In optimal foraging theory, animals should select appropriate choices based on their foraging behavior, such as length of searching, processing, and choice of feeding patches/food items (Stephens and Krebs 1987). Studying foraging strategies, thus, is useful for understanding the life history and fitness of target animals, especially predators, whose prey move freely. Conversely, in the applied field, food choice and environmental background are clues for considering conservation plans, especially for endangered species. In recent decades, studies on carnivorous mammals and meta-analyses orienting environmental determinants of their feeding have been conducted. For example, diets of Eurasian otters (Lutra lutra) were more diverse in the south as compared to the north (Clavero et al. 2003). Wildcats (Felis sylvestris) mainly feed on rabbits at lower latitudes and on rodents in boreal regions (Lozano et al. 2006). Martens (Martes spp.) prefer vegetable matter in the south, and mammals and birds in the north (Zhou et al. 2011). Finally, the red fox (Vulpes vulpes) feeds on lagomorph and invertebrates in the south, and on rodents and fruits in the north (Díaz-Ruiz et al. 2013). These examples imply that feeding strategy of carnivores is plastic and observed feeding behavior in each habitat would reflect food environment there.

Japanese badgers (Meles anakuma), an endemic mustelid in Japan, are distributed on three main islands: Honshu, Shikoku, and Kyushu (Kaneko 2009). Previous studies on their diet have emphasized a strong dependency on earthworms (e.g., Yamamoto 1991; Tanaka 2002; Kaneko et al. 2006; Hijikata et al. 2020), but case studies on the food habits of Japanese badgers in northern Japan, in which deciduous/conifer forests are dominant, are limited. In addition, previous studies have not examined the feeding strategy of badgers. In this study, we examined the food habits of Japanese badgers in northern Japan, focusing on their temporal variation and their relationship with the availability of the main diets. We then discuss the feeding strategy of Japanese badgers with reference to present and past studies.

Materials and methods

Fecal sample collection and its analysis

Fecal sampling was conducted every month between June 2020 and December 2021, except for winter and early spring (between January and March 2021) when the badgers were hibernating (Tanaka 2006). The collected fecal samples were sieved through 0.5-mm meshed sieve with 1 L of tap water. After washing, the residue was retrieved from the sieve and stored in a plastic bottle with 70% ethanol until analysis. The tap water used for washing feces was used to analyze earthworm availability (see a later section).

We evaluated the dietary composition of each fecal sample using two methods: 1) the point-frame method (Stewart 1967; Takatsuki et al. 2007) and 2) frequency of occurrence (FO).

Point-frame method: A tap water was spread over a glass slide fit with a 20 × 50 mm metal frame and covered with a 1 mm grid, and the residue was spread onto the glass slide (Hijikata et al. 2020). Using an optical microscope (Nikon Eclipse Ei, Tokyo), the points of the grids covered by the fragments were counted. A total of 200 points were counted, and the proportions in the fecal composition (%) of the food categories were calculated. Food items were visually categorized into eight types: 1) fruits (including seeds), 2) herbaceous plants, 3) woody leaves, 4) arthropods (mainly insects), 5) insect larvae, 6) mammals and birds, 7) reptiles, and 8) unknowns. For fruits, before analyzing we identified plant species in whole samples based on the size and shape of the detected seeds with reference to Nakayama et al. (2000) and Kominami et al. (2016). By the point-frame method, we evaluated the temporal change in the feeding of target food items by showing monthly and yearly changes in their proportions.

Frequency of occurrence (FO): To compare the dietary composition of Japanese badgers in Ishinomaki with those in other study sites, we calculated FO for each item, calculated as follows:

It is difficult to detect earthworm remnants in feces because they are broken into small pieces during mastication (Battisti et al. 2019; Tsukada et al. 2021). Therefore, we employed a different method to evaluate earthworm feeding by the badgers, modified from Seki et al. (2015): we kept water used for washing fecal samples for 15 min, and picked up its sediments (approximately 1 ml) using a dropper. We then placed a piece of the sediment on a slide-glass with 1 mm aperture grids. Under the optical microscope, we counted the number of earthworm chaetae within a 1 cm² area (representing 100 grid cells). We checked 10 areas for each sample (i.e., 10 cm² in total) and represented the number of earthworm chaetae as the degree of feeding.

Results

During the study period, we collected 169 fresh fecal samples (n = 84 in 2020 and 85 in 2021). The dietary composition (in terms of FO) of Japanese badgers in Ishinomaki during the study period is shown in Table 1 and Appendix 1. Among the eight food items, four showed a higher FO (> 50%): fruits, arthropods (mainly insects), earthworms, and woody leaves. We detected the seeds of 14 different plant species in badger feces (Appendix 2).

Conversely, food items with higher proportions in point-frame methods were fruits (average in the study period: 71.9%) and arthropods (13.7%). The percentage of woody leaves (9.8%) was lower for their FO. Therefore, we conducted detailed analyses of three food items, fruits, arthropods, and earthworms, whose chaetae were detected throughout the year (annual mean: 3.1/10 cm²).

Figure 1 shows monthly changes in the feeding of a) fruits, b) arthropods, and c) earthworms (in terms of number of chaetae). For each food item, we found significant effects of month, year, and the month × year interaction (P < 0.05) (summarized in Appendix 3). The percentage of fruits was consistently high (> 50%), and it increased in fall, especially in 2021 (Fig. 1a). The percentage of arthropods was higher during summer and lower in fall. The decrease during fall was much greater in 2021 (Fig. 1b). There was a significant negative correlation between the proportion of arthropods and fruits in feces (Spearman's rank correlation test: r_s = –0.818, P < 0.001). Earthworms were detected every month, but the degree of feeding varied between years; during summer in 2021, the number of earthworm chaetae was greater, whereas during fall, an opposite trend was found (Fig. 1c). We found no significant correlations between earthworm feeding and the proportions of the other two main diets (fruits: r_s = –0.032, P = 0.905; arthropods: r_s = 0.139, P = 0.609).

Fig. 1.

Monthly change in a) mean (± SD) percentages of fruits (including seeds), b) mean (± SD) percentages of arthropods, and c) mean (± SD) number of earthworm chaetae (Number / 10 cm²). Open circles and filled circles represent 2020 and 2021, respectively.

Fig. 2.

Monthly changes in mean (+ SD) availability of a) fruits (including seeds), b) arthropods (represented by ground prowling insects), and c) earthworms. The same symbol represents significant differences between months (Bonferroni post-hoc tests).

Fig. 3.

Results of the Spearman's correlation analyses: relationships between availability (fruits [left], ground prowling insects [center], and earthworms [right]) and feeding: a) % points of fruits (including seeds), b) % points of arthropods, and c) earthworm chaetae in feces.

Figure 2 shows the monthly changes in food availability for 2021. The availability of fruits was greater during summer and fall (Fig. 2a), whereas that of insects was the highest during summer (Fig. 2b). Finally, the availability of earthworms had two peaks: spring and fall (Fig. 2c).

The results of the correlation analyses between food availability and the degree of feeding are summarized in Fig. 3. None of the combinations showed significant correlations (P > 0.05).

Discussion

Through fecal analyses, we found that Japanese badgers in Ishinomaki mainly fed on fruits, arthropods, and earthworms. This composition was similar to that of Japanese badgers in other study sites (Mt. Nyugasa: Yamamoto 1991; Yamaguchi: Tanaka 2002; Hinode: Kaneko et al. 2006; Kozu: Hijikata et al. 2020, see details in Table 1), which shows that the badgers are omnivorous. In addition to this similarity, we found several regional variations in feeding; badgers in Ishinomaki, Hinode, and Kozu frequently fed on woody leaves, herbaceous plants, and fibers, respectively (Table 1). The reason why specific population relied on specific types of food is unclear, but it may be attributed to differences in fauna, flora and/or soil characteristics among the study sites. Therefore, the food environment can affect food choices of Japanese badgers.

Table 1.

Diet composition (in terms of frequency of occurrence, FO) of Japanese badgers (Meles anakuma) in five study sites

Woody leaves and herbaceous plants were detected in fecal samples of the badgers throughout seasons, but nutritional implication of the non-fruit plant materials for the badgers is unknown (Cleary et al. 2009). The badgers might ingest them inadvertently while foraging for prey in soil (Neal et al. 1988).

This study demonstrated that dietary composition, in terms of FO, of Japanese badgers to be common among study sites. In the case of European badgers, earthworms and vegetable matter were the dominant food types, but the relative importance of the former was greater at higher latitudes (Goszczyński et al. 2000). Studying such geographical food patterns would be necessary to understand the feeding strategy of Japanese badgers.

Previous studies have emphasized earthworm feeding by Japanese badgers (e.g., Yamamoto 1991), but we should also pay attention to their frugivorous nature: we found seeds of 14 different plant species. From the seed dispersal background, defecation in latrines implies that ingested seeds are gathered in small areas. This would affect the initial stage of seed fitness differently than seeds dispersed by sympatric frugivores such as bears (Koike et al. 2011), martens (Tsuji et al. 2016), raccoon dogs (Sakamoto and Takatsuki 2015), and macaques (Tsuji and Su 2018).

The badgers in Ishinomaki fed mainly on arthropods during the summer, and fruits and earthworms throughout the year. Considering inter-yearly difference in diets, in 2021, percentage of fruits in fall increased, while that of earthworms and insects in this season decreased. These results imply that the main food items of the badgers are fixed, but their relative contribution can be changed inter-yearly, likely due to inter-year differences in food availability.

The three main diets were constantly consumed across seasons, and we found no relationships between fruit availability and feeding on the main diets. Similarly, Roper (1994) reported that European badgers' diet contained a constant proportion of any food over the study period and did not make a functional response. These findings imply that badgers should be viewed as either generalist or opportunistic feeders. This is different from other mustelids, such as martens, whose diet composition promptly changes in response to temporal fluctuations in fruit/vertebrate availability (e.g., Jędrzejewski et al. 1993).