Skip to main content
SpringerLink
Log in

Temporal variations in seed dispersal patterns of a bird-dispersed tree, Swida controversa (Cornaceae), in a temperate forest

  • Original Article
  • Published:
Ecological Research

Abstract

The seed dispersal patterns of bird-dispersed trees often show substantial seasonal and annual variation due to temporal changes in frugivorous bird and bird-dispersed fruit distributions. Elucidating such variation and how it affects plant regeneration is important for understanding the evolution and seed dispersal maintenance strategies of these plants. In this study, we investigated the seed dispersal quantity and distance of a bird-dispersed plant, Swida controversa, for 2 years and detected large seasonal variations in dispersal pattern. Early in the fruiting season, short seed dispersal distance and large amounts of fruit consumption by birds (seed dispersal quantity) were observed. In contrast, late in the fruiting season, a long seed dispersal distance and small seed dispersal quantity were observed. This relationship between seed dispersal distance and quantity may help to maintain constant seed dispersal effectiveness during the long S. controversa fruiting season. Annual variation was also detected for both seed dispersal quantity and distance. More effective seed dispersal was achieved in the masting year, because both seed dispersal quantity and distance were greater than that in the non-masting year. These seed dispersal dynamics may contribute to the evolution and maintenance of S. controversa masting behavior. Thus, we identified substantial temporal variation on both seasonal and annual scales in the seed dispersal pattern of a bird-dispersed plant. The temporal variation in seed dispersal pattern revealed in this study probably plays a substantial role in the life history and population dynamics of S. controversa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Burns K (2005) Is there limiting similarity in the phenology of fleshy fruits? J Veg Sci 16:617–624. doi:10.1111/j.1654-1103.2005.tb02404.x

    Article  Google Scholar 

  • Carlo T, Morales J (2008) Inequalities in fruit-removal and seed dispersal: consequences of bird behaviour, neighbourhood density and landscape aggregation. J Ecol 96:609–618. doi:10.1111/j.1365-2745.2008.01379.x

    Article  Google Scholar 

  • Cheung WY, Hubert N, Landry BS (1993) A simple and rapid DNA microextraction method for plant, animal, and insect suitable for RAPD and other PCR analyses. PCR Methods Appl 3:69–70. doi:10.1101/gr.3.1.69

    Article  CAS  PubMed  Google Scholar 

  • Corlett RT (1998) Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) Region. Biol Rev 73:413–448. doi:10.1111/j.1469-185X.1998.tb00178.x

    Article  CAS  PubMed  Google Scholar 

  • Corlett RT (2009) Seed dispersal distances and plant migration potential in tropical East Asia. Biotropica 41:592–598. doi:10.1111/j.1744-7429.2009.00503.x

    Article  Google Scholar 

  • Cramer JM, Mesquita RCG, Williamson GB (2007) Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biol Conserv 137:415–423

    Article  Google Scholar 

  • Crawley MJ (2005) Statistics An introduction using R. WIley, West Sussex

    Book  Google Scholar 

  • Dennis AJ, Schupp EW, Green RJ, Westott DA (2007) Seed dispersal: theory and its application in a changing world. CAB International, Wallingford

    Book  Google Scholar 

  • Fleming TH, Kress WJ (2011) A brief history of fruits and frugivores. Acta Oecol 37:521–530. doi:10.1016/j.actao.2011.01.016

    Article  Google Scholar 

  • Fukui A (1995) The role of the brown-eared bulbul Hypsypetes amaurotis as a seed dispersal agent. Res Popul Ecol 37:211–218. doi:10.1007/bf02515822

    Article  Google Scholar 

  • Godoy J, Jordano P (2001) Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites. Mol Ecol 10:2275–2283. doi:10.1046/j.0962-1083.2001.01342.x

    Article  CAS  PubMed  Google Scholar 

  • Hamilton MB (1999) Tropical tree gene flow and seed dispersal. Nature 401:129–130. doi:10.1038/43597

    Article  CAS  Google Scholar 

  • Hanya G (2005) Comparisons of dispersal success between the species fruiting prior to and those at the peak of migrant frugivore abundance. Plant Ecol 181:167–177. doi:10.1007/s11258-005-5914-4

    Article  Google Scholar 

  • Herrera CM (1984) A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecol Monogr 54:2–23. doi:10.2307/1942454

    Article  Google Scholar 

  • Herrera C (1995) Plant-vertebrate seed dispersal systems in the mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26:705–727. doi:10.1146/annurev.es.26.110195.003421

    Article  Google Scholar 

  • Herrera CM (1998) Long-term dynamics of Mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecol Monogr 68:511–538. doi:10.1890/0012-9615(1998)068[0511:ltdomf]2.0.co;2

  • Herrera CM (2002) Seed dipersal by vertebrates plant–animal interactions: an evolutionary approach. Blackwell Publishing, Oxford, pp 185–208

    Google Scholar 

  • Herrera CM, Jordano P, Guitián J, Traveset A (1998) Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. Am Nat 152:576–594. doi:10.1086/286191

    Article  CAS  PubMed  Google Scholar 

  • Herrera J, Morales J, Garcia D (2011) Differential effects of fruit availability and habitat cover for frugivore-mediated seed dispersal in a heterogeneous landscape. J Ecol 99:1100–1107. doi:10.1111/j.1365-2745.2011.01861.x

    Article  Google Scholar 

  • Higuchi H, Morioka H, Yamagishi S (1997) The encyclogedia of animals in Japan vol 4: bird 2. Heibonsya, Tokyo

    Google Scholar 

  • HilleRisLambers J, Clark J, Beckage B (2002) Density-dependent mortality and the latitudinal gradient in species diversity. Nature 417:732–735. doi:10.1038/nature00809

    Article  CAS  Google Scholar 

  • Jordano P, Garcia C, Godoy J, Garcia-Castano J (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Natl Acad Sci USA 104:3278–3282. doi:10.1073/pnas.0606793104

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kalinowski S, Taper M, Marshall T (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. doi:10.1111/j.1365-294X.2007.03089.x

    Article  PubMed  Google Scholar 

  • Kelly D (1994) The evolutionary ecology of mast seeding. Trends Ecol Evol 9:465–470. doi:10.1016/0169-5347(94)90310-7

    Article  CAS  PubMed  Google Scholar 

  • Kitamura S (2011) Frugivory and seed dispersal by hornbills (Bucerotidae) in tropical forests. Acta Oecol 37:531–541. doi:10.1016/j.actao.2011.01.015

    Article  Google Scholar 

  • Koike S, Masaki T (2008) Frugivory of carnivora in central and southern parts of Japan analyzed by literature search. J Jpn For Res 90:26–35. doi:10.4005/jjfs.90.26 (in Japanese with English summary)

    Article  Google Scholar 

  • Koike S, Masaki T, Nemoto Y, Kozakai C, Yamazaki K, Kasai S, Nakajima A, Kaji K (2011) Estimate of the seed shadow created by the Asiatic black bear Ursus thibetanus and its characteristics as a seed disperser in Japanese cool-temperate forest. Oikos 120:280–290. doi:10.1111/j.1600-0706.2010.18626.x

    Article  Google Scholar 

  • Kominami Y, Sato T, Takeshita K, Manabe T, Endo A, Noma N (2003) Classification of bird-dispersed plants by fruiting phenology, fruit size, and growth form in a primary lucidophyllous forest: an analysis, with implications for the conservation of fruit-bird interactions. Ornithol Sci 2:3–23. doi:10.2326/osj.2.3

    Article  Google Scholar 

  • Kwit C, Levey DJ, Greenberg CH, Pearson SF, McCarty JP, Sargent S, Mumme RL, Stouffer PC (2004) Fruit abundance and local distribution of wintering Hermit Thrushes (Catharus guttatus) and Yellow-rumped Warblers (Dendroica coronata) in South Carolina. Auk 121:46–57. doi:10.1642/0004-8038(2004)121[0046:FAALDO]2.0.CO;2

  • Levey DJ, Silva WR, Galetti M (2002) Seed dispersal and frugivory: ecology, evolution, and conservation. CAB International, Wallingford

    Google Scholar 

  • 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 34:575–604. doi:10.1146/annurev.ecolsys.34.011802.132428

    Article  Google Scholar 

  • Levine JM, Murrell DJ (2003) The community-level consequences of seed dispersal patterns. Annu Rev Ecol Evol Syst 34:549–574. doi:10.1146/annurev.ecolsys.34.011802.132400

    Article  Google Scholar 

  • Martínez I, González-Taboada F (2009) Seed dispersal patterns in a temperate forest during a mast event: performance of alternative dispersal kernels. Oecologia 159:389–400. doi:10.1007/s00442-008-1218-4

    Article  PubMed  Google Scholar 

  • Martinez I, Garcia D, Ramon Obeso J (2008) Differential seed dispersal patterns generated by a common assemblage of vertebrate frugivores in three fleshy-fruited trees. Ecoscience 15:189–199. doi:10.2980/15-2-3096

    Article  Google Scholar 

  • Masaki T, Kodani J (2009) Swida controversa Silvics of Japan. Japane Forestry Investigation Committee, Tokyo, pp 611–633

    Google Scholar 

  • Masaki T, Nakashizuka T (2002) Seedling demography of Swida controversa: effect of light and distance to conspecifics. Ecology 83:3497–3507. doi:10.1890/0012-9658(2002)083[3497:SDOSCE]2.0.CO;2

    Article  Google Scholar 

  • Masaki T, Suzuki W, Niiyama K, Iida S, Tanaka H, Nakashizuka T (1992) Community structure of a species-rich temperate forest, Ogawa Forest Reserve, central Japan. Vegetatio 98:97–111. doi:10.1007/BF00045549

    Article  Google Scholar 

  • Masaki T, Kominami Y, Nakashizuka T (1994) Spatial and seasonal patterns of seed dissemination of Cornus controversa in a temperate forest. Ecology 75:1903–1910. doi:10.2307/1941595

    Article  Google Scholar 

  • Masaki T, Takahashi K, Sawa A, Kado T, Naoe S, Koike S, Shibata M (2012) Fleshy fruit characteristics in a temperate deciduous forest of Japan: how unique are they? J Plant Res 125:103–114. doi:10.1007/s10265-011-0423-0

    Article  PubMed  Google Scholar 

  • McConkey KR, Brockelman WY (2011) Nonredundancy in the dispersal network of a generalist tropical forest tree. Ecology 92:1492–1502. doi:10.1890/10-1255.1

    Article  PubMed  Google Scholar 

  • Milligan BG (1992) Plant DNA isolation Molecular genetic analysis of populations: a practical approach. IRL Press, Oxford, pp 59–88

    Google Scholar 

  • Mizoguchi Y, Morishita T, Ohtani Y (2002) Climate in Ogawa Forest Reserve diversity and interaction in a temperate forest community: Ogawa Forest Reserve of Japan. Springer, Tokyo, pp 11–18

    Book  Google Scholar 

  • Morales J, Carlo TS (2006) The effects of plant distribution and frugivore density on the scale and shape of dispersal kernels. Ecology 87:1489–1496. doi:10.1890/0012-9658(2006)87[1489:TEOPDA]2.0.CO;2

  • Nakashizuka T, Iida S, Tanaka H, Shibata M, Abe S, Masaki T, Niiyama K (1992) Community dynamics of Ogawa Forest Reserve, a species rich deciduous forest, central Japan. Vegetatio 98:105–112. doi:10.1007/BF00047696

    Google Scholar 

  • Naoe S, Sakai S, Sawa A, Masaki T (2011) Seasonal difference in the effects of fragmentation on seed dispersal by birds in Japanese temperate forests. Ecol Res 26:301–309. doi:10.1007/s11284-010-0783-2

    Article  Google Scholar 

  • Noma N, Yumoto T (1997) Fruiting phenology of animal-dispersed plants in response to winter migration of frugivores in a warm temperate forest on Yakushima Island, Japan. Ecol Res 12:119–129. doi:10.1007/BF02523777

    Article  Google Scholar 

  • Noshiro S (1999) Cornaceae Flora of Japan. Kodansha, Tokyo, pp 254–258

    Google Scholar 

  • Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281. doi:10.1038/35005072

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Sakai S, Momose K, Yumoto T, Nagamitsu T, Nagamasu H, Hamid AA, Nakashizuka T (1999) Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. Am J Bot 86:1414–1436

    Article  CAS  PubMed  Google Scholar 

  • Schupp E (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107–108:15–29. doi:10.1007/BF00052209

    Google Scholar 

  • Schupp E, Jordano P, Gomez J (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353. doi:10.1111/j.1469-8137.2010.03402.x

    Article  PubMed  Google Scholar 

  • Sekercioglu CH (2006) Increasing awareness of avian ecological function. Trends in Ecol and Evol 21:464–471. doi:10.1016/j.tree.2006.05.007

    Article  Google Scholar 

  • Shibata M, Tanaka H, Iida S, Abe S, Masaki T, Niiyama K, Nakashizuka T (2002) Synchronized annual seed production by 16 principal tree species in a temperate deciduous forest, Japan. Ecology 83:1727–1742. doi:10.1890/0012-9658(2002)083[1727:SASPBP]2.0.CO;2

  • Spiegel O, Nathan R (2007) Incorporating dispersal distance into the disperser effectiveness framework: frugivorous birds provide complementary dispersal to plants in a patchy environment. Ecol Lett 10:718–728. doi:10.1111/j.1461-0248.2007.01062.x

    Article  PubMed  Google Scholar 

  • Takanose Y, Kamitani T (2003) Fruiting of fleshy-fruited plants and abundance of frugivorous birds: phenological correspondence in a temperate forest in central Japan. Ornithol Sci 2:25–32. doi:10.2326/osj.2.25

    Article  Google Scholar 

  • Tanaka H, Nakashizuka T (2002) Ground design of the research site Diversity and Interaction in a Temperate Forest Community: Ogawa Forest Reserve of Japan. Springer, Tokyo, pp 43–49

    Book  Google Scholar 

  • Thompson J, Willson M (1979) Evolution of temperate fruit-bird interactions—phenological strategies. Evolution 33:973–982

    Article  Google Scholar 

  • Tojo H (2009) Breeding bird community of the Ogawa Forest Reserve, an old-growth deciduous forest in central Japan. Ornithol Sci 8:105–115. doi:10.2326/osj.8.105

    Article  Google Scholar 

  • Weir J, Corlett RT (2007) How far do birds disperse seeds in the degraded tropical landscape of Hong Kong, China? Landsc Ecol 22:131–140. doi:10.1007/s10980-006-9002-5

    Article  Google Scholar 

  • Wenny DG, Levey DJ (1998) Directed seed dispersal by bellbirds in a tropical cloud forest. Proc Natl Acad Sci USA 95:6204. doi:10.1073/pnas.95.11.6204

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Westcott DA, Graham DL (2000) Patterns of movement and seed dispersal of a tropical frugivore. Oecologia 122:249–257. doi:10.1007/PL00008853

    Article  Google Scholar 

  • Wheelwright NT (1986) The diet of American Robins: an analysis of US Biological Survey records. Auk 103:710–725

    Google Scholar 

  • Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc (B) 73:3–36. doi:10.1111/j.1467-9868.2010.00749.x

    Article  Google Scholar 

  • Yamazaki M, Iwamoto S, Seiwa K (2009) Distance- and density-dependent seedling mortality caused by several diseases in eight tree species co-occurring in a temperate forest. Plant Ecol 201:181–196. doi:10.1007/s11258-008-9531-x

    Article  Google Scholar 

  • Yamazaki Y, Kaneko S, Naoe S, Masaki T, Isagi Y (2010) Isolation and characterization of 11 microsatellite loci in Swida controversa (Cornaceae). Conserv Genet Resour 2:145–147. doi:10.1007/s12686-010-9276-4

    Article  Google Scholar 

  • Yasuda M, Okumura M, Yamazaki K (2010) Mammal records in the Ogawa Forest Reserve and the surrounding area, Kitaibaraki, Ibaraki Prefecture, Japan. Bull Ibaraki Nat Mus 13:99–104

    Google Scholar 

  • 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. doi:10.1007/s11284-009-0612-7

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker MJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

We thank Dr. S. Abe, A. Fujitsu, S. Harasawa, H. Yamagata, and many others for field assistance; Dr. S. Kaneko for instructing us in the technique used for the genetic experiments; and Dr. M. Yamasaki and Dr. M. Terakawa for useful advice. This work was supported by the Japan Society for the Promotion of Science (JSPS) Research Fellowship for Young Scientists to Yoshihiro Yamazaki and by a Grant-in-Aid for Scientific Research (Grant 19201048) from the JSPS to Takashi Masaki. Part of this study was financially supported by the Pollution Control Research Fun from the Ministry of the Environment, Japan.

Author information

Authors and Affiliations

  1. Laboratory of Forest Biology, Division of Forest and Biomaterials Science, Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto, 606-8502, Japan

    Yoshihiro Yamazaki & Yuji Isagi

  2. Forestry and Forest Products Research Institute, Tsukuba, Ibaraki, 305-8687, Japan

    Shoji Naoe & Takashi Masaki

Authors
  1. Yoshihiro Yamazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shoji Naoe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takashi Masaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuji Isagi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoshihiro Yamazaki.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 166 kb)

Supplementary material 2 (XLSX 53 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yamazaki, Y., Naoe, S., Masaki, T. et al. Temporal variations in seed dispersal patterns of a bird-dispersed tree, Swida controversa (Cornaceae), in a temperate forest. Ecol Res 31, 165–176 (2016). https://doi.org/10.1007/s11284-015-1324-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-015-1324-9

Keywords

Search

Navigation