Ecological Research

, Volume 33, Issue 2, pp 495–504 | Cite as

Highly toxic seeds of the Japanese star anise Illicium anisatum are dispersed by a seed-caching bird and a rodent

  • Tetsuro YoshikawaEmail author
  • Takashi Masaki
  • Makoto Motooka
  • Daichi Hino
  • Keisuke Ueda
Original Article


Many field studies on plant seed dispersal teach us that we cannot judge the effective dispersal mode of plants by examining only the morphologies of the fruits and seeds. In the present study, we explored the seed dispersal process of an evergreen tree, the Japanese star anise Illicium anisatum, which is highly toxic, containing neurotoxins in both the fruits and seeds. The fruits exhibit ballochory, a mode of seed dispersal characterized by explosive fruit dehiscence, and the extreme toxicity apparently seems to deter fruit and seed consumption by animals. However, we found that the dispersal distance afforded by this mode was very short (≤ 6 m). In the field, we confirmed that a passerine species, the varied tit Poecile varius, was the only consumer of the seed in foliage, and the bird actively transported seeds or fruits to either cache or consume them. Seeds setting on the forest understory were removed by the small Japanese field mouse Apodemus argenteus, and were also dispersed by this animal. Analysis of seedling spatial distribution revealed that seedlings were highly aggregated near standing trees or fallen logs, suggesting that caching facilitated seed dispersal. This study warns that plant toxicity and the ecological function thereof should not be evaluated based only on limited knowledge of the effects on humans and mammals. Our results pose further questions on the evolution of toxin tolerance in seed-caching animals and on the mutualism between toxic plants and animals.


Ballochory Secondary metabolites Plant defense Toxicity 



We are grateful to Yuji Suda, the members of the Animal Ecology Laboratory at Rikkyo University, and those of the Community Dynamic Laboratory of the Forestry and Forest Products Research Institute for their assistance and constructive comments on our study. We thank Naoko Sashimura for informing us of the study site, Kaoru Niiyama for his help in identifying tree seedlings, and Shoji Naoe for allowing us to use his monitoring devices. We thank James Worth for checking English writing. We are grateful to the Izu Forest Management Office of the Forest Agency of Japan for permission to work in a national forest. During the study, the first author was partly supported by a Research Fellowship from the Japan Society for the Promotion of Science for Young Scientists (; Grant number 2610007) and the second author was supported funding by JSPS KAKENHI (Grant number JP17H00797).

Supplementary material

ESM 1 Footage of a varied tit Poecile varius handling the fruit of the Japanese star anise Illicium anisatum and then transporting a seed and a fruit. (MP4 24321 kb)


  1. Abe H, Matsuki R, Ueno S, Nashimoto M, Hasegawa M (2006) Dispersal of Camellia japonica seeds by Apodemus speciosus revealed by maternity analysis of plants and behavioral observation of animal vectors. Ecol Res 21:732–740. CrossRefGoogle Scholar
  2. Aiba S-I, Kohyama T (1997) Crown architecture and life-history traits of 14 tree species in a warm-temperate rain forest: significance of spatial heterogeneity. J Ecol 85:611–624. CrossRefGoogle Scholar
  3. Beck MJ, Vander Wall SB (2010) Diplochory in western chokecherry: you can’t judge a fruit by its mesocarp. Oecologia 165:131–141. CrossRefPubMedGoogle Scholar
  4. Briggs JS, Wall SBV, Jenkins SH (2009) Forest rodents provide directed dispersal of Jeffrey pine seeds. Ecology 90:675–687CrossRefPubMedGoogle Scholar
  5. Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu Rev Ecol Evol Syst 36:169–189CrossRefGoogle Scholar
  6. Ehrlén J, Eriksson O (1993) Toxicity in fleshy fruits: a non-adaptive trait? Oikos 66:107–113CrossRefGoogle Scholar
  7. Fujita K (1996) Habitat characteristics of food storage sites of Varied Tits Parus varius. Strix 14:41–54 (in Japanese with English abstract) Google Scholar
  8. Hashimoto H, Kamijyo T, Higuchi H (2002) Seed dispersal of Styrax japonica by Varied Tits Parus varius on Miyake-jima, Izu Islands. Jpn J Ornithol 51:101–107 (in Japanese with English abstract) CrossRefGoogle Scholar
  9. Higgins SI, Nathan R, Cain ML (2003) Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology 84:1945–1956CrossRefGoogle Scholar
  10. Higuchi H (1975) Comparative feeding ecology of two geographical formas of the Varied Tit, Parus vaius vaius in southern Izu peninsula and P. v. owstoni in Miyake I. of the Izu Is. Tori 24:15–28 (in Japanese with English abstract) Google Scholar
  11. Higuchi H (1976) Ecological significance of the larger body sizes in an island subspecies of the varied tit Parus varius. Proc Jpn Soc Syst Zool 12:78–86Google Scholar
  12. Hirano A, Sakuratani Y (2013) The relationship between Styrax japonica and Parus varius on the Nara Campus of Kinki University. Mem Fac Agric Kinki Univ 46:101–132 (in Japanese with English abstract) Google Scholar
  13. Ide Y, Wong BY-L, Sashimura N (2013) The status of forest in the Amagi Mountains in 1811 recorded in a historical document. Bull Tokyo Univ For 128:87–120 (in Japanese with English abstract) Google Scholar
  14. Iida S (1996) Quantitative analysis of acorn transportation by rodents using magnetic locator. Vegetatio 124:39–43. CrossRefGoogle Scholar
  15. Iwabe Y (1991) Poisoning by Japanese star anise seeds. Food Hyg Saf Sci (Shokuhin Eiseigaku Zasshi) 32:472–474. (in Japanese) CrossRefGoogle Scholar
  16. Iwatsuki K, Boufford DE, Ohba H (2006) Flora of Japan, vol 2a. Kodansha, TokyoGoogle Scholar
  17. Kiyosu Y (1966) Encyclopedia of wild birds in Japan. Tokyodo, Tokyo (in Japanese) Google Scholar
  18. Kobayashi H, Kubota Y, Yamada H, Yasumoto T, Okita M, Hirata H, Kanamori H, Toyota A (2003) Illicium religiosum poisoning in Japanese black cattle. J Jpn Vet Med Assoc 56:15–20. (in Japanese with English abstract) CrossRefGoogle Scholar
  19. Kudo Y, Oka J-I, Yamada K (1981) Anisatin, a potent GABA antagonist, isolated from Illicium anisatum. Neurosci Lett 25:83–88. CrossRefPubMedGoogle Scholar
  20. Lane JF, Koch WT, Leeds NS, Gorin G (1952) On the toxin of Illicium anisatum. I. The isolation and characterization of a convulsant principle: anisatin. J Am Chem Soc 74:3211–3215. CrossRefGoogle Scholar
  21. Levin SA, Muller-Landau HC, Nathan R, Chave J (2003) The ecology and evolution of seed dispersal: a theoretical perspective. Annu Rev Ecol Evol Syst 34:575–604CrossRefGoogle Scholar
  22. Marsh KJ, Wallis IR, Andrew RL, Foley WJ (2006) The detoxification limitation hypothesis: where did it come from and where is it going? J Chem Ecol 32:1247–1266. CrossRefPubMedGoogle Scholar
  23. Matsui T, Iida S, Kawahara T, Namikawa K, Hirakawa H (2010) Estimation of home range for Varied Tits (Parus varius) in late autumn near the northern range boundary of Siebold’s beech (Fagus crenata) in the scope of estimating dispersal distance of beech seeds. J Jpn For Soc 92:162–166. (in Japanese with English abstract) CrossRefGoogle Scholar
  24. McLean S, Duncan AJ (2006) Pharmacological perspectives on the detoxification of plant secondary metabolites: implications for ingestive behavior of herbivores. J Chem Ecol 32:1213–1228CrossRefPubMedGoogle Scholar
  25. Miyaki M, Kikuzawa K (1988) Dispersal of Quercus mongolica acorns in a broadleaved deciduous forest 2. Scatterhoarding by mice. For Ecol Manag 25:9–16CrossRefGoogle Scholar
  26. Murakami T, Hayashida M, Ogiyama K (2006) Effect of seed caching by Parus varius on germination in Styrax japonica. J Jpn For Soc 88:174–180. (in Japanese with English abstract) CrossRefGoogle Scholar
  27. Nakazawa Y, Takenaka F, Sakai K, Matsunaga Y, Oka T, Sadamatsu S, Kono S (1959) On the isolation of an active principle from Illicium anisatum L., its content and toxicity. Folia Pharmacol Jpn 55:524–530. (in Japanese) CrossRefGoogle Scholar
  28. Nathan R, Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A (2008) Mechanisms of long-distance seed dispersal. Trends Ecol Evol 23:638–647. CrossRefPubMedGoogle Scholar
  29. Oka T (1992) Home range and mating system of two sympatric field mouse species, Apodemus speciosus and Apodemus argenteus. Ecol Res 7:163–169. CrossRefGoogle Scholar
  30. Pearson KM, Theimer TC (2004) Seed-caching responses to substrate and rock cover by two Peromyscus species: implications for pinyon pine establishment. Oecologia 141:76–83CrossRefPubMedGoogle Scholar
  31. Perea R, San Miguel A, Gil L (2011) Acorn dispersal by rodents: the importance of re-dispersal and distance to shelter. Basic Appl Ecol 12:432–439CrossRefGoogle Scholar
  32. Ridley HN (1930) The dispersal of plants throughout the world. L. Reeve, AshfordGoogle Scholar
  33. Roberts ML, Haynes RR (1983) Ballistic seed dispersal in Illicium (Illiciaceae). Plant Syst Evol 143:227–232. CrossRefGoogle Scholar
  34. Romanov MS, Bobrov AVFC, Endress PK (2013) Structure of the unusual explosive fruits of the early diverging angiosperm Illicium (Schisandraceae s.l., Austrobaileyales). Bot J Linn Soc 171:640–654. CrossRefGoogle Scholar
  35. Sakakibara S (1989) The role of the varied tit, Parus varius T. and S., in the seed dispersal of Japanese yew, Taxus cuspidata S. and Z. J Jpn For Soc 71:41–49 (in Japanese with English abstract) Google Scholar
  36. Sakes A, van der Wiel M, Henselmans PWJ, van Leeuwen JL, Dodou D, Breedveld P (2016) Shooting mechanisms in nature: a systematic review. PLOS ONE 11:e0158277. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Seidler TG, Plotkin JB (2006) Seed dispersal and spatial pattern in tropical trees. PLoS Biol 4:e344. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Seiwa K, Watanabe A, Irie K, Kanno H, Saitoh T, Akasaka S (2002) Impact of site-induced mouse caching and transport behaviour on regeneration in Castanea crenata. J Veg Sci 13:517–526CrossRefGoogle Scholar
  39. Sherry F (1989) Food storing in the Paridae. Wilson Bull 101:289–304Google Scholar
  40. Shimada T (2001) Hoarding behaviors of two wood mouse species: different preference for acorns of two Fagaceae species. Ecol Res 16:127–133. CrossRefGoogle Scholar
  41. Shimada T, Saitoh T, Sasaki E, Nishitani Y, Osawa R (2006) Role of tannin-binding salivary proteins and tannase-producing bacteria in the acclimation of the Japanese wood mouse to acorn tannins. J Chem Ecol 32:1165–1180CrossRefPubMedGoogle Scholar
  42. Struempf HM, Schondube JE, Del Rio CM (1999) The cyanogenic glycoside amygdalin does not deter consumption of ripe fruit by cedar waxwings. Auk 116:749–758CrossRefGoogle Scholar
  43. Suganuma Y, Ishihara K (1953) Poisoning by Japanese star anise in sheep. J Jpn Vet Med Assoc 6:410–411 (in Japanese) Google Scholar
  44. van der Pijl L (1982) Principles of dispersal in higher plants. Springer, BerlinCrossRefGoogle Scholar
  45. Vander Wall SB (1991) Mechanisms of cache recovery by yellow pine chipmunks. Anim Behav 41:851–863. CrossRefGoogle Scholar
  46. Vander Wall SB, Longland WS (2004) Diplochory: are two seed dispersers better than one? Trends Ecol Evol 19:155–161CrossRefPubMedGoogle Scholar
  47. Vittoz P, Engler R (2007) Seed dispersal distances: a typology based on dispersal modes and plant traits. Bot Helvetica 117:109–124CrossRefGoogle Scholar
  48. Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379–386CrossRefGoogle Scholar
  49. Wenny DG (2001) Advantages of seed dispersal: a re-evaluation of directed dispersal. Evol Ecol Res 3:37–50Google Scholar
  50. Willson MF (1993) Dispersal mode, seed shadows, and colonization patterns. Vegetatio 107:261–280Google Scholar
  51. Yoshikawa T, Isagi Y, Kikuzawa K (2009) Relationships between bird-dispersed plants and avian fruit consumers with different feeding strategies in Japan. Ecol Res 24:1301–1311. CrossRefGoogle Scholar
  52. Yui M (1988) Mori ni sumu yacho no seitaigaku (Ecology of wild birds in forests). Sobun, Tokyo (in Japanese) Google Scholar

Copyright information

© The Ecological Society of Japan 2018

Authors and Affiliations

  1. 1.Department of Forest VegetationForestry and Forest Products Research InstituteTsukubaJapan
  2. 2.Department of Life ScienceRikkyo UniversityTokyoJapan
  3. 3.Forest Biology Lab, Graduate School of AgricultureKyoto UniversityKyotoJapan

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