Tsuji, Yamato

Mammal Study

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Title Seed Dispersal by Japanese Macaques (Macaca fuscata) inWestern Tokyo, Central Japan: A Preliminary ReportAuthor(s)Tsuji, YamatoCitationMammal Study (2011), 36(3): 165-168Issue Date2011-09URL http://hdl.handle.net/2433/197179Right© the Mammalogical Society of JapanType Journal ArticleTextversionpublisherKyoto UniversityMammal Study 36: 165–168 (2011) © the Mammalogical Society of Japan Short communicationSeed dispersal by Japanese macaques (Macaca fuscata) in western Tokyo, central Japan: a preliminary reportYamato TsujiPrimate Research Institute, Kyoto University, Aichi 484-8506, JapanJapanese macaques, Macaca fuscata, play an importantrole in dispersing seeds of plants in both warm and cooltemperate forests in the Japanese archipelago (e.g.,Yumoto et al. 1998; Otani 2003; Tsuji et al. 2011a).  Thefrugivorous diet of the macaques, which was recordedby direct observation of their foraging behavior (e.g.,Maruhashi 1980; Tsuji et al. 2006) or indirect fecalanalyses (e.g., Hayashi 1992; Koganezawa 1996) impliesthat they act as seed dispersers everywhere in Japan.  Inorder to evaluate a species’ role as a seed disperser, itis essential to examine which plant species and/orhow many seeds they actually disperse (Otani 2003).However, in central Japan (Kanto and Tokai Districts),which is one of the core habitats of Japanese macaques(Muroyama and Yamada 2010), there are few study siteswhere enough information about seed dispersal charac-teristics of macaques: list of plant species whose seedsare dispersed, rate of seed appearance, life form com-position, seed size, number of seeds dispersed at once,number of plant species per feces, and intact rate.  Thus,in this study I preliminary report results of the analysisof fecal samples of macaques collected along an intercityforest path in western Tokyo, central Japan.  I then com-pare the results with those of previous studies conductedin other sites in order to address the uniqueness of charac-teristics of seeds detected from feces of the macaques inwestern Tokyo.Materials and methodsFecal sampling was conducted along the BonboriForest Path (36°N, 139°E, 400–500 m a.s.l.) betweenHachioji City and Akiruno City in Tokyo.  The vege-tation at the study site is dominated by deciduous–coniferous mixed natural forest, as well as plantedconiferous forest species such as Cryptomeria japonicaand Chamaecyparis obtusa (Nakamura et al. 2001; Tsujiet al. 2011b).I collected all amount of feces of the macaques bywalking or cycling (less than 10 km·hr–1) surveys alongthe forest path on clear days (number of collected feces:1–12).  I conducted these surveys at least once a monthbetween July 2007 and July 2008 (23 surveys in total,and I found at least one feces at 10 out of 23 surveys).  Idiscriminated the feces of the macaques from those ofsympatric canids (red fox Vulpes vulpes and raccoon dogNyctereutes procyonoides) and of mustelids (Japanesemarten Martes melampus and Japanese weasel Mustelaitatsi), on the basis of their shape, content, and size.Feces were washed through a 0.5-mm-mesh sieve andany seeds remaining in the sieve were identified andcounted.  Seed identification was based on Nakayama etal. (2000).  According to Tsuji et al. (2011a), I classifiedthe identified species into four life forms: tall trees (≥5 min height), shrubs (<5 m), vines, and herbaceous plants.I measured the longest axis (a1), second longest axis(a2), and third longest axis (a3) of 10 randomly selectedseeds for each plant species to the nearest 0.05 mm usinga vernier caliper (Tsuji et al. 2011b).  For Berchemiaracemosa, I only measured five seeds for each dimensiondue to a dearth of seeds in my samples.  From averagedvalues, I calculated the mean cubic diameter (MCD) ofseeds (Tsuji et al. 2011a).All data analyses were carried out using the statisticalsoftware R. 2.9.1 (R Development Core Team 2009).For all analyses, significance levels (α) were set at 0.05.Results and discussionA total of 52 fecal samples were collected during thestudy period.  Considering the small sample size, Idivided the whole year into three seasons, not fourseasons: spring and summer (March to August), fall(September to November), and winter (December toFebruary).  Seed dispersal characteristics discussedbelow are based on this classification.E-mail: ytsuji@pri.kyoto-u.ac.jpMammal Study 36 (2011)166In total, 84.6 % (44/52) of feces contained seedsconsisting of 20 plant species: 7 high tree species, 4shrub species, 5 vine species, and 4 herbaceous plants(Tables 1 and 2).  Percentage of freshy-fruit species inmy study site (80.0%) was similar to other study sitesexcept for Kinkazan Island (Table 2).  Rate of seedappearance in spring and summer, fall, and winter were100.0% (10/10), 87.1% (27/31), and 63.6% (7/11), respec-tively, and did not change seasonally (chi-square test,χ2 = 0.50, df = 2, P = 0.778).  This result was differentfrom that in Kinkazan Island in which the rate of dis-persal event was greater in summer and fall and lower inwinter (Tsuji et al. 2011a).Numbers of plant species detected in spring andsummer, fall, and winter were 9, 14, and 5, respectively.Among them, seeds of Actinidia arguta (Actinidiaceae)appeared frequently in all seasons.  In spring and sum-mer, seeds of Ilex macropoda (Aquifoliaceae), Akebiasp. (Lardizabalaceae), and two herbaceous plant species(Poaceae) appeared several times.  In fall and winter,seeds of non- A. arguta species appeared less frequently.In fall, seeds of cultivated Diospyros kaki (Ebenaceae)and Citrus junos (Rutaceae) sometimes appeared (Table1).  Seeds of Vitis sp., those were found from feces ofthe macaques in the cool temperate region (Hayashi 1992;Otani 2003), were rarely found in this study site.The mean number of seeds in a single fecal samplewas 341.8 ± 405.6 (±SD, n = 44).  Number of seeds insingle fecal samples in spring and summer, fall, and win-ter were 314.3 ± 484.4, 438.0 ± 388.9, and 10.1 ± 11.3,respectively (Table 1), and significantly changed season-ally (Kruskal-Wallis test, χ2 = 14.95, df = 2, P < 0.001).Table 1. Seasonal changes in mean ± SD number of seeds obtained from fecal samples of the Japanese macaques at Bonbori Forest Path, centralJapan from 2007 to 2008Species Life formMCD (mm)b(mean ± SD)Number of seeds/feces (mean ± SD)Spring and Summer(Mar–Aug)Fall(Sep–Nov)Winter(Dec–Feb)n = 10 n = 31 n = 11Actinidia arguta vine 2.64 ± 0.24 535.3 ± 879.6 (3) 504.4 ± 374.3 (23) 11.0 ± 14.1 (2)Ilex macropoda high tree 4.64 ± 0.28 317.0 ± 284.6 (3) — —Akebia sp. vine 5.59 ± 0.23 256.0 ± 11.3 (3) 1.0 (1) —Poaceae species A* herbaceous 3.17 ± 0.27 12.0 ± 10.5 (3) — —Actinidia polygama vine 1.61 ± 0.19 10.0 (1) — —Poaceae species B* herbaceous 2.75 ± 0.35 7.5 ± 9.2 (2) — —Polygonaceae sp.* herbaceous 2.49 ± 0.27 7.0 (1) 13.3 ± 12.7 (2) 3.0 ± 1.4 (2)Berchemia racemosa vine 2.96 ± 0.32 5.0 (1) — —Rubus sp. shrub 1.60 ± 0.07 1.0 (1) — —Ilex pedunculosa shrub 4.22 ± 0.08 — 27.0 ± 36.8 (2) —Diospyros kakiahigh tree 9.24 ± 0.36 — 18.3 ± 23.4 (3) —Eurya japonica shrub 1.94 ± 0.22 — 13.0 (1) —Aphananthe aspera high tree 3.47 ± 0.62 — 12.0 (1) —Celtis sinensis high tree 6.14 ± 0.50 — 8.5 ± 9.2 (2) —Citrus junosahigh tree 11.83 ± 1.60 — 7.0 ± 7.3 (4) 5.5 ± 0.7 (2)Stachyurus praecox high tree 1.64 ± 0.11 — 2.0 ± 1.4 (4) 2.5 ± 0.7 (2)Sorbus sp. high tree 4.40 ± 0.15 — 2.0 (1) —Amphicarpaea sp.* herbaceous 3.77 ± 0.36 — 1.7 ± 1.2 (3) 8.7 ± 11.6 (3)Viburnum dilatatum shrub 5.05 ± 0.29 — 1.0 (1) —Vitis sp. vine 3.98 ± 0.24 — 1.0 (1) —unidentified — 1.0 (1) 1.0 (1)Total number of seeds 314.3 ± 484.4 (10) 438.0 ± 388.9 (27) 10.1 ± 11.3 (7)# Species detected/feces 1.7 ± 1.3 (10) 1.9 ± 0.7 (27) 1.7 ± 1.0 (7)Species are arranged in decreasing order of the mean seed number.  n means number of collected fecal samples.  MCD: mean cubic diameter.Figures in parenthesis mean number of fecal samples containing seeds of given species.aCultivated species.bFrom Tsuji et al. (2011b) except for Berchemia racemosa.*Not fleshy-fruited species.Tsuji, Seed dispersal by Japanese macaques 167Further, Scheffe’s Post-hoc tests showed that mean seednumber in fall was significantly greater than that in win-ter (P < 0.05).  Obtained seasonal pattern in seed numberwithin the feces was clearly attributed to the greaternumber of Actinidia arguta seeds in fall, and such clearseasonal changes in seeds in a single fecal sample havebeen also found in other study sites in cool temperateregion: Shimokita Peninsula (Otani 2003), Kashima(Otani 2003), Hakusan mountains (Hayashi 1992), andKinkazan Island (Tsuji et al. 2011a).  On the other hand,on Yakushima Island belonging to the warm temperateregion, much number of seeds of Ficus spp. were dis-persed for longer period (7–8 month per year), anddegree of seasonal change is known to be low (Yumotoet al. 1998).  From the viewpoint of this, seasonality inseed dispersal in western Tokyo seemed similar tomacaques inhabiting the cool temperate zones, in spite oftheir warm temperate habitat.The mean (±SD) number of plant species whose seedswere detected in a single fecal sample was 1.8 ± 0.9,which was lower than corresponding values in otherstudy sites: Yakushima Island (2.8 ± 1.4, Otani andShibata 2000), Shimokita Peninsula (1.9 ± 0.8, Otani2003), Kashima (2.4 ± 1.5, Otani 2003), and KinkazanIsland (2.0 ± 0.9, Tsuji et al. 2011a) (Table 2).  I cannotclearly explain the reason of the small value in my studysite, but there is a possibility that effects of previousforestation and/or existence of the paved path loweredthe diversity of available plant species at Bonbori, whichthen affected the result.  On the other hand, number ofseed species in single fecal samples in spring and sum-mer, fall, and winter were 1.7 ± 1.3 (n = 10), 1.9 ± 0.7(n = 27), and 1.7 ± 1.0 (n = 7), respectively, and did notchange seasonally (Kruskal-Wallis test, χ2 = 1.62, df = 2,P = 0.444).  Again, this result was different from that inKinkazan Island in which the seed species in single fecalsamples was greater in summer and fall and lower inwinter (Tsuji et al. 2011a).Seed size (as MCD) ranged from 1.6 mm to 11.8 mmwith a mean (±SD) of 4.2 ± 2.6 mm (Tables 1 and 2).Seeds of two cultivated species, Diospyros kaki andCitrus junos were both approximately 10 mm in diameter.The annual mean MCD in this study was greater thanthose in other study sites: Yakushima Island (2.5 ± 1.7,Otani and Shibata 2000), Shimokita Peninsula (2.7 ± 1.2,Otani 2003), Kashima (2.3 ± 1.1, Otani 2003), andKinkazan Island (3.0 ± 2.0, Tsuji et al. 2011a) (Table 2),even when I omitted two large-seeded cultivated speciesfrom the analysis (3.4 ± 1.4).  Further, maximum MCDin this study was also greater than those in other studysites (Table 2).  These implied that the macaques in west-ern Tokyo potentially disperse a wider range of seedsthan the macaques in other habitats.  However, furtherdiscussion without data regarding composition of avail-able fruits is difficult.  On the other hand, in future analy-sis, we should also consider the effects of other factorsthat we did not consider in this study, such as fruit pulpproperties (e.g., texture and chemistry), and shape ofTable 2. Regional variation in characteristics of seeds detected from feces of Japanese macaquesStudy site Yakushima Bonbori Kashima Kinkazan ShimokitaClimate zone W W C C CSampling period 1995–2004 2007–2008 2000–2001 2000–2009 2000–2001# Fecal samples 132 52 107 1294 75# Feces contained seeds (%) 131 (99.2) 44 (84.6) 99 (92.5) 747 (57.7) 59 (78.7)# Identified plant species 33 20 18 35 12Life-form composition (%)High trees 13 (38.2) 7 (35.0) 3 (16.7) 11 (30.6) 1 (8.3)Shrubs 11 (32.4) 4 (20.0) 7 (38.9) 5 (13.9) 3 (25.0)Vines 9 (26.5) 5 (25.0) 6 (33.3) 5 (13.9) 7 (58.3)Hemi-parasites 0 (0.0) 0 (0.0) 0 (0.0) 1 (2.8) 0 (0.0)Herbaceous plants 0 (0.0) 4 (20.0) 2 (11.1) 13 (36.1) 1 (8.3)# Freshy-fruit species (%) 31 (91.2) 16 (80.0) 16 (88.9) 20 (55.6) 11 (91.7)MCD (Mean ± SD) (mm) 2.5 ± 1.7 (n = 12) 4.2 ± 2.6 (n = 20) 2.3 ± 1.1 (n = 15) 3.0 ± 2.0 (n = 35) 2.7 ± 1.2 (n = 11)Range 1.1–6.4 1.6–11.8 1.2–4.1 0.8–10.8 1.2–4.1# Species/feces (Mean ± SD) 2.8 ± 1.4 (n = 131) 1.8 ± 0.9 (n = 44) 2.4 ± 1.5 (n = 99) 2.0 ± 0.9 (n = 747) 1.9 ± 0.8 (n = 59)References Otani (2005) This study Otani (2003) Tsuji et al. (2011a) Otani (2003)C: cool temperate zone, W: warm temperate zone, MCD: mean cubic diameter of seeds.Mammal Study 36 (2011)168seeds, on defecated seed size.Evidence of seed destruction was obtained only forCeltis sinensis: several cracked seeds of this relativelylarge-seeded species were found in fecal samples.  Thisfinding indicates that macaques in my study site act notonly as seed dispersers, but also sometimes as seeddestroyers of some (perhaps large-seeded) plant spe-cies.  Tsuji et al. (2011a) showed that intact rate of seedswas negatively correlated with the seeds’ MCD.  Infuture, with more fecal samples, we should test whethersuch relationship to be applicable in my study site.In western Tokyo (and perhaps, in central Japan), sim-ilar to other study sites, Japanese macaques dispersedseeds of high tree, shrub, vine, and herbaceous species inevery season, though there were several main plant spe-cies, like Actinidia arguta.  Several dispersal characteris-tics shown by the macaques at Bonbori, such as rate ofseed appearance and life form composition, were inter-mediate between those in cool and warm temperateregion (Table 2).  This seemed a reflection of environ-mental inclination, like vegetation.Acknowledgments:  I thank Mr. E. Kanda and T.Tatewaki for their assistance during fieldwork, Mrs. T.Harasaki of Gifu University and volunteer students fromAzabu University for their assistance in fecal analysis.  Ialso thank Dr. S. Takatsuki for his advice regarding seedidentification, Dr. K. Matsubayashi for his financialsupport, and Dr. M. A. Huffman and two anonymousreviewers for their constructive comments on an earlierdraft of this paper.  Part of this research was supportedby the Environment Research and Technology Develop-ment Fund (D-1007) of the Ministry of the Environment,Japan.ReferencesHayashi, T. 1992.  Sap fruit seeds in Japanese monkey’s droppingsof Jadani Valley, Mt. Hakusan, Ishikawa Prefecture—on seedsof Vitaceae and Actinidiaceae—.  Bulletin of Hakusan NatureReserve Center, Ishikawa Prefecture 19: 29–41 (in Japanese withEnglish summary).Koganezawa, M. 1996.  Seasonal changes on food habits of Japanesemonkeys in Nikko, central Japan.  Bulletin of UtsunomiyaUniversity Forest 32: 1–16 (in Japanese with English summary).Maruhashi, T. 1980.  Feeding behavior and diet of the Japanesemonkey (Macaca fuscata yakui) on Yakushima Island, Japan.Primates 21: 141–160.Muroyama, Y. and Yamada, A. 2010.  Conservation: present statusof the Japanese macaque population and its habitat. In (N.Nakagawa, M. Nakamichi and H. Sugiura, eds.) The JapaneseMacaques, pp. 143–164.  Springer, Tokyo.Nakamura, T., Kanzaki, N. and Maruyama, N. 2001.  Seasonalchanges in food habits of Japanese martens in Hinode-cho andAkiruno-shi, Tokyo.  Wildlife Conservation Japan 6: 15–24 (inJapanese with English summary).Nakayama, S., Inokuchi, M. and Minamitani, Y. 2000.  Seeds of WildPlants in Japan.  Tohoku University Press, Sendai, 642 pp. (inJapanese).Otani, T. 2003.  Seed dispersal and predation of fleshy-fruited plantsby Japanese macaques in the cool temperate zone of northernJapan.  Mammal Study 28: 153–156.Otani, T. 2005.  Characteristics of middle-size mammals as a seeddisperser of fleshy-plants.  Nagoya University Forest ScienceResearch 24: 7–43 (in Japanese with English summary).Otani, T. and Shibata, E. 2000.  Seed dispersal and predation byYakushima macaques, Macaca fuscata yakui, in a warm temperateforest of Yakushima Island, southern Japan.  Ecological Research15: 133–144.R Development Core Team. 2009.  R: A Language and Environmentfor Statistical Computing. Version 2.9.1. R Foundation for Statis-tical Computing, Vienna, Austria.Tsuji, Y., Fujita, S., Sugiura, H., Saito, C. and Takatsuki, S. 2006.Long-term variation in fruiting and the food habits of wildJapanese macaques on Kinkazan Island, northern Japan.  Ameri-can Journal of Primatology 68: 1068–1080.Tsuji, Y., Sato, K. and Sato, Y. 2011a.  The role of Japanese macaques(Macaca fuscata) as endozoochorous seed dispersers onKinkazan Island, northern Japan.  Mammalian Biology 76: 525–533.Tsuji, Y., Tatewaki, T. and Kanda, E. 2011b.  Endozoochorous seeddispersal by sympatric mustelids, Martes melampus and Mustelaitatsi, in western Tokyo, central Japan.  Mammalian Biology 76:628–633.Yumoto, T., Noma, M. and Maruhashi, T. 1998.  Cheek-pouchdispersal of seeds by Japanese monkeys (Macaca fuscata yakui)on Yakushima Island, Japan.  Primates 39: 325–338.Received 4 February 2011. Accepted 15 April 2011.

Seed Dispersal by Japanese Macaques (Macaca fuscata) in Western Tokyo, Central Japan: A Preliminary Report

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Seed Dispersal by Japanese Macaques (Macaca fuscata) in Western Tokyo, Central Japan: A Preliminary Report

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