The EcologicalSocietyEcological Society of Japan
Ntil2kftst (Jap, J. Ecol.), 31: 247-256, 1981
REPRODUcrIVE IN CLETHRIOIVOMYS RUFOCAIVUS BEDFORDIAEACTrvITY4. NUMBER OF EMBRYOS AND PRENATAL MORTAI,rltYi)
Yluzo FUJIMAKI,Laboratery of PVildtijli Resource Eceiqgy,, Obthiro U}tiversityofAgriculture
arid P;eterinary Medicine, Obihiro 080
= V'Vf*-' .: Oecvatsnt4 . ta va tu t di fii ntu fi t ' rstaIEv(#"thitthlo`elfeemza$ wt g ws di
Synopsis FunMAKi, Yuzo (Lab. Wildl. Resou. Ecol., Obihiro Univ. Agric. Vet. Med., Obihiro). 1981. Repro- ductive activity in CZethrionomys rnjbcanus becefordiae 4. Number of embryos and prenatal mortality. Jap.J.Eco1.31:ZtP7-256. Variatjons in the number of embryos of Clethrionomys rtofbcanus beeUbrdlae were cxamined using 747 pregriant fernales obtained from various areas of Hokkaido in 1967-1974. The numberofem- bryos per pregriant female ranged from l to 10 and averaged 5.3. The mean was srnaller than that in high latitudes of th6 Eurasian Continent: However, regional variation was not recognized within Hok- and 5.2inOctober. The number of kaido. Tbe mean pumber of ¢ mbryos was 5.9 in June, 4.8 in August embryos tended to increase with advanoed age and increased body weight of females, but it decreased in females of 12 months old. Thus the declinein the number ofembryos in August and October was at- tributed to advanced ago in overwintered females and recmitnrent of young fernales to the population, There was no difference in the number ofembryos between primiparous females and multiparous ones, Tbe number of corpora lutea per pregnant female ranged from 2 to 14 and averaged 6.1. Prenatal loss ef embryos was found in 36.0% of the 439 pregnant females examined. The prenatal mortality was 9.0% for overwintered females and 16.5% for females of the year, and it increased with the increas-
ing number of corpora lutea.
major roles in determining the pattern of popula- Introductien tion fluctuation. FuJiMAKi (1972, 1973, 1975) lhe red-backed vole, CVlethrionomys reijbcanus investigated regional variations in the reproduc- betUZ}rdiae, is disuibuted in Hokkaido, Japan, as a tive activity of the species throughout Hokkaido common inhabitant of forests, brushy areas, and in relation to the population trend, and found oocasionally grassy areas. Many papers have been that in the southern part, the enset of breeding - published on its ecological distribution, reproduc- was earlier in spring and the termination was later tion, food habits and flycLuation (see in autumn than in the northern and eastern parts. population 'aspects UEDA et al., 1966). Since these papers were based T he present study aims to show several on data obtained from only one or a few locali- of variations in the pumber of embryos and the ties, they do not present a wide perspective on the prenatal mortality in the red-backed vole based on species' breeding biology throughout Hokkaido. the data obtained from various areas ofHokkaido. It is well known that the'vole shows a high am- Materials and Methods plitude of population fluctuations in northern and eastern Hokkaido (UEDA, et al., 1966; FuJiMAKi, The trapping was carried out at 40 sites in 1971). However, the mechanism of these fluctua- Hokkaido during the months of June, August tions has not been clarified because of insuMcient arid October in evefy year from 1967 to 1974 (Fig. knowledge about birth and death playing the 1). Each site censisted of young Larix ioj)tolqpis or Abies sachalinensis plantation (O.5 ha) and its Aooepted Dec. 17, 1980 neighboring area (O.5 ha). The trapping methods 1) Contribution from the LaboratQry of Wildlife Re- used were described elsewhere 1972)- source Ecology, Obihiro University of Aghculture and (FuJiMAKi, trapped were weighed and pre- Veterinary Medicine, No. 33 AII of the females
247
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Vel. 31. No, 3 H* th me #k ss Sep., 1981
.LiY'tt 31
4S..lo-3rD
-T9tll- ss
-ZB-34- { tl TII [V V VI .?1-"' 44o Fig. 2. Age classes based on the groove closing and Lir)..x:iilc!",,'25' root forrmation in the upper socond molar. 13. ;V!1,. .14Xl.t2t{3fiE:S19'
-11t12 dla"-4--.-5rN6 were foTmed, but they were less than 1!3 of the Bs.7t IT -io-gN-?ox whole length of M2 ; V: the roots were 113 to 1/2 of
the ]ength ofM2; VI: the roots wcre more than ta-1N A3 1/2 of the length of M2. The females of the year 41. -!1 belonged to age classes I and II in June, I to III in
August, and I to V in October, Overwintered
females were in age class IV to VI in June, V and Fig. 1. Locations of sampling sites and five areas in VI in August, and VI in October (ABE, 1976). Hokkaido. 1; Esashi, 2: Hakodate, 3: Meri, 4: Hekkaido was dividedinto 5 areas, A, B, C, D, rrnagene. 5: Toyoura, 6: Soubetsu, 7: Urakawa, and E 1) according to the pattern of popula- 8: Mitsuishi, 9: Biratori, 1O: Hayakita, 11 : Yoichi, (Fig. tion fluctuations and the reproductive activities of 12: Sapporo, 13: Toubetsu, 14: lwarnizawa, 15: Bibai, 16: Fukagawa, 17: Rumoi, 18:Touma, 19: the species. As has been reported, in D and E the Biei, 20: Taiki,21: Toyokoro, 22: Ashoro, 23: voles increase abruptly in number from spring to Oketo, 24: Rubeshibe, 25: Kitami, 26: Abashiri, autumn, exhibiting a high amplitude of popula- 27: Obira, 28: Haboro, 29: Shozanbetsu, 30: Te- tion fluctuations, whiie in A and B, they inerease shio, 31: Hamatonbetsu, 32: Nakatonbetsu, 33: slightly from spring to autumn. [[he population BifUka, 34:Nayoro, 35: Okeppe, 36: Akan, 37: trend in C is intermediate between thes¢ two pat- Akkeshi, 38: Shibecha, 39: Bekkai, 40: Nakashi- terns 1971). In A the breeding season betsu. (FuJIMAKi, extends from mid-March to late October, an in D and E from mid-April to mid-October. The re- served in IO% formalin so]ution to examine the productive activity in summer is more intense in D uterus, ovarjes and upper second molar. Of a total and E than in A. The onset and termination of the
visible seasons, and the of reproductive of 3415 femalescaptured, 747 (21.9%) had breeding degree embryos in their uterus. [(lhe numbers of preg- actjvity in B and C are intermediate between nant femares captured were yariable from year to these ofA and E (FuJiMAKi, 1972, 1973, l975). year: 44, 50, 128, 94, 154, 71, 111 and 95, respec- Results and Discussion tively during the 8 year examination period. The number of visible embryos in the uterus was count- Regiona} yariation in the number of embryos ed with the naked eye, but that of the plaoental The rnean numbers of embryos in the 5 areas sears was not consideTed. Ihe number of embryos are given in Table 1 . The mean ranged from 3.7 to in one litter did not include the resorbing ones. 5.2 in June, 4.1 to 5.0 in August, and 5.0 to S.5 in The number of corpora lutea in the ovaries was October for the females of the year. The corre- counted with the naked eye in 439 ofthe 747 preg- sponding valiles fbr overwintered females were
nant femaies,Tliebody weight of the pregnant 5.6to 6.2,4.1 to 5.0,and 4.7 to 6.0 , respect:vely females was determined by subtracting the weight (Table 1). No significant differences were found ef the embryos. among the 5 areas in the respective months in the The ages of the pregnant females were deter- overwintered females as well as in the females of mined aecording to the groeve closing and root the year (Student t-test, P>O.1). The combined formation in the upper second rnolar (M2) as il!u- data ofthe three months in one area did not reveal strated in Fig. 2. As shown, I: the grooves did not any significant difTbrences in the mean among the close at the basal tip of M2; II: the grooves were 5 areas in either of the age groups (P>O.1). In closed at the basar tip; III: after closing of the PreviOus papers (FuJIMAKI, 1972, 1973. 1975), of grooyes, the neck grew; IV: two separate roots there were some indicationsthatthe number
24g
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VoL 31, No. 3 JAPANESE JOURNAL OF ECOLOGY Sep,, 1981
Table 1. The number of embryos (rnean [l SE) in females of the year (above) and in overwintered females (belew) obtained from fivc areas of Hokkaido in 1967-1974 (see Fig. 1), Aiea .Whole Overallfemales A B C D Ezz area
Number of females 111 113 97 184 242 747 examined June 5.2±O.46.04.8± O.46.15.0± O.65.63.7± O.96.24,2± O.56,OtO.2S.O4.8± 026.1 5.9± O,1 ±O.24,1 ± 024.2 ± O.34.9 ± O,24.S ± O.14,8 August ±O.34.1 ± O.24.8 ± O,35.0 ± O.25.0 ± O.1 ± O,14.84,8± O.1 ±O.45.4 ± O.352 ± O.35.5 ± O.25.04.6± O.35,1 ± O.152 October ± O.25.4 ± O.34.9 ± O.36.e ± O,26,O ± O.44,7 ± O.15.35.2± O.] ± O.25.2 ± O,44,8 ± o.s5.1 ± O.64.6 ± O.5S.O ± e,24.9 June to October ± O.25.6 ± O.25.8 ± O.25.5 ± O,15.7 ± O.1S.5 ± O.15.6S.3± O.1 ± 02 ± O.2 ± O.2 ± O.1 ± O.2 ± O.1
embryos for the overwintered females was larger Table 2. The frequency distribution of the number of in the northern or eastern part than in the southern embryos.
part in June, but this trend was not recognized in Number ef females Number of Augusgt and Octeber. embryos Observed Expected The number of embryos did not appear to vary 12345678910 3 within the narrow range of between 41"50' and 13 } 13,9 45010' latitude of Hokkaido (see Fig. 1). Thus the 43140241180 54.3142.2214.8189.4 regional difTbrences in popUlation trends cannot be interpretcd as beeing due to the variation in the number of embryos. In summer, the reproductive activity is known to be more intense in D and E 93 97.8 than in A, because animals of the year, comprising 24 29.1 6 of 70 to 80% of the summer population, attain to 4 } S.7 sexual maturity in younger ages in D and E than in A (FuJIMAKI, 1973). An abrupt increase in the population density may be attributed partly to the large samples found in Finland and in the Kora
high reproductive activity. Peninsula, 91 and 92%, respectively, were in a
For the 747 pregnant females obtained from the rangeof4to7embryos(KALELA,1957;KosHKiNA entire study area, the number of embryos ranged 195n, In conclusion, the number of embryos
from 1 to 10 with a mean of 5,3. The frequcncy ranges from l to 13 and varies usually between 4 distribution was normal (O.1>P>O.05, Table 2). and 7 throughout the distribution ranges. Eighty-eight percent of the 747 litters were in a The number of embryos in the present study range of 4 to 7 embryos, which correspended ex- was similar to that in the central Shiknote-Alin
actly with the figures reported previously: the Mountains, which are situated approximately in number ofernbryos was usually 4 to 7, 5 and 6 be- the same latitude as Hokkaido (SMiRNov, 1970; ing the most abundant number (UEDA et al., 1966 ; BRoMLEi & Kos:[ENKo, 1970) (Table 3). Ihe other KuwAHATA, 1966). The largest number that has l5 localities listed in Table 3 are situated in higher so fatr been reported is 12 from Nopporo, which is latitudes (53-69") than that ofHokkaido (42-450). located near Sapporo (site 12 in Fig. 1) (KuwA- Smaller numbers than the 5.3 reported in Hokkai- HATA, 1966). do were report ¢ d from only three other localitias. Besides Hokkaido, C. rwfbcanus is widely distri- The data in two of the thi'ee were based on small buted in the Eurasian Continent east to the Far samples (IV == 9 and 11). [[he numbers ofembryos East and west to Europe. Available information in some northern localities such as Finland and
on the number of embryos of the species in the southern Yakutia were significantly larger than Continent is summarized in Table 3. The number those from Hokkaido (P NII-Electronic Library Service The EcologicalSocietyEcological Society of Japan Vol. 31, No. 3 m th ma*ft su Sep., 1981 Table 3.The number of embryos (meanpt± SE) of Clethriononrys rsofloccmus in various tocalities. Numbor of Number of Locality(latitude) femalesexamined embryos Source (mcan± SE)Range Kilpisiarvi, Finland (68") 28S195* 6,O± O,15.1 2-101-8 KALELA, 1957 Kora Peninsula (68S ± O.1 KosHKINA, 1957 Ura1 Mountains Po]yarnyi (660-68e) 6.76.052 o POKROVSKII& Central (6oe) BoL'sHAKov, 1979 Southern (55D) 1'I!} Yakutiya Eastern (66e-6ge) 85232 6.7± O.25.7 TAvRovsKIIet Southern (56e-65e) ± O,1 Iil;l aL, 1971 Chukot Chaunsk Lowland (680) 617 7.5±O,55.7 6-93-9 Kolyma Mountains (650) ± 1.2 Upper reaches of YuDIN et al., Omolon Rivcr <650) 659 5.4± O,67.6 3-86-93-10 1976 Basin of Anadyr River (65D) ± O.76.7 Koryak Mountains (62e) ± O.6 PoRTENKo et al., 1963.* Upper reaches of Lena River (57e) 9* 5.1± O.7 1-8 IUIIMERs, 1966 Upper reaches of Lena River (57e) 17 SJ ± O.7 1-11 REIMERS & VoRoNov. 1963** Pribaikal (53") 11147 4.4± O.35.45･3m5a63-6 REIMEms, 1959 Centra1 Shikhote-Alin (45") SMIRNov, 1970 Central Shikhote-Alin (45e) 2-11 BROMLEI & KosTENKo, 1970 Nopporo, Hokkaido (430) 192747 5.4± O.15.3 2-121-10 KuwAHATA, 1966 Hokkaido (420-4s') ±O.1 kesentstudy 'Counts of plaoental scars are excluded, .*Data are cited from TAvRovsKii et al,, (197t). ficant correlation between the rnean number of O.1). The mean in age class IV in October was embryos and the latitude (r t= O.53, O.02>P> significantly larger than in all of the other age ' O.el, N = 19). It is well known that in other small classes (P each age class.- In June, there were no significant cenditions. differences in the mean between age classes I and KvwAHATA (1973) reported that in captive fe- II (P>O,1). The females of age classes IY, V and males of the species the litter size tended to in- YI had the larger number of embryos than in the crease from 5.0 for the first litter to 5.5 for the younger age classes (P 250 NII-Electronic Library Service The EcologicalSocietyEcological Society of Japan Vol. 31, No. 3 JAPANESE JOURNAL OF ECOLOGY Sep., 1981 Table 4` Age vuriations in the number of embryos (mean ± SE). Age classes I Il III IV v VI Number of females examined 1534,8 1774.1 59 925.5 l556.2 1116.1 JuneAugustOctoberJune ± O.24.9 ± O.94.7 ± O.1* ± O.2. ± 02* ± O.15.2 ± O.15.14.5± O.45.2 4.7±O.2* 4.8± 02. ± O.24.9 ± O.24.8 ± O.25.06.1± O.35,6S.O±O.6. 5.4± O.2* to Cictober ± O.1 ± O.1 ± O,2 ± O,1 5.9± O.1 5.4± O.1 'Overwintered female. days, parturition of the fifth litter should occur at 9 or 10 months old, Tlierefore, it that the appears 7 litter size of the captiye females decrease in advenced age. AIso, in C. although the glareoins, June mean number of embryos increased with advanc- 6 h---'"'"'i ing age, it doc reased in femalcs of more than 15 months old (ZEJDA, 1966 ; AM,NNTAEvA, 1974). 5 When the data of the throe months were com- bined, the mean number of embryos was 4.9 for 4mgts female of the year and 5.6 for overwintered fe- males (see Table 1), and the difference betwcen the two values was significant (P yariations were found also in Finland (KALELA, 65g.-stse42August 1957), the Kora Peninsula (KQsHKiNA, 1957), Chukot CYruDiN et al., 1976) and the Shikhote-AIin Mountatins, Primorie (SMiRNov, 1974). It was e.i"=kl" reported that the litter sizc of Microtus montantes +-""R was larger in fernales beginning reporoductive activity at more than 12 weeks old than in those beginning at 6 to 9 weeks old (NEGus & PINTER, October 1965). If this is also the case fbr C. rsijbcanus, the 6 larger number of embryos of overwintered females in June may then be aocounted for. Females born × 5 in the autumn of the preeeding year were deliy- ered of the first iitter in the spring at 6 to 7 months 4 i/vy-:kl-A>s-sc old, while those born in the spring and early sum- mer started reproductive activity at 2 to 3 months old. 23 26 31 36 41 46 ss ss ss 25 30 35 40 45 54g Relationship between the number of embryos and Body weight the body weight of pregnant females Fig. 3. Retationships In the 747 pregnant females weighing from 23 to betweenthe number ofembryos and body weight. Solid circ]e: females of the year, 54 g, 6 body-weight classes were designated. The open c{rcle: overwintered females, vertical bar: mean number ofembryos in each class is shown in SE. Fig. 3. In June, the mean increased with the in- crease in the body weight of the pregnant fernales. In August and October, the females of the year males from June to August, the mean number of showed a slight increase in the mean as the body embryos did not increase in the females of the weight increased, but the overwintered females year, but it decreased in the overwintered fe- showed no variation in the mean. Despite the in- males (Fig, 4). crease in the rnean body weight of pregnant fe- The combined data of the three rnonth period 251 NII-Electronic Library Service The EcologicalSocietyEcological Society of Japan Vol. 31, No. 3 H* th me #k sh Sep,, 1981 Table 5. Relationships betweenthe number of embryos(mean ± SE) and the body weight of preg- nant females. Body weight classes 23-25 g26-30 g31-3S g36-40g 41-4Sg46--54 g Number of fernales examined 254.3 1544.6 2165.0 1955.3 1145.ltO,15.9435.3 Females of the ycar ± O.3 ± O.l5.3 ± O.1S.2 ± O.15,6 ± O,45.8 Overwintered females ± O.24.8 ± 025.1 ± O.l5.4 ± O,25.7 ± O.35,7 Overall feTmales 4.3± O.3 ± O.1 ± O.1 ± O.1 ± O.1 ± O.3 in summer during certain years (UEDA et al., 1966; FuJiMAKi, 1973). T[herefor, if ambient temperature oJ .6o..Iist5tsA.z=4 had a similar effect on the number ofembryos in summer, the docline in the aboye means in Au- gust may have been due to high temperatures dur- oO eoeA ing that summer. Most overwintered fernales are known to attain to 12 montbs old or more in Oc- eJ oA tober, since thc overwintered population is com- posed mainly of animals born in September and October of the preceding year (UEDA et al.l 1966). ' Thus the small number of embryos fbund jn the overwintered females in October may be attrib- 30 35 4eg uted to their advanced age. Body weight The mean for the total numbes of females was Fig. Relationships between the number of embyos 4, 5,9 in June, 4.8 in August and 5.2 in October, and body weight. So]id circle: females of the year, although the difference between the values in Au- open cirele: overwintered females, J: June, A: gust and October was not siginificant (P>O.1). In August,O:October. August, the popuration was composed mainly of animals of age classes I and II, which showed revealed the tendency for the mean to inerease as smaller embryo counts than the other age classes the body weight increased in both the females of (Table 4), and the mean number of embryos from the year and the overwintered females (Table 5). the overwintered females was also small. Thesc In the captive females, the mean litter size tended facts may account for this seasonal trend in all of to inerease with the increase in the body weight the females examined. In Nopporo and Shibecha (KuwAHATA, 1973). A similar phenomenon has (site 38 in Fig. 1), the numbers ofembryos showed also been found in this species in Finland (KALE- a similar tendency to decrease in summer and to LA, 1957). However, these findings differed from increase again in autumn (OTA et al,, 1964 ; KuwA- et small those reported by KuwAHATA (1966), whe did not HATA, 1966).OTA al. (1964)associated the find any relationship between the number of ern- value in summer only with the recruitment of bryos and the body weight of pregnant females. small-sized females showing small embryo counts to the population, Seasonal yariation in the number of embryos ZEJDA (1966) reported that in C. glareolas the May In the females of the year, the mean number of number of embryos was largerin Apriland in August, and it than during the frorn June to September, embryos was 4,8 in June and period then inereased to 5.2 in October (Table 1), The and suggested that this variation was due to some mean of 6.1 for the overwintered females ip June unfavourable conditions resulting frorn a high docreased to 4.8 in August and slightly increased population density. This hypothesis was not to 5.3 in October (Table 1). In August, the mean adopted for the present study because the data different was small in proportion to the mean body weight were obtained from many localitieswith of the two age groups (see Fig, 4). It has been re- population density levels. ported that the reproductive activities of the spe- cies were repressed in areas with high ternperature Variations in the number of emhryos between pri- 252 NII-Electronic Library Service The EcologicalSocietyEcological Society of Japan VoL 31, No,3 JAPANESE JOURNAL OF ECOLOGY Sep,, 1981 Table 6. Variationsin the number of embryos (mean± SE> between primiparous and multiparous femalcs. Females of the yearOyerwintered females Overall females Primi-parousMulti-parousPrimi-parousMulti-parousPrimi-parousMulti-parous Number of femalos examined 2054.8 1694.8 1106.1 2636.0 3155.7 4326.0 JuneAugustOctoberJune ± 024.9 ± O.34.6 ± O.24.7+O,26.3± O.14,8 ± e.l4,9 ± O.14,7 ± O,15,3 ± O,15.2 ± O.25.1 ± O,15.4 ± O,15.4 ± O,15.0 ± O.14.9 ± O.35.8 ± 025.6 ± O.15,3 ± O.1S.3 to October ± O.1 ± O.l ± O.1 ± O.1 ± O.1 ± O.1 miparous and multiparous females ed as pregnant. The females of the year were fbund to be mui- Both the corpora Iutea and the embryos were tiparous in June, which is early in the breeding examined in 439 pregnant fernales. The number of season. The mean numbers ofembryos in both the corpora lutea per pregnant female varied from 2 primiparous and multiparous females are shown to 14 and averaged 6.1. Seasonal variations in the in Table 6. No signMcant differences in the mean number of corpora lutea were similar to the trend were found in any set of the paired samples from for the number of embryos (Table 7), but there the two groups (P>O.1). KALELA (1957) also re- were no significant differences in these values be- ported that these are no apparent differences be tween the two age groups in the respective montbs tween the two groups in this speeies. Under natural (P>O.1). The mean of 6.3 of the number of conditions, the females are known to have more corpora lutea giyen by KuwAHATA (1966) does than 4 litters during their life. Moreover, the difi not diffler significantly from the mean obtained in ferences between the mean litter sizes of sucoessive the present study (P>O.1). litters are very slight, in spite of the trend for the Of the 439 pegnant females, 158 animals, or litter size to inerease from the first to the fourth 36.0 %, showed embrye loss. The rate of females of litters (KuwAHATA, 1973). the year shewjng embryo loss was 40D% in June 36.5 % in August and 43.9 % in October. The cor- Prenatal loss of embryos responding values for the overwintered fernales Comparisons were made between the number were 28.0, 31.9 and 44.1, respectively. And for the of corpora lutea and the number of visible em- total number of females the rate was 29.7% in bryos. The diserepancy between these two values June, 35.2% in August and 43.9% in October. was regarded as the number of prenatal loss of em- The combined data from the three month period bryos, including ,both pre- and postimplantation showed a decline in this rate from 39.9% fbr the losses, sinoe the number of corpora lutea corres- females of the year to 3 1 .6 % for the overwintered ponded to the number of ova oyulated. However, ones ; thus it was clear that seasonal and age varia- this loss did not include the loss ofthe whole litter, tions occurred, However, there was net such an in which case none of the ovulated ova beeame outstanding difference in the rate betwecn the pri- implanted. In this case the femles were not regard- miparous and multjparous females, whiQh was Table 7. Variations in number of corpora lutea (mean± SE) and prenatal mortality (figures in parentheses).the June August October June to October Number of females examined 14562 1625.7 1326.5 4396.1 Females of the year ±O,4(21.8 ± 02(16.3%)5.4± O.2(19,4%)6.2± O.1(18.8%)6.2 %)6.5 Overwintered females ±O.1(6.3)6.4 ± 02(12.7)5,6 ± O.3(15,1)6.4 ± O.1(19.1)6.1 Overa11 females ±e.1(8.6) ±O,1(15.5) ± O,2(18.3) ± O.1(14.0) 253 NII-ElectronicNII-ElectronicMbraryService Library Service The EcologicalSocietyEcological Society of Japan Vol. 31,No.3 H * th ma *ct sk Sep., 1981 Table 8. Relationships between the number of corpora lutea and the number of lost embryos. Prenatal mortality and percentage of embryo loss are also shown. Number of corpora lutea Number of losternbryos 2 3 45678910ll121314 o123456782814852 8518618432101391612281l127443 1115 11 1 13312 1l11 Prenatal mortality o3.74.16.072 11.5IZ5 38.9 35.3 45.5 41.7 46.2 52.4 (%) Percentage of embryoloss O 11.1 12.7 22.7 33.9 45.1S5.6 1oo 93.3 loo 1oo 100 1oo Table 9,Seasonal variations in prenatal mortality. June August October June to October Number of females examined 145 162 132 439 FeTmales of the year 17.9% 14.5% lg.8% t65% Overwinteied females Z6 9,6 12,1 9.0 Overal 1 females 8,1 13.1 17,3 12.9 37.2% and 35.3 %, respeetively. In contrast to the season. As in the rate of embryo loss, the prenata1 findings of the present study, AMANTAEyA (1974) mortality increased with the increasing number of found that the rate was higher in primiparous fe- corpora lutea per pregnant female, showing an males than in rnultiparous ones in C. glareolus. abrupt inerease in thc females having more than8 There was no prenatal loss of embryos in the cerpora lutea (Table 8). The rate of the females females 2 corpora lutea, but the rate of em- having having more than 8 corpora lutea was l1,6 % for bryo loss was 11.1 in the females having 3 cor- % the females of the year, but 5.3 % fbr the overwin- pora lutea, and it then increased as the number of tered females, which explain why there was a highr corpora lutea increased. The rate increased ab- er prenatai mortality in the females of the year. ruptly to 93 or 1oo% in the females more having The combined data from the tlu;ee month period than 8 corpora lutea (Table 8). This phenomenon showed a prenatal mortality rate of 12,9% in con- to correspond seems closely with the faetthat fe- trast to that of KuwAHATA (1966), who reported males of this species have 8 nipp]es. ZEJDA (1968) a rate of 20,1 % with a range of 17% in June to found a similar phenomenon in C glareotus by 33% in August in Nopporo. The reason for the counting the number of resorging embryos. high mortality in Nopporo is not clear. Prenatal mortality is defined as the ratio of the The prenatal mortality mentioned above is the number oflost embryos to that ofcorpora lutea in minimum es timate, because the embryos may have a pregnant female. In this study, the mortality was been affected by postimplantation loss. If con- lower in the overwintered femaleg than in the fe- siderable postimplantation loss occurs during males ofthe year (Table 9). The prenatal mortality pregnancy, the number of embyos is expected to as a whole increased from 8.1 % in June to 17.3% be smaller in the later stages of pregnancy than in in October, because the mortality for overwintered the early stages. The mean number ofembryos was increased =: = females inOctober and becausethere 4.9 (IV 248) fOr small-sized embryes, 5.5 (N was nurnerical a superiority of young voles show- 306) for medium-sized ones and 5.1 (N =t 183) for ing high prenatal mortality later in the breeding254 large-sized ones. TIhis suggests that the postim- NII-Electronic Library Service The EcologicalSocietyEcological Society of Japan VoL 31, No. 3 JAPANESE JOURNAL OF ECOLOGY Sep., 198t plantation loss was very slight if it oocurred. IV Biol., 34: 1-60. Kost{KiNA, T. V. 1957. Comparative ecology KALELA (1957) stated that the postimplantation of thered- backed voles in the northem taiga. Fauna and loss was not important as a factor influencing the Ecol- ogy of Rodents, 5: 3-6S (in Russian with English reproduction rate based on the slight diserepancy summary). in the number of embryos betwecn the early and KuwAHATA, T. 1966. Studies on the population fluctua- later stages of pregnancy. AMANTAEvA (1974) tion of the red backed vole, Clethriononots rnj?)caneLs showed for C. that the rate of resorption glareoins be`VbrdVae CTHoMAs) n. Reproductjve activity. Ann. of embryos was onc tenth of the whole prenatal Rep. Hokkaido Bra, For. Exp. Sta., 1965, 210-236 mortality. (in Japanese with English surnmary). The factors which affected the prenatal mortali- . 1973. 0n the breeding of cage reared red- ty in this study are not knovvn. BRAMBELL & backed vole, Clethrionomys rtij?)canus betUbrditte Exp. Anim., 22 231-236. RowLAND (1936) working with C. glareoins asgo- ClrHoMAs). (Suppl.): Neeus, N. C. & PimeR, A. J. 1965. Litter sizes of ciated the higher embryo loss with a deficientcy of Microtus montanus in the laberatory. J. Mamrn., 46: nutritiye or other substances required for em- 434-43T bryonic development. Another consideration, OTA, K., ABE, H., TAI[ATsu, S. & FuJIKuRA, J. 1964. which is suggested by the difference in the rate of Seasonal changes in the number of cmbryos of embryo loss between the two age groups, is that C7ethibnomys rnj?)canus becijbrdVae in Konsen Dist- embryo Ioss may be causod by partly physiological rict. Zool. Mag., 73 : 383-384 (in Japanese). fernales. imperfectionsinyoung Pol[RovsKII, A. V, & BoL'sHAKov, B. N. 1979. Experi. mental ecology of voles. 147pp. Nauka. Moscow References (in Russian). .}LoRTENKo, L. A., KIsHINsKII, A, A. & CHERNYAVSKII, ABE, H, 1976. Age detamination of Clethriononrys F. B. 1963. Mamrnals of Koryak Mountains. Acade- rt{focancfis betUbr`hae CIIHoMAs). Jap. J. Ecol., 26: my of Sciences, USSR, Moscow (in Russian). 221-227 (in Japanese with English summary). RErMERs, N. E 1959, Sbrex and small rodents of oeder AMANTAEvA, R. A. 1974. Age changes of fbcundity taiga of tbe Baikal tenitory and their role in the life and embryonic mortality in the cornmon red-backed of the forest. Zool. Zhur., 38: 1249-1256 Russiap vole (Clethriononrys glarelous). Zool. Zhur., S3: (in with Eng]ish summary). 1865-1868 an Russian with English sumrnary). , 1966. Birds and mammals of soutbern taiga of "BRAMBELL, F. W. R, & RowLANDs, I. W. 1936. Re- central Siberia, 420pp. Academy ef Sciences, USSR, production of the bank vole (Evotonrys glareoins Moscow (in Russian). ScHREBER) I. The oestrous cycle of the female. Phiols. ' & VoRoNov, G. A. 1963. Insectivores arid Trans., London, B, 226: 71-120. in tbe upper reaches of Lena Riven BRoMLEJ, G. F. & KosTENKo, V. A, 1970. Relation be- rodents Irkutsk tween forest rodents and Korean pine in the forest of (in Russsian). "Small central and southern Shikhote-Alin. ma:n- SMnH, M. H. & McGINNis, J. T. 1968. Relationships of altitude, and size size and mals of Priamurie and Primorie" (ed. BRoMLEi, G. latitude, body to litter Tnean annual of offspring in Peronryseus. E), 5-6S (in Russian). production FuJiMALKi, Y. 1971, Population fluectuations in Clethti- Res. Popul. EcoL, 10: 11S-l26. E. N, 1970. 0n fbcundity of onomys rtijbcanus beceiorziiae. Nonezumi, 101: 3-6 SMiRNov, Al,ottemusspe- ciosus and CZethrienono,s rLij2,c(mus in the middte (in Japanese), "Smal] mammals of and . 1972. Reproductive activity in CVbthriononrys ShikhotbAlin. Priamurie BRoMLEi, G. F.), 160-169 Rus- rtijbeanus bece?)rdiae 1. Regional differences in spring ,Primorie"(ed. (in sian). reproductive activity. Bull. Hokkaido For. Exp. Sta,, 10: 56-67 (in Japanese with English summary>. ,1974,Fecundityofthemouse-likerodentsinthe the Shikhoto-Alin, 2: . 1973. Ditto. 2, Regional differences in sunmier forestsof middle feriologiya, 259-269 Russian with English summary). reproductive activity. Ibid., 11: 121-131 (in Japa- (in nese tvith English surnmary). TAyRovsKII, V. A., EGoRov, O. V., KRIyosHEEv, V. G., . 1975, Ditto. 3. Regional differences in autumn P()pov, M. V. & LABvnN, Yu.V. I971. Mamrnals of 660pp. Nauka, Moscow Rusian). reproductiye activity. Ibid,, 13: 37-4S (in Japanese Yakutiya. (in with Eng}ish sumrnamy), UEDA, M., HIGu( HJ, S., IGARAsHl, B., MmoA, M., JAcKsoN,W.B.I965.LittersizcinrelationtoIatitudein KuwAHATA, T. OTA, K., ABE. H., FunMAKI, Y., two murid rodents, Amer. Midl. Nat., 73 : 245-Z47. FunKuRA, J. & TAIcAyAsu, T. I966. Historical review KALELA, O. 1957. Regulation of repr6duction rate in ofstudies on the Bedford's red-backed vole, Clethrith subarctic popu!ations of the vole CVlethriononrys nonrys rnj2)canus becVbtziiae CTiioMAs). Bull. Goy･ rnjbcanus (SuND,), Ann, Acad. Sci Fennicac, Ser. A,255 For. Exp. Sta., 191 : 1-1oo (in Japanese). NII-ElectronicNII-ElectronicMbraryService Library Service The EoologioalEcological SocietySooiety of Japan Vol ．31， No ．3 日 本 生 態 学 会 誌 Sep． ， 1981 YuDIN B ， S ． KRIvosHEEv V G ＆ B 肌 YAEv V ． ． で 6 8 4 10 ， ， ， ， ， ， G 当年雌 は ， 月 は ．8， 月 は 5．2 で ，季節変化 は 缸 1976，Smali − lsof the north of the F 恥 t． み られなか っ た・ 270pp Nauka Novosibirsk in Russian ． ， （ ）． 4 ．胎児 数 は 齢段 が進 む に し た が っ て 階 増加 し た が ， ZEJDA， J．1966． Litter size 洫 Ciethriono〃 げ 5 gtarθotμs 老齢雌 で は や や 減少 し た ．平均 は 当年雌 で は 4，9 で ，越 − S6hreber1780．Zool．Listy，15： 193 206， 冬雌 の 5，6 よ り小 さか っ た ． ．1968，Astudy on emblyos and newbom of 5 ． の の 妊娠雌 体重が 増す る に し た が っ て 胎児数 は 増 − Ctethrionomys glareolus Sc hreb， Ibid．，17 ：115 126． 加 す る 傾 向 が あ っ た ． ゆ The author was unable to refer to these papcrs 6 ．初回 妊娠 と 2 回 以上 の 妊 娠 と の 間 に 胎児数 の 差 は dir tly． み られ な か っ た ・ 7 ．排卵黄体 数 は 2 〜 14の 範囲 で ，平 均 は 6 ．1 で あ り， 摘 要 そ の 季節変化 は 胎児数の もの に 似 て い た ． 8 ． の の 6 29 ． 出 生前 死 亡 み ら れ た 雌 割 合 は ， 月 7％ ， 1 ．1967〜1974 で エ ズ の 年 に 北海道各地 ゾ ヤ チ ネ ミ 妊 8 月35．2％ ，10月43． 9％ で あ り ，当年雌 で は 39．9％ ，越 つ い べ 娠個体 747 を 採集 し ，胎児数 と 出生前死 亡 に て 調 冬雌 で 31．6％ ， 雌全体 で は 36．0％ で あ っ た ． た ． 9 ． 亡 12 9 で 出生前死 率 は ．％ ， 月別 に み る と， 8 月 〜 〜 2 ．胎児数 は 1 10の 範囲 で ，妊娠例 の 88％は 4 7 8．1％， 8 月13．1％， 10月17．3％ と次第 に 増 加 し ，まtこ ． ． の 範囲 で あ っ た 平均胎児数は 5 3 で ，こ の 値に 地 域差 当年雌 で 16．5％，越冬雌 で 9 ％ で あ っ た ． ， は み られ な か っ t 10，出生前死 亡 の み られ た 雌 の 割合 と出生前死亡 率 は ， 6 3 ．平均胎児数 は ，越冬雌 で は 月 Ic6．0 で あ っ た が ， 黄体数 が 増加す る に し た が っ て 増 加 し ，と く に 黄 体 数 9 ． 8 月ICは 4．8 と減少し， 10月 に は 5 3 とや や 増加 し た ． 以上 の 雌 で 急激に 増加 し た ． 256 一 NII-ElectronicN 工 工 Eleotronio Library Service