Size and Distribution of Home Ranges of the Japanese Shrew-Mole Urotrichus Talpoides

J. Mamm. Soc. Japan 18(2) : 87-98 December 1993

Size and Distribution of Home Ranges of the Japanese Shrew-mole Urotrichus talpoides

Nobuo ISHII

Japan Wildlife Research Center, Bunkyo - ku, Tokyo 113, Japan (Accepted 23 September 1993)

Abstract. Size and spatial distribution of home ranges of the Japanese shrew- mole Urotrichus talpoides were studied by live-trapping in a mature mixed (broadleaved and coniferous) forest in Chiba Prefecture, Honshu. During the non-breeding season, no significant differences in home range size were found between sexes. The home ranges of breeding males were significantly larger than those of non-breeding males, while no significant differences were found in range size between non-breeding and breeding females. During the non- breeding season, home ranges were mutually exclusive among individuals of the same sex, but overlapped extensively with those of the opposite sex. In the breeding season, male ranges largely overlapped each other. Female ranges also overlapped each other, but to a lesser extent. The tolerance between the sexes during the non-breeding season is unusual in comparison with other mole and shrew species, whose individual ranges are exclusive to each other irrespective of sex.

Key words : Japanese shrew-mole ; Urotrichus talpoides ; home range size ; spatial organization.

The shrew-moles Urotrichus, Neurotrichus and Uropsilus, though talpids (Fam- ily Talpidae), are less well adapted to the fossorial way of life than are the typical moles. The life-style of the shrew-moles is, therefore, of interest from the view point of comparative ecology, however, detailed information on the population ecology of shrew-moles has not previously been available. In this paper seasonal changes in the size and distribution pattern of the home ranges of the Japanese shrew-mole Urotrichus talpoides are described.

Study Area and Methods

Study area The study was carried out in Compartment 24 of the Tokyo University Forest located on the Boso Peninsula, Chiba Prefecture, Honshu. A live-trapping plot, consisting of 88 trapping stations set ten meters apart in an 8 x 11 array encompassing 0.7 ha, was established in a mature mixed forest of 51.6 ha surrounded by young broadleaved forests and conifer plantations. The domi- nant trees were Abies firma, Quercus acuta, Q. glauca, Q. salicina, and Castanop- sis cuspidata var. sieboldii. The understory was composed mainly of Eurya 88 Ishii japonica, Camellia japonica, Cinnamomum japonicum, Dendropanax trifdus, and Illicium religiosum. The undergrowth consisted mainly of Trachelospermum asiaticum, Maesa japonica, Arachniodes sporadosora and Gleichenia japonica.

Trapping procedure One Sherman live-trap (SFA type) baited with a mixture of chopped cheese and oatmeal was placed at one opening of a burrow system near each station. Live-trapping was conducted once a month from June 1977 until December 1978, and then biweekly between January and July 1979. Trapping was operat- ed for five consecutive nights monthly until December 1978, and then for three to five nights in each trapping session thereafter. The traps were set in the evening and checked at midnight and again in the morning, until October 1978. To avoid trap mortality, from November 1978 onwards, I checked the traps three times each night at four-hourly intervals. The traps had to be closed during the day otherwise jungle crows Corvus macrorhynchos disturbed them. Shrew-moles were individually marked by toe-clipping ; their sex, reproductive condition, weight, age, and the point of capture were recorded before their release. Sexing of live shrew-moles was difficult (except in the breeding season), but could be done by physically checking for the presence of a penis, using the finger tips. Further details of methods for estimating reproductive condition are given by Ishii (1982). The current year's young were identifiable because they had milk teeth or only slightly worn teeth and they could be easily distinguished from adults that had overwintered and had more worn teeth.

Methods of analysis Home range size was estimated using two methods : (1) the minimum range area (Stickel, 1954), and (2) the probability ellipse (Jennrich & Turner, 1969 ; Mazurkiewicz, 1969). The minimum range area was obtained by connecting the outermost capture sites of an individual and measuring the area inside. Using the probability ellipse, the area was calculated to contain 95 percent of expected captures. To examine the distribution pattern of home ranges, I mapped the capture sites of each individual as a minimum range area. Only those individuals captured at more than three different sites were included. In addition, the degree of range overlap (DRO) was calculated among the individuals of the same sex and between the sexes using the following equation : DRO=100 x CAoICAh where Ah is the range area of an individual (holder) concerned, and Ao the area occupied by other individuals (invaders) within the holder's range. Also, social interactions were considered when two individuals were captured simultaneous- ly with one trap (double captures). Home Range of Shrew-mole

Results

Trapping success Shrew-moles were easily captured using Sherman live-traps. During the course of the study, 85 shrew-moles (49 males and 36 females) were captured and marked individually. Between June 1977 and October 1978, however, 15 individuals died of starvation in the traps. After November 1978, when traps were checked every four-hours, trap mortality was reduced to just one case.

Home range size To determine the number of captures needed to calculate home range size, I plotted range size, calculated by the minimum area method, as a function of the number of consecutive captures for several individuals having high fre- quencies of recapture within a constant reproductive condition. Some of the results are shown in Fig. 1. On the basis of those results, about 20 captures was established as the necessary minimum for calculating actual home range size for observing comparison with other species, and set 10 captures was regarded as the minimum for observing the size differences between the sexes and between the seasons of this study. This compromise was unavoidable due to data limitation. The calculation was only made for those individuals whose ranges were entirely within the trapping area.

CONSECUTIVE CAPTURES

Fig. 1. Change in home range size plotted against consecutive captures for five individuals. The range size was calculated as the minimum range area. Breeding condition is given in parentheses after each individual's number ; N = non-breeding, B = breeding.

Home range sizes were calculated separately for the breeding and non- breeding periods. Males in the study area became sexually mature in early February, and active males decreased rapidly during May. Mature females were observed in February and March, pregnant females in March and April, and lactating females in April and May (Ishii, 1982). During the non-breeding season, no significant difference was found between the range sizes of males and females (Mann-Whitney U-test: the minimum range area, U = 11 ; the probability ellipse, U = 13). The home range of breeding males was, however, significantly larger than that of non-breeding males (the minimum range area, U = 9, p < 0.05 ; the probability ellipse, U = 1, p <0.01). Six males were captured 10 or more times both as non-breeders and as breeders, and in five cases the breeding home range size was the larger of the two. In contrast, no significant difference was found in range size between non-breeding and breeding females (the minimum range area, U = 5 ; the probability ellipse, U =2), though female #69 enlarged her home range during the breeding season. There was no significant difference between male and female range sizes during the breeding season (the minimum range area, U= 4 ; the probability ellipse, U = 3). Home range sizes of individuals that were captured 10 or more times within a constant reproductive condition (non-breeding or breeding) are listed in Table 1, and home range size statistics are given in Table 2.

Table 1. Home range sizes (m2) calculated using two different methods for individuals captured 10 or more times. The number of captures= n. Non-breeding Breeding Individual No. Min. range 95%.prob. Min. range 95% .prob. n area ellipse area ellipse Male # 59 74 77 83 96 99 101 105 105* 116

Female # 43 55 69 72 80 81 - * different period Home Range of Shrew-mole Table 2. Mean home range sizes (m2)with standard deviations (SD) as estimated for individuals captured 10 or more times and those captured 19 or more times. The sample size = n. Min. range area Prob. ellipse n Mean SD Mean SD Individuals captured 10 or more times Non-breeding Males 10 1160 560 3537 1128 Females 4 1563 539 4700 2056 Total 14 1275 566 3869 1468 Breeding Males 6 2825 1396 8729 2670 Females 3 1450 540 6304 2197 Individuals captured 19 or more times Non-breeding Males 5 1510 607 3899 1513 Females 4 1563 539 4700 2056 Total 9 1533 542 4255 1705 Breeding Males 3 3933 520 10120 2403

Distribution pattern of home ranges During the non-breeding season, male ranges more or less overlapped each other, but were exclusive at least between resident individuals which remained until the beginning of the breeding season. During the breeding season, male ranges overlapped extensively as they expanded their ranges. Female ranges showed little overlap during the non-breeding season, especially among residents, with this tendency being more distinct than that shown among males. During the breeding season female ranges tended to overlap to a lesser extent than male ranges. Male and female ranges overlapped throughout the year, and during the non-breeding season there were some cases in which one male and one female occupied almost identical areas. For example, in the non- breeding season of 1977-78 male #77 and female #55, and in 1978-79 male #96 and female #72, and male #I05 and female #69 were such pairs. After the breeding season, among males, the ranges of the current year's young and overwintered adults overlapped, whereas the ranges were exclusive among the individuals of the same age group. Among females, the home ranges of the current year's young were exclusive and they were also distinct from the ranges of overwintered adults which had ceased breeding activity. The minimum area ranges were mapped separately for males and females during the seasons of 1977 through 1979 (Fig. 2). Table 3 lists the degree of range overlap (DRO). Double captures occurred five times during the study (twice in March, twice in April and once in December), and were always a combination of one male and one female. Ishii

MALES FEMALES

NON-BREEDING SEASON (SEP. 1977 - JAN. 1978)

NON-BREEDING SEASON (SEP. 1978 - JAN. 1979)

BREEDING SEASON (FEB. - EARLY MAY 1979) Home Range of Shrew-mole

NON-BREEDING SEASON (MID MAY - JUL: 1979)

Fig. 2. Spatial distribution of minimum area home ranges. Home ranges are drawn with broken lines for non-breeding individuals which disappeared before the breeding season and for breeding individuals which disappeared during the first half of the breeding season (by the end of March). Asterisks indicate individual born during the preceding breeding season.

Table 3. Degree of range overlap among individuals of the same sex and between sexes. "Residents" refers to non-breeding individuals which remained until the beginning of the breeding season, and refers to breeding individuals which remained during the first half of the breeding season.

Period

Non-breeding Season Sep. 1977 - Jan.1978 Residents All individuals Sep. 1978 - Jan. 1979 Residents All individuals Mid May - Jul. 1979 Current year's young All individuals Total Residents* * All individuals Breeding Season Feb. - Apr. 1978 Residents 0.0 26.7 0.0 0.0 All individuals 20.4 17.5 25.9 28.1 Feb. - Early May 1979 Residents 54.4 49.1 68.0 95.9 All individuals 84.3 68.6 88.8 98.5 Total Residents 48.0 43.5 60.0 72.3 All individuals 69.5 54.3 '74.2 78.7 * M, Male ; F, Female. ** Not including the current year's young. Ishii

Discussion

Home range size The two different methods for range size calculation gave strikingly different estimates. The values, especially for the breeding season, might have been underestimated since the trapping area was relatively small. However, the relative differences in range size between sexes and seasons showed clear tendencies, and the estimates could be compared with others obtained using the same methods. Home range sizes of other mole and shrew species are sum- marized in Table 4.

Table 4. Average home range sizes of mole and shrew species (m2). Note that the estimation method differs between species as described in the text. Range size (m2) Species Habitat Sex Weight (g) breedingNon- Breeding Talpa europaea Woodland M 110 F 85 Pasture M 110 F 85 Neurotrichus gibsii T 10 Sorex monticolus M - F - T 7 Sorex vagrans M - F - T 6 Sex : M, Males ; F, Females ; T, Total.

For the European mole Talpa europaea, Stone and Gorman (1985) calculated home range sizes using the restricted polygon method, which is similar to the minimum area method. Average home range size of American shrew-mole Neurotrichus gibbsii was calculated from M. L. Hawes' data, using the probability (95 %) ellipse method (Harestad & Bunnell, 1979). Hawes (1977) used the same method for the shrews. During the non-breeding season, no significant differences were observed between the range sizes of male and female Urotrichus talpoides. This may be related to the lack of remarkable sexual differences in body weight. During the breeding season, however, males considerably increased the size of their ranges, while female ranges remained essentially the same size. As in U. talpoides, the range size of female Talpa europaea does not vary seasonally (Corbet & Harris, 1991), however, during the non-breeding season, males occupy ranges about twice as large as those of females, and they increase three-fold during the breeding season. Among the shrews, Hawes (1977) found no significant differences in the range sizes between the sexes in the non- Home Range of Shrew-mole 95 breeding season, but with the onset of reproductive activity range size increased significantly, with males enlarging their ranges to a greater extent than females did. Regarding the actual size of home ranges, as expected from the differences in body weight, the estimates for Urotrichus talpoides (about 16 g) are mid-way between those for Talpa europaea and the Sorex species, and are almost equal to those of Neurotrichus gibbsii (Table 4, sources of body weight : Ishii, 1982 ; van Zyll de Jong, 1983 ; Corbet & Harris, 1991). The range size of T. europaea, however, appears to be surprisingly small considering its weight, perhaps as a consequence of three-dimensional habitat use. Generally home range size has been thought to be correlated with body weight, food type, food distribution and the way in which food is obtained (McNab, 1963 ; Harestad & Bunnell, 1979 ; Mace et al., 1983). Unlike T. europaea and the Sorex species, due to the tolerance between the sexes, each individual of U. talpoides is not a sole user of food resources available within their home ranges during the non-breeding season. This phenomenon may have an effect on range size, in as much as each individual is likely to require larger home range than if individuals hold exclusive territories irrespective of sex. Furthermore, the methods used to calculate home range sizes vary among the studies cited, and for precise examination, additional information is needed.

Spatial pattern The area that an individual traverses in its normal activities is generally referred to as its home range, and if the area is defended, then it is called a territory (Burt, 1943). In this study, since no direct observation of behavior was made, the presence of territories must be judged from the spatial distribution of the capture sites. Individuals were considered to be territorial when their home ranges were mutually exclusive. During the non-breeding season, home ranges of U. talpoides were mutually exclusive among resident individuals of the same sex, especially among females. Between sexes, however, home ranges overlapped extensively, and some bisexual spatial associations were observed perhaps indicating that there may be a positive male-female bond. The relative distribution of home ranges during the non-breeding season suggests that individuals become territorial among individuals of the same sex, but not between sexes. Territoriality appears to be more remarkable among females than males. With the onset of reproductive activity, male ranges were found to enlarge and extensively overlap each other, whereas female ranges were found to overlap to a lesser extent. Home ranges of the current year's young usually do not overlap those of other individuals of the same sex, suggesting that the young may establish territories soon after weaning. The occurrence of double captures suggests that mature males and females may pair and move together, especially during the breeding season. The degree of tolerance between the sexes of U. talpoides during the non- breeding season is unusual when compared with that of other mole and shrew 96 Ishii populations. For example, during the non-breeding season, the individual ranges of T. europaea are largely exclusive irrespective of sex (Corbet & Harris, 1991 ; Haeck, 1969 ; Stone & Gorman, 1985). Of the shrews Sorex araneus, S. minutus (Michielsen, 1966), S. uagrans, S. monticolus (Hawes, 1977) and S. unguiculatus (Inoue, 1988), during the non-breeding season (or among sexually immature individuals), each individual is solitary and defends a territory against other individuals, irrespective of sex. For a semi-fossorial species, the short-tailed shrew Blarina breuicauda, Platt (1976) found that the population contained both resident and nomadic components with the residents occupying fixed ranges that overlapped slightly during the non-breeding season. Tolerance between the sexes during the non-breeding season has been observed in an aquatic talpid, the Pyrenean desman Galemys pyrenaicus (Stone & Gorman, 1985) and the white-toothed shrew Crocidura russula (Cantoni & Vogel, 1989). After the breeding season (in June and July), usually a pair of G. pyrenaicus (male and female) share an essentially linear home range along a stream that largely excludes others. C. russula during winter (non-breeding season), by contrast, share large overlapping home ranges. The spatial distribution of U. talpoides during the breeding season is essentially similar to that of other mole and shrew species, though it may be unique that female ranges overlap more during the breeding season than in the non-breeding season. Male T. europaea expand their ranges during the breeding season to the point where they largely overlap those of other males and those of females, while female ranges remain relatively constant throughout the year (Haeck, 1969 ; Stone & Gorman, 1985). In both sexes of S. araneus, S. minutus, S. uagrans and S. monticolus, territoriality breaks down with the onset of reproductive activity (Michielsen, 1966 ; Hawes, 1977), though Buckner (1969) stated that female S. araneus continue to maintain territories throughout the breeding season. Inoue (1991) showed that in the large-clawed shrew Sorex unguiculatus overlapping of male home ranges occurs more extensively than of females, and he also showed that male ranges may overlap several female ranges. In B. brevicauda (Platt, 1976), individuals of the same sex have non- overlapping ranges, although there is some overlap between the sexes during the breeding season. Regarding C. russula, the females become territorial in ' the breeding season and share their nests with only one male, thus range overlap was significantly greater between, than within the sexes (Cantoni & Vogel, 1989). The tolerance between the sexes of U. talpoides during the non-breeding season, may be related to breeding biology. Territoriality, in this species, appears to become weaker or disappears during the breeding season, thus its significance seems unrelated to reproduction; its value may be in defending food resources during the remainder of the year. During the breeding season territoriality would hinder the males' efforts to maximize reproductive poten- tial by reducing their chances of encountering receptive females, and for females which are in the midst of pregnancy and lactation territoriality may be too costly in energetic terms. Females might hold small breeding territories, Home Range of Shrew-mole 97 but these cannot be revealed by live-trapping. It remains unclear as to whether tolerance during the non-breeding season is beneficial for both or either sex. It is similarly unclear why territoriality is absent, or becomes weak during the breeding season. To solve these issues, we would need a thorough quantitative cost-benefit analysis of territoriality in U. talpoides and the study of social organization in other related species.

Acknowledgments 1

I am grateful to K. Tachibana for his invaluable suggestions and encour- agement during the study. I thank the personnel of the Tokyo University Forest in Chiba for their kind support in the field, and I would also like to thank F. Bunnell, D. Chitty, C. Krebs, T. Inoue and an anonymous reviewer for provid- ing helpful comments on earlier drafts of this paper.

References

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