Quick viewing(Text Mode)

Food Habits of the Japanese Sable Martes Zibellina Brachyura in Eastern Hokkaido, Japan

Food Habits of the Japanese Sable Martes Zibellina Brachyura in Eastern Hokkaido, Japan

Mammal Study 28: 129–134 (2003) © the Mammalogical Society of

Food habits of the Japanese Martes zibellina brachyura in eastern , Japan

Takahiro Murakami Division of Environmental Conservation, Shari Town Office, Shari-cho, Hokkaido 099-4192, Japan

Abstract. To analyze the seasonal variation in the diet of the Japanese sable Martes zibellina brachyura, 193 and 20 stomachs, collected in eastern Hokkaido from 1998 to 2002, were examined. The Japanese sable proved to be omnivorous, taking various food items including , , , , , , and crustaceans. Mammals were the commonest food items throughout the year, with Clethrionomys spp. (frequency of occurrence 56.5%), Siberian Tamias sibiricus (19.3%) and wood mice Apodemus spp. (14.6%), most often found in feces. Insects appeared mainly in summer (48.8%) and less often in other seasons (9.3% on average). materials, chiefly fruits, were found mainly in autumn (45.7%) and winter (68.4%) but were rare in spring (5.1%) and summer (1.3%). These results suggest that the Japanese sable depends mainly on mammalian prey, but also takes other food items, probably to compensate for fluctuations in abundance. Maintaining natural habitats, which provide various food resources, is thus important for conservation of the Japanese sable.

Key words: conservation, food habits, Japanese sable, Martes zibellina brachyura.

The food habits of various of have been The sable M. zibellina occurs across , , described, including for the Martes and Japan, and is similar in size to the already americana, which occurs throughout mentioned. Although Bakeyev and Sinitsyn (1994) (Murie 1961), the stone marten M. foina, occurring from described the diet of the sable in Russia, theirs was not a to central (Pandolfi et al. 1996), the quantitative study, furthermore, their research was con- marten, M. martes, ranging from to ducted only in coniferous forest in Russia. Buskirk et al. west Asia (Clevenger 1993), and the M. (1996) studied the diet of the sable in mixed coniferous melampus, which occurs throughout Japan and southern and deciduous forest in China, but only during the win- (Tatara and Doi 1994; Nakamura et al. 2001). ter. Thus, information on the food habits of the sable in These studies have revealed that martens are generally mixed forest throughout the year has been lacking. The omnivorous, but that the composition of their diet varies purpose of this research, therefore, was to study the year with species. Mammals are the dominant food of the round diet of the Japanese sable M. z. brachyura, in American marten (Murie 1961) and the pine marten Hokkaido, northernmost Japan. (Clevenger 1993), while wild fruits predominate in the The Japanese sable is categorized as Data Deficient diet of the stone marten (Pandolfi et al. 1996) and the (DD) in the IUCN Red List (Hilton-Taylor 2000), mainly Japanese marten (Tatara and Doi 1994; Nakamura et al. because of concerns over competition for food and 2001). However, reviews of marten feeding ecology by habitat with the Japanese marten, which has been intro- Clevenger (1994) and Martin (1994) have indicated that duced into Hokkaido. Describing the food habits of the there is geographic variation in food habits even within Japanese sable and comparing them with those of the the same species. Thus, the food habits of each species Japanese marten is, therefore, an important first step in should be evaluated by studies throughout their distribu- evaluating whether competition between these two tion. species is likely or not. This information will help to

E-mail: [email protected] 130 Mammal Study 28 (2003)

Fig. 1. Map of the study area (dark gray portion). The estimated distribution in the Hokkaido mainland of M. zibellina is shown in white, and that of M. melampus in , based on Murakami and Ohtaishi (2000). Open circles indicate where carcasses used for stomach analysis were found. decide the of the Japanese sable. chipmunks Tamias sibiricus, Siberian flying squirrels Pteromys volans, mountain Lepus timidus, bats, Study area birds, amphibians, reptiles, insects and other inverte- brates. The study area (approximately 3,500 km2) is located in Four other sympatric mustelids occur in the study eastern Hokkaido (43°–44°50’N, 144°–145°50’E, Fig. 1). area, these are the Japanese Mustela itatsi, the Most of the samples were obtained in the intensive study M. erminea, the M. nivalis and the area (approximately 50 km2, Fig. 1), where the annual introduced American M. vison. Although the intro- mean temperature is 6.1°C (Monthly mean temperatures duced Japanese marten also occurs now in Hokkaido, its range from –7.1°C to 19.4°C). The annual mean precipi- current distribution is limited to the central and southern tation is 1,102.8 mm and the annual maximum part of the island (Murakami and Ohtaishi 2000, Fig. 1). depth in each winter during the study period ranged from 65 cm to 112 cm. Materials and methods The predominant vegetation consists of mixed forest including: todo fir Abies sachalinensis, Mongolian oak Feces of Japanese were collected along trails, Quercus mongolica var. grosseserrata, Erman’s streams and sable tracks on the snow in the intensive Betula ermanii and various maples Acer spp. At eleva- study area from 1998 to 2002. One fecal sample was tions above 500–600 m, the Japanese stone pine Pinus defined as one cohesive lump of droppings. Sable feces pumila is dominant. were searched for on foot on a total of 50 days by one to The potential prey species of the Japanese sable in five persons. The total distance surveyed (calculated eastern Hokkaido include: shrews Sorex spp., voles from a map) was 243.1 km ranging in altitude from sea Clethrionomys rufocanus, C. rutilus, and C. rex, wood level to 1,300 m. Surveys were made on 18 days in mice Apodemus argenteus, A. peninsulae, and A. specio- spring, covering 75.3 km, 12 days in summer covering sus, Eurasian red squirrels Sciurus vulgaris, Siberian 74.5 km, nine days in autumn covering 42.0 km, and on Murakami, Food habits of the Japanese sable 131

11 days in winter covering 51.3 km. (14.6%), sika deer Cervus nippon carrion (6.3%), and Feces were identified by their size, shape, smell Siberian flying squirrels (4.2%) were also taken. Voles (Tatara and Doi 1994) and partial sequences of mito- comprised the major part of the diet in spring (62.7%), chondrial DNA (Murakami 2002). In to evaluate summer (57.5%) and autumn (54.3%). In winter, al- the accuracy of species identification by smell, blind though the percentage occurrence of voles declined, it tests repeated 100 times were undertaken using six feces was still high (31.6%). Sika deer occurred in the diet (two each from the Japanese sable, the , mainly in spring (13.6%) and winter (15.8%). and the ). During these tests I identified Insects, chiefly beetles, mainly occurred in summer 98% of the samples correctly. In contrast, the success (48.8%), while plants, chiefly Chinese gooseberries rate of species identification by mitochondrial DNA par- spp. and crimson glory vine coignetidae, tial sequences was only 2.6% (Murakami 2002). occurred in autumn (45.7%) and winter (68.4%). As the In order to complement the results of fecal analysis, remains of these plant species in fecal samples consisted stomachs of Japanese sables were collected from mainly of seeds or pericarps, it is presumed that the sable carcasses provided by sub-prefectural offices of the fed mainly on their fruits. Hokkaido government, by road management agencies, It was not possible to identify to species the remains of museums, and wildlife researchers from 1998 to 2002. amphibians or reptiles, although these involved at least The sampling localities of these carcasses are shown in one kind of and one kind of . Several fish figure 1. bone fragments appeared in one fecal sample, but it was Feces and stomach contents were washed through not possible to identify the species. 5 mm and 1 mm sieves, and the remains were identified Of the total of 20 stomach samples obtained from to the narrowest taxonomic level possible. The shape carcasses found in the study area from 1998 to 2002, of teeth and the cross section of hairs were used for four were obtained in spring, eight in summer, four in mammals, feathers for birds, the shape of teeth and bones autumn, and four in winter. The frequency ratio of three for reptiles and amphibians, bones and scales for fish, food categories (mammals, non-mammals, and plants) wings and other organs for insects, exoskeletons for detected by stomach content analysis was 15, 7, 4, and crustaceans, and seeds of plants, were all used to identify did not differ from the ratio detected by fecal analysis the food remnants in the feces. Samples collected during (158, 72, 33) (G-test, df = 2, P > 0.90). However, some 1998–2002 were pooled and the percentage occurrence food items, such as shrews and squirrels, identified in of food items in each season was calculated. If even one fecal samples were not detected in stomach samples. hair or scale appeared in a fecal sample that counted as one record. Spring was defined as the month March to Discussion May, summer as June to August, autumn as September to November and winter as December to February. Mammals, followed by insects and fruits, were found to be the major food items eaten by the Japanese sable in Results east Hokkaido. Among them, voles were so frequently taken that they alone make mammals the main food of A total of 193 fecal samples and 20 stomachs were sables. Although the relatively small number of fecal collected. Fifty-nine fecal samples were collected in samples in winter might have led to an underestimation spring, 80 in summer, 35 in autumn, and 19 in winter. In of the significance of some food items such as fruits, the winter, it is likely that feces were missed because of importance of voles in the diet is incontrovertible. How- regular snow falls. Fecal analysis revealed that the diet ever, populations are known to fluctuate seasonally. of the Japanese sable consisted mainly of mammals Yoneda (1982), for example, found that numbers (occurring in 81.9% of the fecal samples), insects in his study area near the Shiretoko Peninsula followed (26.9%) and plants (17.1%, Table 1-a). Whereas birds a particular characteristic trend; i.e. numbers were (5.7%), reptiles (1.6%), crustaceans (1.6%), amphibians lowest in April or May, increased towards summer, and (1.0%) and fish (0.5%) were less frequently eaten then decreased towards winter. This seasonal trend is (Table 1-a). common among Clethrionomys species, although C. Among mammals, voles occurred most frequently rufocanus experiences two population peaks in summer (56.5%), but Siberian chipmunks (19.3%), wood mice and autumn. The numbers of wood mice (also an impor- 132 Mammal Study 28 (2003)

Table 1. Frequency of occurrence of each food items in (a) feces and (b) stomachs. The values in parenthes represent percentage occurrence. (a) Spring n =59 Summer n = 80 Autumn n = 35 Winter n =19 Total n =193 Mammals 52 (88.1) 68 (85.0) 24 (68.6) 13 (68.4) 158 (81.9) Sorex spp. 4 (6.8) 5 (6.3) 1 (2.9) 1 (5.3) 11 (5.7) Clethrionomys spp. 37 (62.7) 46 (57.5) 19 (54.3) 6 (31.6) 109 (56.5) Apodemus spp. 11 (18.6) 14 (17.5) 1 (2.9) 2 (10.5) 28 (14.6) Tamias sibiricus 12 (20.3) 18 (22.5) 5 (14.3) 2 (10.5) 37 (19.3) Sciurus vulgaris 1 (1.7) 0 (0.0) 0 (0.0) 1 (5.3) 2 (1.0) Pteromys volans 3 (5.1) 2 (2.5) 1 (2.9) 2 (10.5) 8 (4.2) Cervus nippon 8 (13.6) 1 (1.3) 0 (0.0) 3 (15.8) 12 (6.3) Other mammals 0 (0.0) 1 (1.3) 0 (0.0) 0 (0.0) 1 (0.5) Birds 3 (5.1) 8 (10.0) 0 (0.0) 0 (0.0) 11 (5.7) Reptiles 1 (1.7) 1 (1.3) 1 (2.9) 0 (0.0) 3 (1.6) Amphibians 1 (1.7) 1 (1.3) 0 (0.0) 0 (0.0) 2 (1.0) Fish 0 (0.0) 0 (0.0) 1 (2.9) 0 (0.0) 1 (0.5) Crustaceans 2 (3.4) 1 (1.3) 0 (0.0) 0 (0.0) 3 (1.6) Insects 8 (13.6) 39 (48.8) 5 (14.3) 0 (0.0) 52 (26.9) Coleoptera spp. 8 (13.6) 38 (47.5) 5 (14.3) 0 (0.0) 51 (26.6) Hymenoptera spp. 0 (0.0) 1 (1.3) 0 (0.0) 0 (0.0) 1 (0.5) Plants 3 (5.1) 1 (1.3) 16 (45.7) 13 (68.4) 33 (17.1) Actinidia spp. 1 (1.7) 0 (0.0) 14 (40.0) 0 (0.0) 15 (7.8) Vitis coignetiae 0 (0.0) 0 (0.0) 3 (8.6) 3 (15.8) 6 (3.1) Other plants 2 (3.4) 1 (1.3) 1 (2.9) 10 (52.6) 14 (7.3)

(b) Spring n = 4 Summer n = 8 Autumn n = 4 Winter n = 4 Total n =20 Mammals373215 (75.0) Clethrionomys spp.252110 (50.0) Apodemus spp.10012 (10.0) Tamias sibiricus 00011 (5.0) Pteromys volans 02103 (15.0) Cervus nippon 00011 (5.0) Birds01012 (10.0) Fish10012 (10.0) Insects03003 (15.0) Plants01214 (20.0) Actinidia spp.01102 (10.0) Vitis coignetiae 00101 (5.0) Other plants00011 (5.0) tant food item for the Japanese sable), also showed a Summer feces often contained large numbers of seasonal trend similar to that of Clethrionomys voles in beetles and other insects, coinciding with their peak eastern Hokkaido (Yoneda 1982). abundance (Tsukada and Nonaka 1997), indicating that Autumn and winter feces commonly contained large sables readily eat insects when they are available. volumes of seeds and pericarps of fruits. Fruits may be The food items found to have been eaten by the an important food when voles and wood mice are scarce, Japanese sable in Hokkaido were very similar to those especially in winter. Fruits are available for the Japanese identified in Russia by Bakeyev and Sinitsyn (1994). sable throughout the winter, because some fruits remain Both populations depend on small mammals, fruits and on their vines, while some of the fallen fruits remain insects, but there are some differences between Russia under the snow. and Japan. For example, pine seeds Pinus spp., one of Murakami, Food habits of the Japanese sable 133

Table 2. A comparison of the food habits of Martes species based on fecal analyses. In order to compare, percentage occurrences were calculated for four categories. The values in parentheses are based on different methods from this study.

Species Source Study area Mammals Birds Insects Plants n M. zibellina This study Norhtern Japan 81.9 5.7 26.9 17.1 193 Buskirk et al. 1996i China (40.3) (8.6) (0.0) (26.2) 221 M. americana Murie 1961 North America (65.4) 4.7 0.5 (31.5) 384 (Voles) (Crategus) M. martes Clevenger 1993 Spain 39.6 31.7 44.1 40.4 1180 M. foina Pandolfi et al. 1996ii Italy (18.6) (4.1) (16.8) (55.0) 89 M. melampus Tatara and Doi C, 1994iii Southern Japan (19.5) (9.3) (2.2) (55.6) 975 Nakamura et al. 2001 Central Japan 20.8 7.1 48.2 76.8 168 Notes: i) Feces collected only in winter ii) Number of each food item/Total number of items iii) Relative frequenciy of occurrences (Recalculated from their results) the major foods of the sable in Russia, did not occur in Japanese marten, then those now occurring sympatrically the Japanese sable diet, despite their abundance in the with the Japanese sable in Hokkaido may show similar study area. The Japanese sable may prefer voles and food habits, and thus may compete with the sable for fruits to pine seeds. Bakeyev and Sinitsyn (1994) also food. described the sables in the as often eat- In the IUCN Red List (Hilton-Taylor 2000), the status ing salmon Salmonidae spp., whereas the occurrence of of the Japanese sable is categorized as DD (Data Defi- fish was extremely low in the Hokkaido study, perhaps cient) because of the lack of information on the possible because of the low availability of salmon in the study competition with the Japanese marten. Thus, a compara- area. In China, mammals and plants (fruits) were found tive study of the food habits of both species in an area of to be the major food items of sables in winter (Buskirk sympatry is urgently needed. et al. 1996), as has been confirmed in this study. The This study has revealed clear seasonal variation in the annual food habits of the Japanese sable may perhaps diet of the Japanese sable, with mammals being the most resemble those of the sable in China more closely than in important food item throughout the year, but with insects Russia. commonly taken in summer, and fruits often taken in The omnivorous food habits of the Japanese sable autumn and in winter (Table 1). Seasonal changes in were similar to other Martes species, such as the Ameri- the availabilities of these food items are likely to be can marten, the pine marten, the stone marten, and the the cause of the seasonal differences in the diet of the Japanese marten. However there were several differ- Japanese sable. The percentage occurrence of sika deer ences among their diets (Table 2), with the Japanese carrion among food items also showed seasonal change, sable, for example, being less dependent on plants than being highest in winter (15.8%) and in spring (13.6%). other martens are (Table 2). Recently, mass mortality of Sika Deer has been reported In Japan, the previously allopatric Japanese marten in eastern Hokkaido (Uno et al. 1998). Indeed, large depends more on fruits than does the Japanese sable numbers of deer carcasses were observed mainly from (Table 2). This difference may be related to differences winter to spring during this study, representing an in habitat characteristics. Studies of the Japanese marten abundant potential food resource for the Japanese (e.g. Tatara and Doi 1994, Nakamura et al. 2001) have sable. However, the frequency of occurrence of deer been conducted in central and southern Japan, areas remains in fecal samples was lower than that of voles. which have a wide range of fruits and lighter snowfalls As Cumberland et al. (2001) have pointed out, research (Nakayama et al. 2000) than the Hokkaido study area. based on percentage occurrences may underestimate the Pandolfi et al. (1996) studied relationships between importance of larger prey, which may contribute sig- latitude and winter food composition among several nificantly to caloric intake. In order to reveal whether stone marten populations in Europe and found that the Japanese sables depend more on deer carcasses or not, southern populations tended to consume more fruits than the caloric intake of each food item should be evaluated the northern ones. If this relationship is applicable to the (Cumberland et al. 2001). Alternatively, the low occur- 134 Mammal Study 28 (2003) rence of deer remains in fecal samples may be attribut- Buskirk, S. W., Ma, Y., Xu, L. and Jian, Z. 1996. Diets of, and prey able to the feeding behavior of the Japanese sable. If selection by, sables (Martes zibellina) in northern China. Journal of Mammalogy 77: 725–730. they prefer to catch live prey, then scavenging Clevenger, A. P. 1993. Pine marten (Martes martes Linne, 1758) from deer carcasses would remain low. In addition, the comparative feeding ecology in an island and mainland popula- digestibility of each food item also affects the results. tion of Spain. Zeitschrift Saugetierkunde 58: 212–224. Other species were identified in the diet from their Clevenger, A. P. 1994. Feeding ecology of Eurasian pine martens and stone martens in Europe. In (S. W. Buskirk, A. S. Harestad, M. G. hard remains, but if deer meat alone were eaten from Raphael and R. A. Powell, eds.) Martens, Sables, and Fishers carcasses, then the percentage occurrence of deer would Biology and Conservation. Pp. 326–340. Cornell Univ. Press, be underestimated. In order to evaluate the importance New York. Cumberland, R. E., Dempsey, J. A. and Forbes, G. J. 2001. Should of deer carcasses for Japanese sable in east Hokkaido, diet be based on biomass? Importance of larger prey to the further investigation considering feeding behavior and American marten. Wildlife Society Bulletin 29: 1125–1130. prey digestibility is needed. Hilton-taylor, C. 2000. 2000 IUCN Red list of Threatened Species. The availability of various food items, mainly voles IUCN, Gland, Switzerland and Cambridge, UK, 61 pp. Martin, S. K. 1994. Feeding ecology of American martens and fishers. and insects, and alternative foods such as fruits in In (S. W. Buskirk, A. S. Harestad, M. G. Raphael and R. A. autumn, and deer carcasses in winter and spring, is Powell, eds.) Martens, Sables, and Fishers Biology and Conser- necessary for Japanese sables to be able to cope with vation. Pp. 297–315. Cornell Univ. Press, New York. Murakami, T. 2002. Species identification of mustelids by comparing the fluctuating abundance of each food item. Therefore, partial sequences on mitochondrial DNA from fecal samples. maintaining natural habitats, which provide a range of Journal of Veterinary Medical Science 64: 321–323. food resources, is important for the conservation of the Murakami, T. and Ohtaishi, N. 2000. Current distribution of the sable and introduced Japanese marten in Hokkaido. Mammal Study 25: Japanese sable. 149–152. Murie, A. 1961. Some food habits of the marten. Journal of Mammal- Acknowledgments: I wish to thank: N. Ohtaishi for his ogy 42: 516–521. helpful suggestions. I am also grateful to H. Abe, M. Nakamura, T., Kanzaki, N. and Maruyama, N. 2001. Seasonal changes in food habits of Japanese martens in Hinode-cho and Asano, M. Takahashi, M. Aida, K. Yamada, S. Yorifuji, Akiruno-shi.Tokyo. Wildlife Conservation Japan 6: 15–24 (in K. Yanaoka, A. Ookawa, A. Imai, M. Hamamoto, T. Japanese with English summary). Yamamoto, A. Fujita, A. Anagawa, K. Miyoshi, K. Nakayama, S., Inokuchi, M. and Minamitani, T. 2000. Seeds of Wild Plants in Japan. Tohoku Univ. Press, Sendai (in Japanese). Waseda, A. Ichimoto and H. Matsudate who supported Pandolfi, M., Marinis, A. M. D. and Petrov, I. 1996. Fruit as a winter field studies. My thanks also go to Y. Hayashi, T. feeding resource in the diet of stone marten (Martes foina) in east Takenaka, K. Ito, Y. Fukuda, the Japan Highway public central Italy. Zeitschrift fur Saugetierkunde 61: 215–220. corporation, the Shiretoko Museum, the Shiretoko Tatara, M. and Doi, T. 1994. Comparative analysis on food habits of Japanese marten, and in the Tsushima Nature Center, and the Kushiro sub-prefectural office of islands, Japan. Ecological Research 9: 99–107. Hokkaido, for providing sable carcasses. I am also Tsukada, H. and Nonaka N. 1997. Foraging behavior of red grateful to N. Nakamura and M. A. Brazil who improved vulpes schrencki utilizing human food in the Shiretoko National Park, Hokkaido. Mammal Study 21: 137–151. the manuscript. Uno, H., Yokoyama, M. and Takahashi, M. 1998. Winter mortality pattern of Sika deer (Cervus nippon yesoensis) in Akan National Park, Hokkaido. Mammalian Science 38: 233–246 (in Japanese References with English summary). Yoneda, M. 1982. Prey preference of the red , Vulpes vulpes Bakeyev, N. N. and Sinitsyn, A. A. 1994. Status and conservation schrencki Kishida (: ), on small . of sables in the commonwealth of independent states. In (S. W. Applied Entomology and Zoology 17: 8–19. Buskirk, A. S. Harestad, M. G. Raphael and R. A. Powell, eds.) Martens, Sables, and Fishers Biology and Conservation. Pp. 246– Received 9 April 2003. Accepted 6 October 2003. 254. Cornell Univ. Press, New York.

Top View