior L. with a ground layer of mainly dog's mercury Mercurialis perennis L., and other parts are open stands of oaks Quercus robur L. (more or less hybridized with Q. petraea (Mattuschka) Liebl.) with a field layer dominated by bracken Pteridium aquilinum (L.) Kuhn and bramble Rubus fruticosus L. The vegetation of Marley Wood, about 1P5 km away, is similar except that it contains some unkept hazel coppice Corylus avellana L. with a ground layer of mainly dog's mercury. In both of these woods the two most abundant small rodents are bank voles and wood mice; field voles Microtus agrestis occur in small numbers in some places.

THE RELATION BETWEEN WINTER BREEDING AND ACORN CROPS SINCE 1949

Winter breeding since 1949 Information about winter breeding in Great Wood comes from an analysis of data

generously provided by Mr H. N. Southern. Southern himself has been mainly interested in the population dynamics of the tawny owls Strix aluco on the Wytham Estate in relation to the numbers of their main prey, and he has published a preliminary analysis (Southern 1959). Those relevant details of his methods which were not given in that

* Present address: Department of Zoology, University of Adelaide, South Australia.



472 Winter breeding in mice and voles

paper are as follows: he trapped, marked and released rodents once every 2 months on 96 ha from September 1948 until August 1952, and in collaboration with Mr V. P. W. Lowe on 48 ha of the same woodland from October 1954 until April 1956. Between August 1952 and October 1954, and after April 1956, he trapped and released every June and December on two 0-8 ha areas selected near the middle of the larger trapping areas. Breeding seasons were determined as follows:

In a female mouse or vole in breeding condition, the vagina is open (perforate), except that sometimes the external opening is scarred over for a while during pregnancy. If she

1962 1960 1949 1950 1951 1952 1953

22-0-23-5

14-0-15-5 L 9 /

10-0-1 1E5 CDn 37 68 43 121 72 32 23

3 Scale 74 1 9 50 an per cent

26 0-27 5 < --- V- --

10 0-11 5,C

31 44 74 161 93 30 14 FIG. 1. The body weight distribution per cent of male and female Clethrionomys glareolus in several Decembers. The first distribution for each sex is from a population in Great Wood which was known to have been breeding in December, the second from a population in Marley Wood known not to have been breeding in December. The other distributions are from Southern's data from Great Wood. The number below each distribution is the

sample size.

is not in breeding condition, the vagina is almost always closed, though sometimes a small opening may appear. The season during which females are in breeding condition can therefore be approximately defined from the condition of the vaginas. If no observations are made on breeding condition, it is still sometimes possible to judge the average breeding condition of a population if the distribution of body weights is known. At the end of a breeding season the body weight of a previously breeding animal falls. At the same time the population comes to consist mostly of young animals born late in the season, which postpone puberty until the following spring and live over winter at much less than their later breeding weight. The distribution of body weights in a non-breeding



MICHAEL SMYTH 473

population is therefore very different from that in a fully breeding population; compare, for example, the first two distributions for both males and females in Fig. 1, which are from bank vole populations known respectively to have been breeding and not to have been breeding in December.

In Southern's study, female breeding condition was recorded at all trappings after June 1949 except those of Decembers 1952 and 1953. These data are set out in Table 1. The most reliable are those for the condition of the vaginas; pregnancies are likely to have been noticed only in the late stages and were therefore probably under-estimated, and lactation was not always looked for. For most winters, however, it is obvious whether there was breeding or not. But some data need special consideration.

(1) In December 1949 a single pregnant bank vole was recorded in a sample of seventy- four females; the condition of the vaginas was not noted this month. Since only this one pregnancy was recorded, it is possible that it was wrongly diagnosed; it is not always easy to tell if a swollen abdomen is due to embryos or a full stomach, and there were several people helping with the trap rounds, not all equally experienced. But some wood mice were still breeding, and since the breeding seasons of bank voles usually correspond fairly closely to those of wood mice, the single pregnant bank vole cannot be dismissed as a certain mistake. Fig. 1 shows that both male and female body weight distributions were rather like those in December 1951, when at least some breeding was known to have occurred, though it had stopped by February. In neither of these years, however, does the distribution resemble that of a fully breeding population. It is possible that breeding continued later than usual in 1949 and that it had stopped just before December.

(2) In December 1950, out of 161 female bank voles examined, two were recorded as being pregnant. Since only two other female bank voles were recorded as having perforate vaginas, there is some cause to doubt these pregnancies. The distribution of male body weights this month was that of a population almost completely out of breeding condition, but it is possible that a very few females maintained breeding condition later than the rest. Evidence will be given later that breeding can, in fact, vary from one area to another, even in the same wood, so it is quite possible that over as large an area as was trapped at this time a few females still maintained breeding condition while others did not.

(3) In the Decembers of 1952 and 1953 breeding condition was not recorded, but the body weight distributions suggest that there was very probably no breeding either winter.

If it is allowed that bank voles were not breeding in December 1950, or that if there was breeding it was an insignificantly small amount, then these results can be summarized thus: both bank voles and wood mice bred into the Decembers of 1951, 1956, 1958, 1962 and 1964. Wood mice bred into the December of 1949, and bank voles might also have bred later than usual that year. In no other winter since 1949 has either species bred as late as December.

A partial check on these data is available in the data of several other people who have studied bank voles and wood mice in Wytham Woods. (Where these additional data are unpublished, they have been deposited at the Bureau of Animal Population, Oxford.) Miller (1951, 1958) found no breeding bank voles or wood mice in Great Wood in the winter of 1950-51. Todorovic (unpublished), working in Marley Wood, found no breeding in either species in the winters of 1952-53 or 1953-54. Kikkawa (1964), who worked in a small isolated patch of wood called The Pasticks, near Marley Wood, saw no breeding in the winters of 1955-56 and 1956-57. Newson (1963) found bank voles and wood mice breeding throughout the winter of 1958-59 in Great Wood, but not in the winter of 1957- 58 or 1959-60. Smyth (1963) found no winter breeding in Marley Wood in 1960-61

E JAE



Table 1. Winter breeding condition of female Clethrionomys glareolus and Apodemus sylvaticus in Great Wood, 1949-65

C. glareolus A. sylvaticus r -,

No. No. No. No. No. No. perforate pregnant examined Summary perforate pregnant examined Summary

1949-50 12-20 Dec. * 1 74 ? *(3) 4 130 + 13-22 Feb. 2 0 79 - 14 0 130 -

1950-51 12-21 Dec. 2 2 161 ? 2 0 41 - 26 Feb.-6 March 10 0 166 - 12 0 63 -

1951-52 1-8 Dec. 23 7 93 + 30 18 121 + 16-23 Feb. 3 0 146 - 6 0 81 -

1952-53 15-16 Dec. No information 30 No information 5 1953-54 21-22 Dec. No information 14 No information 15 1954-55 29 Dec.-8 Jan. 0 0 138 - 1 0 30 - 1955-56 28 Dec.-5 Jan. 2 0 119 - 2 0 88 -

27 Feb.-7 March 2 0 121 - 1 0 37 - 1956-57 5-6 Dec. 16(2) 2 28 + 16(4) 3 23 + 1957-58 12-13 Dec. 1 0 31 - 1 0 13 -

1958-59 10-11 Dec. 15 3 18 + 21(1) 4 30 + 1959-60 30 Nov.-l Dec. 0 0 67 - 2 0 16 - 1960-61 1-2 Dec. 4 0 25 - 4 0 10 - 1961-62 13-14 Dec. 0 0 25 1 0 18 1962-63 21-22 Dec. 26(3) 6 31 + 6 6 7 + 1963-64 30 Nov.-l Dec. 1 0 44 - 0 0 10 1964-65 3-4Dec. 5 2 12 + 11 4 25 +

* The condition of the vaginas was not noted. Figures in parentheses refer to the number of lactating females noticed. In the summary column: + means that there was breeding, - means

that there was not.



MICHAEL SMYTH 475

and 1961-62 but both species were still breeding in December 1962. Watts (unpublished) found no winter breeding in Marley Wood in 1963-64, but in 1964-65 he found that both species bred later than usual both in Marley Wood and Great Wood, and that in some parts of Great Wood male wood mice maintained breeding condition throughout the winter.

The only data of all these which are inconsistent with Southern's are those of Kikkawa for 1956-57 in The Pasticks, and since there is no reason to doubt either set of data it would seem that there were differences between the populations on different areas this winter. Another example of this is discussed in detail later.

Acorn crops since 1949

The variation of acorn crops from year to year can be enormous. Jones (1959) has recorded up to 90 000 acorns from a single tree which in other years can be almost

Table 2. Data from several sources on the acorn crops around Oxford, 1948-64 Jones* Probitts Others Summary

1948 0 Failed' Failed 1949 420 Good2 Good 1950 44 None Poor2 Very light 1951 405 Fair Good 1952 11 None Very light 1953 - Good Fair, patchy? 1954 - None Failed 1955 - None Failed 1956 + Good Good 1957 - None Failed 1958 + Good Heavy" 3 Good 1959 - None Failed 1960 + Very light Fair, patchy? 1961 - Fair Very light 1962 + Fair Heavy' Good 1963 Poor4 Failed 1964 Good4 Good

* The numbers indicate the relative abundance of acorns until 1952. After 1952, the acorn crop was either fair or good (+) or poor (-).

The superscripts refer to the following sources: 'Elton (personal communication), 2Miller (1954), 3Newson (1963), 4Watts (personal communication).

completely barren. Yet despite such obvious variation, there are no good records of the crops in Wytham Woods, and I have had to collect the evidence from several sources. Dr E. W. Jones gave me information from Bagley Wood, about 8 km south-east of Great Wood. For the period 1948-52 he gave me figures showing the approximate relative abundance of acorns from forty-two to sixty-eight trees; for the years after 1952 he could only say whether the crop was poor or not. Mr H. Probitts, the Head Forester of Wytham Estate, has collected seed acorns from four selected trees in Wytham Woods, and has been able to put the size of the crop each year into four classes; none, very light, fair or good. Other information has been taken from Miller (1954) or given me by Mr C. S. Elton, Dr Robin Newson and Mr C. H. S. Watts.

All the evidence is gathered together in Table 2. Now according to Jones (1959), 'there is very great variation from tree to tree, even of the same species, in capacity for bearing; some individuals never bear good crops'. And again, 'it will often happen that




in a year and a district when there is almost complete failure of seed there will be abundant seed over a limited area-sometimes in a single wood, or in a part of a wood, or on a few trees. Conversely, in a year of heavy crops there may be isolated areas where for no apparent reason crops have failed'. Obviously Table 2 must be interpreted with caution, but for most years the information from various sources is consistent. It is also consistent with two other facts; oaks do not bear well two years in succession, nor if defoliating caterpillars destroy the blossom. From 1948 to 1962, the only years in which severe defoliation has occurred around Oxford have been 1948 (Jones 1958), 1952 and 1954 (Varley & Gradwell 1962 and personal communication). In 1948 acorns were on the average abundant in England (Forestry Commission 1950, p. 50); the crop around Oxford, however, failed that year because of the defoliation, and appeared instead the following year (Jones 1958).

Two other years need special consideration. The first is 1953, when the information from Jones and Probitts is contradictory. Since according to Professor J. D. Matthews, then of the Forestry Commission Research Station at Alice Holt Lodge, Farnham, it was on the average a poor to moderate year over the whole of England, I have guessed that in Wytham Woods it was fair at best, and that fruiting oaks were probably distributed patch- ily. Under these circumstances it is possible that most acorns would be taken by squirrels and wood pigeons before or soon after they fell (Tanton 1965). The same possibly applies for 1960.

The relation between winter breeding and acorn crops since 1949 If December breeding is looked at in relation to acorn crops, it can be seen that in the

last 16 years bank voles and wood mice have bred as late as December only after a good acorn crop; further, a good acorn crop has almost always been followed by an extension to the breeding season.

DIFFERENCES IN BREEDING INTENSITY ON NEARBY AREAS IN 1962

In December 1962, after good acorn crops, another correlation was established, this time between winter breeding and the number of oak trees on nearby areas. In December 1960 I had begun a field experiment on the effects of population density on populations of bank voles and wood mice. The details of the experiment will be published in another paper, but, briefly, I trapped monthly until December 1962 on two areas of 1P8 and 3 0 ha, about 115 m apart. On the first, known in this paper as Plot 1, I marked and released all animals I caught; on the second, Plot 2, I killed most but marked and released a few. Killed animals were almost completely replaced by immigrants in all months except those of late winter and spring 1962.

In October 1962 it was obvious that breeding was going to continue longer than in 1961. I did not trap again until December; I then killed all the bank voles and the field voles caught on both areas and examined them post-mortem for breeding condition. I released the mice. Almost immediately afterwards Southern trapped as usual in Great Wood, and killed a sample of bank voles for dissection. This sample included all that weighed 17-0 g or less, and was therefore biassed towards younger, lighter animals. The breeding condition of females of all three species was determined by examining for perforate vaginas, pregnancy, and lactation, and embryos were counted post- mortem. The testes of dead males were weighed, and breeding condition was determined by whether or not the tubules of the epididymides were clearly visible to the unaided eye (Hamilton 1941).



MICHAEL SMYTH 477

The breeding data for bank voles are given in Table 3; they show that few bank voles were still breeding on Plot 1, but that most were still breeding on the other two areas. The proportions of males in breeding condition on the areas were nicely reflected by the distributions of male body weights (Fig. 2).

(a) (b) (c ) 26 0-27-5-

24 0-2555 A -

22-0- 235

a 200- 21 5 -C

180-195

O 16.0 - 17- 5 -

140 -155-

120 -13-5 -

100 -115.

Scale 0 25 per cent

FIG. 2. The body weight distribution per cent and breeding condition of male Clethrionomys glareolus on the three study areas in December 1962. The breeding condition of males from Great Wood was not determined except for a small sample. (a) Plot 1, N = 71; (b) Great

Wood, N = 37; (c) Plot 2, N = 58. Black area, fecund; white, not fecund.

The experimental culling of the population on Plot 2 cannot account for the extended breeding season on that area, since the breeding season in Great Wood, where there had been no culling, was similarly extended. But differences between the acorn crops on the

Table 3. Breeding condition of Clethrionomys glareolus in December 1962

Females Males

Plot 1 Plot 2 Great Plot 1 Plot 2 Great Wood Wood

Pregnant 0 17 (38) 17 (55)* Lactating 5 (10) 16 (34) 3 (10) Others fecund 3 (6) 6 (13) 6 (19) Total fecund 8 (16) 39 (83) 26 (84) 14 (21) 50 (88) 10 (83) Not fecund 41 (84) 8 (17) 5 (16) 52 (79) 7 (12) 2 (17) Total 49 47 31 66 57 12

* Includes one female with a copulation plug. The percentage which each class forms of the total is in parentheses.

three areas can account for the differences in breeding season. Fig. 3 shows the distribution of oaks on the study areas. Both the density of oaks and the breeding intensity in Great Wood are much more like those on Plot 2 than those on Plot 1. I have no data on the fruiting of individual trees, but as late as 27 March there were still acorns under all but three oaks on the study areas in Marley Wood, and under most oaks in Great Wood. The three exceptional trees in Marley Wood might have borne good crops which had




later been removed, but two of them carried considerable dead wood and there is therefore reason to suspect that they did not bear acorns.

The relation between winter breeding and age

The age of dead bank voles can be judged from the condition of the molar roots (Mazaik 1963; Zejda 1961). In order, therefore, to find the relation between winter breeding and age, I measured the roots of the first lower molars (MI) of all bank voles killed in December 1962. The skulls were firstly cleaned by Dermestes maculatus Deg. larvae; they

MARLEY WOOD

0

o PLot 2REAT W

0

?O 0 100

o 0 0

Plo t 2

FIG. 3. The distribution and fruiting (where known) of oaks on and near the study areas in December 1962. The scale is approximately the same for all areas; the oaks in Great Wood, being in denser stands, have smaller canopies. Acorns: *, abundant; o, not searched for;

o, not found.

were then softened in boiling water for about 10 min, and the incisor of the right lower jaw was split away by striking diagonally down through the bone in front of and slightly inside the M1 with a strong sharp needle. The M1 could usually then be lifted out, and fragments of bone and connective tissue cleaned off with a stiff brush. The teeth were then mounted between strips of transparent adhesive tape laid over empty transparency mounts, and their outline was projected onto a wall and measured with a ruler. The



MICHAEL SMYTH 479

f It~

1 2 3 4

FIG. 4. Four stages in the formation of the roots of the first lower molar of young Clethrionomys glareolus, seen ventrally. The open pulp cavity is in black.

15 _2 0 (a)

7 E

6 15 O ? 6 , 0 0 c

0

5 O O O*

0

0 0 0

U) 2 b

C l 71 S 3- 4 O 5.*. l W

3 -0

(A 0 3 C OD. . . . .

?05

C 2.0 (b)

11

c E o 7 0 3105 E

0 - 0 05

the aprxmt age corsodno the mea M1ro egh sas gvn a lt1 b

4e 00.5 *~~

3

(A 00

6 - (c) 0)

5 - 0

0

4 4Q.

00

Ul

0

o ioo 200 300 400 500 600 700 800 Testes weight (mg)

FIG. 5. The relation between the testes weights of male Clethrionomys glareolus and the conditions or mean lengths of the roots of their first lower molars, December 1962. A scale of the approximate ages corresponding to the mean MI root lengths is also given. (a) Plot 1, (b)

Plot 2, (c) Great Wood (sample). *, Fecund; 0, not fecund.




measurements taken were those suggested by Mazaik (1963, Fig. 2). All the data and the teeth themselves are now at the Bureau of Animal Population, Oxford.

In recently weaned bank voles, the single pulp cavity of the tooth is wide open, with ragged and irregular edges. Then, as the tooth grows, this cavity becomes two separate cavities around which the roots form. Four stages of this sequence are shown in Fig. 4. After these roots have formed, they then elongate gradually but not necessarily at a constant rate. The age of the bank voles was determined by referring the condition or length of their MI roots to a scale which was made using measurements from marked animals whose month of birth was known from their body weight at first capture.

The relation of testes weight and breeding condition of male bank voles to this index of age is shown for the three populations in Fig. 5. It is apparent that among the males, most of the difference between the Plot 1 population on the one hand and the Plot 2

16 (a) (b) (c)

14

12

6

4

2

1 2 3 4 0-5 1-5 2- 5 l 2 3 4 0 51.0 t 2 3 4 0.5 1 5 Class Ml root length (mm) CLass Ml root Class MI root length

length(mm) (mm)

FIG. 6. The relation between the breeding condition of female Clethrionomys glareolus and the condition or mean length of the roots of their first lower molars, December 1962. (a) Plot 1, (b) Plot 2, (c) Great Wood (sample). Solid shading, pregnant; cross-hatching,

fecund not pregnant; unshaded, not fecund.

and Great Wood populations on the other hand was in the breeding condition of young animals before the roots had begun to form-that is, up to about 3 months old. Among the females, the differences between the populations were spread through most age classes (Fig. 6); on Plot 1 there were no pregnant females at all, while on Plot 2 there were pregnancies among all but the youngest females; there were young females pregnant for the first time, and there were nulliparous females with swollen ovarian follicles, possibly of their first oestrous cycle.

Litter size in winter

Litter sizes, counted from embryos post-mortem, or occasionally from litters born in traps, were on the average significantly smaller than they were at the peak of the breeding season, in both parous and nulliparous females (Table 4).



MICHAEL SMYTH 481

Table 4. The frequency distribution and mean of litter sizes of Clethrionomys glareolus in Wytham Woods, 1962 Parous First litters

A I . A. -,

2 3 4 5 6 7 Mean+ S.E. 2 3 4 5 Mean+ S.E. December 9 7 1 3.53+015 1 5 1 3 0 ?0 22 July-September 1 3 7 10 1 1 4 43 ? 023 2 2 7 445 + 025

The figures for December are from animals from Plot 2 and Great Wood. The figures for July-Sep- tember are from animals killed on Plot 2 those months. The differences between summer and winter litter sizes are in both cases statistically significant (P < 0-01).

Wood mice

The information from wood mice is not as detailed because all mice caught in Decem- ber were released, not killed, and those caught in Great Wood were not weighed but only classed as small, medium or large. Table 5 gives the recorded breeding condition of

Table 5. Breeding condition of adult female Apodemus sylvaticus in December 1962

Plot I Plot 2 Great Wood Pregnant 0 0 6 (86) Lactating 2 (29) 8 (47) 0 Others fecund 2 (29) 9 (53)* 0 Total fecund 4 (43) 17 (100) 6 (86) Not fecund 3 (57) 0 1 (14) Total 7 17 7

* Includes two females with copulation plugs. Adults are those weighing 15-0 g or more in Marley Wood, or classed as medium or large in Great Wood. The percentage which each class forms of the total is in parentheses.

females weighing 15-0 g or more in Marley Wood, or classed as medium or large in Great Wood. Small animals have been excluded because in such small samples a variable number of juveniles makes interpretation difficult. It seems from Table 5 that there were similar differences between populations of wood mice asbetweenpopulations of bank voles.

Field voles

Only twenty-seven Microtus agrestis were caught; Table 6 gives the breeding data. All animals were heavy enough and therefore old enough to have been in breeding condition. Earlier, in September, some males had been caught which were not at all in breeding

Table 6. Breeding condition of woodland Microtus agrestis in December 1962 Females Males

Plot I Plot 2 Great Plot 2 Plot 2 Great Wood Wood

Pregnant 0 2 (67) 1 (33) Lactating 0 0 2 (67) Others fecund 0 0 0 Total fecund 0 2 (67) 3 (100) 2 (25) 0 0 Not fecund 8 (100) 1 (33) 0 6 (75) 4 (100) 1 (100) Total 8 3 3 8 4 1

The percentage which each class forms of the total is in parentheses.




condition, yet Table 6 shows that in December there were others still fecund. From such small samples it is difficult to tell if there were any differences between the areas, but two conclusions can be drawn. Firstly, some Microtus were still breeding. Secondly, there is greater variation in breeding season between individual Microtus than between individual bank voles or wood mice.

THE SEVERE WINTER OF 1962-63

At the end of December the winter became one of the severest recently known in Britain, yet it must have been an unusually favourable winter for the mice and voles in Wytham Woods. About a foot of snow fell in the last week of December and lay with additions during 2 months of almost continual frost; where it fell on bracken, bramble or grass there was always enough room for small animals to move about freely beneath it (see Formozov 1946; Coulianos & Johnels 1962), and the ground, insulated in these places by the snow, showed no signs of freezing until the thaw late in February. Many acorns were still available to mice and voles, but were partly protected from squirrels, pheasants, wood pigeons and deer, which had to dig or scratch for them through deep snow which had glazed on top.

On 11-12 February 1963, a sample of six bank voles and four wood mice were caught under the snow. One of two male bank voles and one of two male wood mice were in full breeding condition, with large testes and opaque tubules in the epididymides. Four female bank voles, one parous, and two female wood mice, one parous, were all out of breeding condition. Possibly, therefore, some males of both species maintained breeding condition throughout the winter, but I do not know if there was any reproduction. Frank (1964) found continental voles and wood mice (but not bank voles) breeding under the snow this same winter in Germany.

DISCUSSION

In the last 16 years, bank voles and wood mice have only bred late after a good acorn crop, yet surprisingly there is no simple relationship between them. The possible relation- ships are set out below as a series of hypotheses, and examined in turn.

(1) Both good acorn crops and winter breeding are independently determined by the weather. This is untenable for several reasons; it is ruled out by the fact that in December 1962 there were differences in breeding intensity on areas on which the weather must have been almost exactly the same. Other workers, too, have found differences between breeding intensities of nearby populations of small rodents; Zejda (1962) found them in bank vole populations in southern Moravia, and he too found that breeding intensity was correlated with the abundance of acorns on the areas. Stein (1953) found that the Continental vole Microtus arvalis (Pallas) bred into the winter if it was living among crops of rape and winter rye but not if it was living on uncultivated land nearby.

Further, if both good acorn crops and winter breeding are independently determined by the weather, then winter breeding should sometimes occur when acorn crops have failed, either because oaks fruited well in the previous year, or because oaks were defoliated in a year in which they would otherwise have fruited well. This has not happened in Wytham Woods for the last 16 years.

This first hypothesis can be stated in a rather different way. Chitty (1960) has suggested that during a cycle of abundance of M. agrestis the average behavioural properties of the members of the population change, and that these changes in quality, interacting with



MICHAEL SMYTH 483

the environment, have profound effects on survival and possibly on reproduction (see also Newson & Chitty 1962). The fact that the cycles of several species can be synchro- nous over a very wide area can then be explained only in terms of some effect of the weather. Winter breeding might therefore occur in good acorn years only because the same weather that determines good acorn crops also determines that the phase of the population cycle shall be that in which winter breeding occurs-that is, good acorn crops are not necessary, only coincident. The objections set out above still apply.

(2) Good acorn crops are all that is necessary for winter breeding. Or, since it is not to be supposed that acorns alone are the only food necessary to winter breeding-acorns just happen to be the most variable food on our study areas at this time of the year- this hypothesis can be stated more generally as that very abundant food is all that is necessary for winter breeding. (Note that bank voles and wood mice usually survive well over winter, so that there cannot usually be a winter food shortage; winter breeding must therefore require an excess of food over that necessary for simple survival.)

The hypothesis is, however, untenable for two reasons. Firstly, populations of M. agrestis and M. arvalis in outdoor cages, and of white-footed mice Peromyscus leucopus (Rafinesque) on islands, have been found not to breed into the winter though given all the food they need (Clarke 1955; van Wijngaarden 1960; Bendell 1959), and though all three species have been known to breed into the winter in the wild (Clarke & Forsyth 1964; Stein 1953; Linduska 1942). Secondly, bank voles sometimes stop breeding as early as Sep- tember, well before most tree seeds fall (Zejda 1964), and it seems unlikely that food should be too scarce for breeding as early as this.

(3) A very good food supply is necessary but not sufficient for winter breeding. This implies that in Wytham Woods food is only abundant enough for winter breeding after a good acorn crop. It makes good sense for bank voles and wood mice, both of which are fond of acorns; it would not be surprising if these animals were adapted to take advantage of a sudden and large abundance of food in the autumn by breeding later than usual. But it is more difficult to apply this hypothesis to the field vole, which as far as is known does not eat acorns and which at least in the winters of 1958-59 and 1962-63 maintained breeding condition not only in woodland but in grassland as well (Clarke & Forsyth 1964; Clarke, personal communication). The only way to accommodate these observations is to suppose that the production or quality of grasses, which are the main food of the field vole, is correlated with the fruiting of oaks and other trees (for another statement of this hypothesis, see Kalela 1962). But we are still left with the question of what else is necessary, as well as very abundant food.

One possibility is that high population density, or changes in population quality associated with it, could inhibit breeding even when food is abundant enough. Lemm- ings, for instance, which will breed under the snow throughout the long, dark arctic winter, apparently do not do so when numbers are high or declining, even though in some cases food seems abundant (Krebs 1964). A Moravian population of bank voles which stopped breeding in September was unusually dense (Zejda 1964). Schindler (1960) found a population of bank voles in Germany which stopped breeding in August; this case is complicated, however, by the fact that bank voles were not only very abundant but in September and October they caused severe damage to tree seedlings by eating the bark from them, so in this case they were possibly short of food as well. What little reliable information we have on population densities in Wytham Woods does not contradict the suggestion; the winter breeding in 1958-59 followed a period of very low numbers for both species (Newson 1963), and in Marley Wood in 1962-63 it followed a




time when bank voles had been at intermediate abundance for the previous two years and when wood mice had been very scarce after a decline during the previous winter (Smyth 1963).

The best hypothesis to explain the coincidence of winter breeding and good acorn crops thus seems to be that winter breeding depends both on unusually abundant food and on some other unidentified factor which could be some quality of the population itself. The first part of this hypothesis, as it applies to bank voles and wood mice, could be tested by providing abundant food (preferably acorns) in the late autumn and early winter of a year in which tree seed crops failed.

It is perhaps worth noting that although both bank voles and wood mice can maintain breeding conditions under the snow, where the temperature is almost O C and very little light penetrates (Geiger 1957), nevertheless litter sizes are smaller in the winter, so winter conditions presumably do affect the secretion of gonadotrophins.

ACKNOWLEDGMENTS

I thank Mr C. S. Elton, Director of the Bureau of Animal Population, who provided transport and laboratory facilities, and Mr D. A. Kempson, Mr Ken Marsland and Mr Tony Dunford for technical help. The many people who helped with data and advice, and especially Mr H. N. Southern, have all been thanked privately.

SUMMARY

1. Bank voles and wood mice bred at least as late as December after good acorn crops in 1951, 1956, 1958, 1962 and 1964. After a good acorn crop in 1949, wood mice certainly bred into December; bank voles might have bred later than usual. In no other year since 1949 has there been a good acorn crop or have bank voles or wood mice bred into the winter.

2. In December 1962, more bank voles and wood mice were in breeding condition where oak trees were abundant than where they were sparse. The differences between breeding intensities of male bank voles on these areas in December 1962 were mainly a matter of differences in the number of young males in breeding condition. Bank vole litters are smaller in the winter than in the summer, from both parous and nulliparous. females.

3. Field voles also bred at least into December 1962, both in woodland and grassland. Some male bank voles and wood mice maintained breeding condition under the snow cover during the severe winter of 1962-63.

4. The relationship between winter breeding and acorn crops is not simple. It is argued that a very good food supply is necessary for winter breeding, but that winter breeding also depends on some other unidentified factor which is possibly some quality of the population itself.

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MICHAEL SMYTH 485

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