J. Mamm. Soc. Japan 18(2) : 53-59 December 1993

A Case of Late Breeding in the kobeae and Its Nest

Naohiko SAGARA and Hisashi ABE* Life Web, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-01, Japan *Laboratory of Applied Zoology, Faculty of Agriculture, Hokkaido University, Sapporo 060, Japan (Accepted 5 December 1992)

Abstract. The presence of the mushroom Hebeloma radicosum, which grows specifically on mole latrines, led to the discovery in the montane area of Kyoto in October 1984, of a mole nest and a case of unusually late breeding in Japanese . The nest was excavated near the latrines under the mushroom, and three juvenile Mogera kobeae were collected in and around the nest. These moles presumably belonged to the same litter, aged between four and six weeks old, and appeared to be almost ready for natal dispersal. This is the first published report of talpine moles at such a developmental stage being collected in autumn, in Japan, at their own nesting site. These juveniles might have been the result of delayed breeding but not a second litter, as the early part of that year, i. e. the mole's normal breeding season, was unusually cold. The nest and its surrounding features are also described.

Key words : Mogera kobeae ; Late breeding ; Nesting site ; Mushroom ; Hebeloma radicosum .

Talpine moles breed, in principle, once a year in spring (Godfrey & Crowcroft, 1960 ; Abe, 1968 ; Gorman & Stone, 1990). The Japanese species Mogera kobeae gives birth to young from April through June (Abe, 1968 ; Yukawa, 1977 ; Miyao, 1983). We report here on the unusually late collection of juvenile M. kobeae in October (1984), at a nesting site which was detected by the fruiting of a particular Hebeloma mushroom species. We also describe the nest and its surrounding features, as there has been little reliable information published on the nesting habits of this species.

Study Site and Methods

The study site was located in the Kyoto University Experimental Forest at Ashiu, Miyama-cho, Kita-kuwada-gun, Kyoto Prefecture. The site was near the confluence of the Kami-tani brook and its branch stream the Iwa-tani, in the uppermost reaches of the Yura River, and at the foot of a hill rising from the terrace on the left bank of the Kami-tani : 35O20'47" N, 135O44'54" E, 670 m altitude, and 35" SSE ground inclination (see map by Sagara et al., 1989). 54 Sagara & Abe The deciduous broad-leaved forest at the site was dominated by Fagus crenata with Quercus crispula subdominant, growing on a brown forest soil (Shidei et al., 1958), derived from Mesozoic parent rocks (Imoto, 1986). Meteorological data at the Choji-dani Station of the Experimental Forest, 1.5 km SE of this site and at 640 m altitude, show that the annual mean temperature (10 : 00) is 11.5 "C (the average for 1938-1955) ; the annual maximum tempera- ture is 29.8 "C (1938-1958) ; the annual minimum temperature is -16.2 "C (1938- 1958) ; the annual precipitation is 2,821 mm (1938- 1958) ; and the maxi- mum snow depth is 218 cm (1938-1958) (Ando et al., 1989). Similar data, shown in Table 2, and referred to in the discussion section, were obtained from the Ashiu Station of the Experimental Forest, 4.8 km SSW of the study site (35'18'19" N, 135O43'14" E, 363 m altitude), because no meteorological data for the years in question (1981-1987) were available from the closer Choji-dani Station. The mushroom Hebeloma radicosum (Basidiomycota : Agaricales) is a good indicator of the presence of mole nests, because it grows and fruits specifically on deserted mole latrines usually situated near nests (Sagara, 1978, 1980, 1989 ; Sagara et al., 1989). A young fruiting body of H. radicosum was found on 1 October 1984, and a second was located 25 cm away from the first on 6 October 1984 (Fig. 1). On 9 October 1984, we dug the ground under these fruiting bodies so as to make a soil profile to show locations of deserted latrines and nest (Fig. 1). In the course of this excavation, a mole was seen in a tunnel. This indicated that the nest, which was still untouched, was in use. Vinyl tubes (4 mm in diameter, 50 cm in length) were quickly inserted into each of three tunnels exposed, and the mouth of each tunnel plugged with soil to prevent evaporation. Chloroform was then injected through the tubes using a 50 ml injection syringe. Following this operation, the sound of mole's movement in the tunnels gradually ceased, then the soil was hurriedly removed to uncover the . The specimens were collected, weighed, and then fixed with 3.7 % formaldehyde. Other measurements were made once the fixed specimens had been preserved in 70 % ethanol at the senior author's laboratory. The nest was also collected, and excavations were continued on 10 and 12 October 1984 in order to observe such aspects as the tunnel system, tunnel size, latrine making, and mushroom colonization.

Results

The Specimens Two specimens were collected from the tunnels close to the nest (Fig. 1) and one from within the nest itself. On the basis of dentition (see Abe, 1967) and body weights (Table I), which were intermediate between those (ca. 100 g) of adult M. kobeae and those (ca. 50 g) of adult M. wogura, the smaller species, in this montane area (see Sagara et al., 1989), they were identified as juvenile M. kobeae. They were presumed to belong to the same litter, because they were similar in age, and because they remained in tunnels in the immediate Late Breeding in Mogera kobeae 55

Fig. 1. Soil profile on 9 October 1984 showing the Mogera kobeae nest under the mushroom Hebeloma radicosum and the young animals anesthetized within their tunnels. N : nest ; E : entrance to the nest ; T : tunnel ; L : deserted latrines colonized by the mycelia of the mushroom. The animals were placed at the very points where they were found dead. Another died in the nest itself. The intervals between the lines on the folding scale equal 10 cm. Fig. 2. The nest collected from the soil profile in Fig. 1 and placed in a plastic bag. R : tree roots enclosing the nest. Bar = 10 cm. Fig. 3. Soil profile on 10 October 1984 after further digging, showing the accompanying smaller nest (S). See Fig. 1 for other symbols. 56 Sagara & Abe vicinity of the nest and did not attempt to leave the nesting site while it was being disturbed. They appeared to be almost fully grown and ready to dis- perse from their natal area. A fourth animal attempted to approach the nesting site a little later on the same day (9 October 1984) but evaded capture. This individual was presumed to have been the mother of the young.

Table 1. Measurements of the young moles collected at their nesting site in Ashiu, Kyoto, on 9 October 1984. Hand length and foot length do not include nail length. Body Head and body Tail Hand Hand Foot weight length length length width length (€9 (mm) (mm) (mm) (mm) (mm)

The Nest and Other Subterranean Features The nest was located between 35 and 50 cm under ground (measured vertically) (Fig. 1). It appeared to have been used for some years, as indicated by the tree rootlets which had already enclosed the nest to absorb nutrients (Fig. 2). Another smaller nest was located at a shallower point (Fig. 3). This nest appeared to have been constructed very recently, because there was no penetration by tree roots and because there was a small molehill of recent origin right above the nest. The tunnels appearing in the soil profiles measured 5.5 x 4.5, 4.6 X 4.0, 6.7 X 5.0, 5.6X4.4, 5.5x4.9, and 4.6x4.1 cm in diameter. The tunnel made by the escaping animal measured 5.0 x 4.5 cm. There was a tunnel beneath the bottom of the nest chamber, but it did not penetrate the nest cavity, unlike the "bolt- holes" made by the europaea (Godfrey & Crowcroft, 1960). The site of the deserted latrines, which had been colonized by the H. radicosum mycelia, was located between 15 and 35 cm below ground (Figs. 1 and 3). A new latrine containing a large deposit of fresh dung was found rather close to the smaller nest, between 4 and 15 cm below ground, although this would not mean that there were no more latrines.

Nest Structure and Materials The larger, older nest, which was being used at the time of digging (Fig. I), was subspherical, constructed of fallen broad-leaves pressed to the wall of the nest chamber. There was only one entrance to the nest, measuring 4.9 x 4.5 cm in diameter. The nest measured 20 x 25 cm in lateral diameter and 15 cm in vertical diameter (Fig. 2). It was partially destroyed during the removal of one of the specimens, but its structure did not seem to be fundamentally different from those previously described (Sagara, 1978,1980 ; Sagara et al., 1989). The leaves used in the nest were mainly of Fagus crenata and Quercus crispula, but some Sasa sp. and other species were also noted. Late Breeding in Mogera kobeae 57 The smaller nest (Fig. 3) was also subspherical with only one entrance, but looser, measuring 10 x 14 cm in lateral diameter and 11 cm in vertical diameter. It contained the same kinds of leaves as did the larger nest, but the leaves used here were in a similar stage of decay as those lying on the ground surface at that time, again indicating that the smaller nest had been constructed very recently.

Discussion

So far as the Talpinae in Japan (Mogera and ) are concerned, this is the first published report of juvenile animals being collected in autumn. They had attained 60-80 % of adult body weight, and were moving in tunnels near the maternal nest. By comparison with information on the growth of young T. europaea (Godfrey & Crowcroft, 1960), it would appear that our specimens were between four and six weeks old, and had not been born before 15 August of that year. This is an unusually late breeding record. The latest record previously published of pregnancy in the Japanese Talpinae was of a female M. kobeae collected on 19 June 1961 which contained small embryos to be born probably in mid- July (Yukawa, 1977). However, other unpublished records indicate that such late breeding, as described here, can sometimes occur : The junior author collected a female M. kobeae with four 22 mm-long (crown-rump length) em- bryos at Kooyama, Gotenba City, Shizuoka Prefecture on 15 July 1991 ; a female M. wogura with three 32 mm-long embryos at Kadota-shinden, Joetsu City, Niigata Prefecture on 16 August 1991 ; and a female M. tokudae with two 18 mm-long embryos at Ichishin, Niitsu City, Niigata Prefecture on 23 August 1991. There is also a record of a female M. kobeae which was collected on 7 August 1959 from Okuwa-mura, Nagano Prefecture and found to have "a large and vascular uterus" indicative of breeding (Abe, 1968). The occasional occurrence of probable second litters in a year has been suggested both for T. europaea (Godfrey & Crowcroft, 1960) and for the

Table 2. Meteorological data at Ashiu, Kyoto, showing the unusually cold weather from winter through spring in 1984. Temperature in "C, snow depth in cm. Observations 1981 1982 1983 1984 1985 1986 1987 Mean air temp. (9 : 00) in Feb. -2.6 -2.2 -1.4 -3.3 0.0 -1.8 0.2 Mean min. air temp. in Feb. -4.6 -4.9 -3.8 -5.9 -2.1 -5.9 -2.5 Max. snow depth in Feb. 100 140 18 199 65 109 86 Days in Mar. with snow cover 22 23 13 31t 12 31 20 Days in Mar. with min. air temp. below zero 24 20 16 30 14 18 23 Mean air temp. (9:OO) in Apr. 8.7 8.7 10.5 7.9 10.1 10.9 11.1 Cumulative temp. from Jan. through May* 511 702 772 473 796 788 983 * : Mean air temperature of each month was multiplied by number of days of that month and the result was summed for the five months. 7 : Further 16 days in April had snow cover. 58 Sagara & Abe

Japanese mole Urotrichus talpoides (Usuki, 1968 ; Imaizumi, 1969 ; Yu- kawa, 1977). It is not known, however, whether the litter discovered in this study was a second litter, or the result of delayed breeding, but the weather data, showing that the normal breeding season was unusually cold in 1984 (Table 2); suggest the probability of the latter. The effect of unusual weather conditions on breeding season has been suggested in reverse for the forest shrew araneus which has been found with unusually early young in Germany in 1975 after the unusually mild winter of 1974-1975 (Kapischke, 1976). Furthermore, although very young (Horikoshi et al., 1967 ; Hanamura & Uematsu, 1981) or adult moles (Sagara et al., 1989) have been collected previ- ously, this is the first record from Japan of young talpine moles, presumably belonging to the same litter and approaching natal dispersal, being collected at the nesting site. This study was originally aimed at the correct identification of the nest itself, as talpine species (M. kobeae, M. wogura and E. mizura) are distributed almost contiguously around the study site (Sagara et al., 1989). The success of anesthetization with chloroform may have been due to the fact that the animals were young and did not attempt to leave the nesting site. The same method, however, has not been successful with active adults. The smaller nest (Fig. 3) seems to have been a temporary dwelling because the mole nest is usually located deeper in the ground, being rather spherical, larger and tighter (Sagara, 1978,1980, unpublished observations ; Sagara et al., 1989). It may have been needed by the growing mole family until dispersal of the young. The presence of only a single entrance to the nest or nest cavity (Sagara, 1989 ; Sagara et al., 1989 ; this paper) may raise doubt about the traditional understanding of the mole's nest as having two entrances (Godfrey & Crowcroft, 1960 ; Gorman & Stone, 1990).

Acknowledgments

We are indebted to : Messrs. Shuji Kobayashi, Koichi Kawamura, and Rei- ichi Miura, students of Kyoto University at the time, for assistance with the field work ; the authorities of Kyoto University Forest for allowing our research work in Ashiu and for providing us with the meteorological data used in Table 2 ; and Dr. Chris Maser, Oregon State University, and anonymous referees for critically reading and improving the manuscript.

References

Abe, H. 1967. Classification and biology of Japanese Insectivora (Mammalia). I. Studies on varia- tion and classification. J. Fac. Agr., Hokkaido Univ., Sapporo, 55 : 191-265. Abe, H. 1968. Classification and biology of Japanese Insectivora (Mammalia). 11. Biological aspects. J. Fac. Agr., Hokkaido Univ., Sapporo, 55 : 429-458. Ando, M., H. Noborio, J. Kubota & S. Kawanabe. 1989. Analysis of the meteorological data in Ashiu (1). Bull. Kyoto Univ. Forests, no. 61 : 25-45 (in Japanese with English summary). Godfrey, G. & P. Crowcroft. 1960. The Life of the Mole. Museum Press, London, 152 pp. Late Breeding in Mogera kobeae 59

Gorman, M. L. & R. D. Stone. 1990. The Natural History of Moles. Christopher Helm, London, 138 PP. Hanamura, H. & Y. Uematsu. 1981. On the teeth of juvenile specimens of two species in the Insectivora. J. Growth, 20 : 15-29 (in Japanese with English summary). Horikoshi, I., Y. Imaizumi & K. Tsuchiya. 1967. On a nest of Mogera wogura wogura at Mitsukaido- shi, Ibaraki Prefecture. J. Mamm. Soc. Japan, 3 : 137-139 (in Japanese). Imaizumi, Y. 1969. Reproduction in the in Niigata Prefecture, Honshu. J. Mamm. Soc. Japan, 4 : 81-86 (in Japanese with English summary). Imoto, N. 1986. Geological features of Ashiu. Contr. Kansai Organiz. Nat. Conserv., no. 12 : 5-12 (in Japanese). Kapischke, H. -J. 1976. Erstes Auftreten und friihe Geschlechtsreife juveniler Waldspitzmause, Sorex araneus L. Milu, 4 : 115. Miyao, T. 1983. Research Report of Wild Animals of Nishiharu-cho. Nishiharu-cho, Nishikasu- gai-gun, Aichi Prefecture, 51 pp. (in Japanese). Sagara, N. 1978. The occurrence of fungi in association with wood mouse nests. Trans. Mycol. Soc. Japan, 19 : 201 -214. Sagara, N. 1980. Not mouse but mole. Trans. Mycol. Soc. Japan, 21 : 519. Sagara, N. 1989. European record of the presence of a mole's nest indicated by a particular fungus. Mammalia, 53 : 301 - 305. Sagara, N., S. Kobayashi, H. Ota, T. Itsubo & H. Okabe. 1989. Finding Euroscaptor mizura (Mam- malia : Insectivora) and its nest from under Hebeloma radicosum (Fungi : Agaricales) in Ashiu, Kyoto, with data of possible contiguous occurrences of three talpine species in this region. Contr. Biol. Lab. Kyoto Univ., 27 : 261-272. Shidei, T., T. Tsutsumi & T. Kimura. 1958. Forest soil of the Kyoto University Forest of Ashiu (No. 1) Bull. Kyoto Univ. Forests, no. 27 : 1-19 (in Japanese with English summary). Usuki, H. 1968. Studies of the Shrew Mole (Urotrichus talpoides) IV. Seasonal reproductive condi- tions and some reflections on breeding cycle. J. Mamm. Soc. Japan, 4 : 7-11. Yukawa, M. 1977. of Hiwa-cho, Hiroshima Prefecture. In Hiwa no Shizen (Hiwa-cho Natural History Museum ed.) pp. 157-180. Hiwa-cho, Hiroshima Prefecture (in Japanese).