Abstract
We examined the interactions between bird-dispersed plants and fruit-consuming birds with various feeding strategies, by reviewing the plant species consumed by 14 bird species in Japan with four feeding types: gulpers (five species), grinders (four species), crushers (four species), and peckers (one species). Our literature review provided information on the plant species consumed by the birds in Japan and the morphological traits of the fruits: fruit volume, seed mass and number, pulp type (fleshy, dry, or arillate), and plant height (tall, medium, or small). Using these data, we examined the diversity of plant species consumed by each bird and the fruit morphological traits that affected fruit selection. The five gulpers consumed fruits from the largest number of plants, followed by the four grinders, the four crushers, and the one pecker. The gulpers and grinders consumed a wider variety of fruits than were consumed by the crushers and the pecker. Logistic regression analysis revealed that some crushers and the pecker preferred plants with dry or arillate pulp around the seeds. Our results suggest that a frugivorous bird’s feeding strategies, and particularly its fruit-handling behaviors and the fruit parts it ingests, influence the diversity of plants it consumes. The crushers and the pecker, which feed exclusively on seeds, require more effort and time to consume this type of food, and this might cause a strong preference for specific fruit traits and thus, consumption of a lower diversity of plant species.
Similar content being viewed by others
References
Asakawa S, Katsuta M, Yokoyama T (1981) Seeds of the trees of Japan: broadleaf trees (in Japanese). Zaimoku-ikushu-kyokai, Tokyo
Asano S (2005) Sadao Asano’s biological flora of Japan (in Japanese). Zennkoku-nohson-kyoiku-kyokai, Tokyo
Bollen A, Van Elsacker L, Ganzhorn JU (2004) Relations between fruits and disperser assemblages in a Malagasy littoral forest: a community-level approach. J Trop Ecol 20:599–612. doi:10.1017/S0266467404001853
Carlo TA, Collazo JA, Groom MJ (2003) Avian fruit preferences across a Puerto Rican forested landscape: pattern consistency and implication for seed removal. Oecologia 134:119–131. doi:10.1007/s00442-002-1087-1
Cole FR, Loope LL, Medeiros AC, Raikes JA, Wood CS (1995) Conservation implications of introduced game birds in high-elevation Hawaiian shrubland. Conserv Biol 9:306–313. doi:10.1046/j.1523-1739.1995.9020306.x
Corlett RT (1998) Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) region. Biol Rev Camb Philos Soc 73:413–448. doi:10.1017/S0006323198005234
Dennis AJ, Westcott DA (2006) Reducing complexity when studying seed dispersal at community scales: a classification of vertebrate seed dispersers in tropical forests. Oecologia 149:620–634. doi:10.1007/s00442-006-0475-3
Editorial Department of Yacho (1991) Observations on fruits of birds (in Japanese). Yacho 56:20–21
Edwards W (2005) Within- and between-species patterns of allocation to pulp and seed in vertebrate dispersed plants. Oikos 110:109–114. doi:10.1111/j.0030-1299.2005.12846.x
Englund R (1993) Fruit removal in Viburnum opulus: copious seed predation and sporadic massive seed dispersal in a temperate shrub. Oikos 67:503–510. doi:10.2307/3545362
Fennell CM (1965) Stomach analyses of Korean birds. J Yamashina Inst Ornithol 4:172–183
Fuentes M (1994) Diets of fruit-eating birds: what are the causes of interspecific differences? Oecologia 97:134–142. doi:10.1007/BF00317917
Fukui A (1995) The role of the brown-eared bulbul Hypsypetes amaurotis as a seed-dispersal agent. Res Popul Ecol (Kyoto) 37:211–218. doi:10.1007/BF02515822
Fukui N, Ueda K (1999) Seed dispersal of Chinese tallow-tree Sapium sebiferum by birds (in Japanese with English summary). Jpn J Ornithol 47:121–124. doi:10.3838/jjo.47.121
Gautier-Hion A, Duplantier J-M, Quris R, Feer F, Sound C, Decoux J-P, Dubost G, Emmons L, Erard C, Hecketsweiler P, Moungazi A, Roussilhon C, Thiollay J-M (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324–337. doi:10.1007/BF00378906
Gill F, Wright M, Donsker D (2008) IOC World Bird Names (version 1.6). http://www.worldbirdnames.org/
Hagiwara S (1977) Rapid multiplication on Trachycarpus excelsa and T. fortunei in urban forest 1. Seed dispersal and establishment (in Japanese with English summary). Misc Rep Inst Nat Study 7:19–31
Hamada T, Kon M, Noma N (2007) Fruit consumption and seed dispersal of Cornus brachypoda by birds in the eastern area of Lake Biwa, Shiga (in Japanese with English summary). Bull Kansai Org Nat Conserv 29(2):111–123
Hashiguchi D, Ueda K (1990) The Gray Starling Sturnus cineraceus as a fruit-eater: analysis of regurgitated seeds (in Japanese with English summary). Strix 9:55–61
Hashimoto H, Kamijyo T, Higuchi H (2002) Seed dispersal of Styrax japonica by Varied Tit Parus varius on Miyake-jima, Izu Islands (in Japanese with English summary). Jpn J Ornithol 51:101–107. doi:10.3838/jjo.51.101
Hayashi S (1985) The trees of Japan (in Japanese). Yamatokeikokusha, Tokyo
Hayashi S, Furusato K, Nakamura T (1985) Illustrated trees in colour (in Japanese). Hokuryukan, Tokyo
Higuchi H (1975) Comparative feeding ecology of two geographical forms of the Varied Tit, Parus varius varius in southern Izu peninsula and P. v. owstoni in Miyake I. of the Izu Is (in Japanese with English summary). Tori 24:15–28
Iwatsuki K, Boufford DE, Ohba H (2006) Flora of Japan, vol IIa. Kodansha, Tokyo
Kanagawa Branch of the Wild Bird Society of Japan (2007) The birds in Kanagawa 2001–2005: the list of birds in Kanagawa prefecture 5 (in Japanese). Kanagawa Branch of the Wild Bird Society of Japan, Yokohama
Kanouchi T (2006) Handbook of birds and fruits (in Japanese). Bunnichi-sogo-shuppan, Tokyo
Kitamura S, Murata G (1961) Colour illustrations of herbaceous plants of Japan vol. 2 (in Japanese). Hoikusha, Osaka
Kitamura S, Murata G, Koyama T (1964) Colour illustrations of herbaceous plants of Japan vol. 3 (in Japanese). Hoikusha, Osaka
Kitamura S, Yumoto T, Poonswad P, Chuailua P, Plongmai K, Maruhashi T, Noma N (2002) Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand. Oecologia 133:559–572. doi:10.1007/s00442-002-1073-7
Kiyosu Y (1966) Encyclopedia of wild birds in Japan (in Japanese). Tokyodo, Tokyo
Kojima K, Wada T (1967) On the food habits of some birds in Kochi prefecture (in Japanese). Res Rep Kochi Univ Nat Sci II 16:51–62
Kominami K, 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
Krebs CJ (1989) Ecological methodology. Harper and Row, New York
Krefting LW, Roe EI (1949) The role of some birds and mammals in seed germination. Ecol Monogr 19:269–286. doi:10.2307/1943538
Kwit C, Levey DJ, Greenberg CH, Pearson SF, McCarty JP, Sargent S (2004) Cold temperature increases winter fruit removal rate of a bird-dispersed shrub. Oecologia 139:30–34. doi:10.1007/s00442-003-1470-6
Levey DJ (1987) Seed size and fruit-handling techniques of avian frugivores. Am Nat 129:471–485. doi:10.1086/284652
MacArthur RH, Pianka ER (1966) On the optimal use of a patchy environment. Am Nat 100:603–609. doi:10.1086/282454
McCarty JP, Levey DJ, Greenberg CH, Sargent S (2002) Spatial and temporal variation in fruit use by wildlife in a forested landscape. For Ecol Manage 164(27):7–291
Moermond TC, Denslow JS (1984) Neotropical avian frugivores: patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Ornithol Monogr 36:865–897
Moran C, Catterall CP, Green RJ, Olsen MF (2004) Functional variation among frugivorous birds: implications for rainforest seed dispersal in a fragmented subtropical landscape. Oecologia 141:584–595. doi:10.1007/s00442-004-1685-1
Nakanishi H (1994) Dispersal types of the component species of natural forests in Japan. Nagasaki Womens Jr Coll Ann Rep Study 18:1–5
Nakanishi H (1996) Fruit color and fruit size of bird-disseminated plants in Japan. Vegetatio 123:207–218. doi:10.1007/BF00118272
Nakayama S, Inokuchi M, Minamitani T (2000) Seeds of wild plants in Japan (in Japanese). Tohoku University Press, Sendai
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
Ohwi J, Kitagawa M (1983) New flora of Japan (in Japanese). Shibundo, Tokyo
Okamoto M (2006) Birds and fruits (2) (in Japanese). Planta 108:17–24
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Rey PJ, Gutiérrez JE (1996) Pecking of olives by frugivorous birds: a shift in feeding behaviour to overcome gape limitation. J Avian Biol 27:327–333. doi:10.2307/3677264
Rey PJ, Gutiérrez JE, Alcantara JM, Valera F (1997) Fruit size in wild olives: implications for avian seed dispersal. Funct Ecol 11:611–618. doi:10.1046/j.1365-2435.1997.00132.x
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 (in Japanese with English summary). J Jpn For Sci 71:41–49
Satake Y, Ohwi J, Kitamura S, Watari S (1982) Wild flowers of Japan. Herbaceous plants. Vol 1–3 (in Japanese). Heibonsha, Tokyo
Satake Y, Hara H, Watari S, Tominari T (1989) Wild flowers of Japan. Woody plants. Vol 1–2 (in Japanese). Heibonsha, Tokyo
Sato S, Sakai A (2001) Eaten process of Rhus sylvestris fruits by birds (in Japanese with English summary). Ap For Sci 10:63–67
Sato S, Sakai A (2004) Fruit foraging process and seed dispersal of Angelica tree Aralia elata by birds (in Japanese with English summary). Ap For Sci 13:111–114
Sato S, Sakai A (2005) Birds as dispersers of Mallotus japonicus in a coniferous plantation (in Japanese with English summary). Jpn J Ornithol 54(1):23–28. doi:10.3838/jjo.54.23
Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107(108):15–29
Shimizu T (2003) Invasive plants in Japan (in Japanese). Heibonsha, Tokyo
Silva WR, Guimarães PR, dos Reis SF, Guimarães PG (2007) Investigating fragility in plant-frugivore networks: a case study of the Atlantic forest in Brazil. In: Dennis J, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CABI Publishing, Wallingford, pp 561–578
Snow DW, Snow BK (1987) Some aspects of avian frugivory in a north temperate area relevant to tropical forest. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal. Dr W Junk Publishers, Dordrecht, pp 159–164
Swank WG (1944) Germination of seeds after ingestion by Ring-necked Pheasants. J Wildl Manage 8:223–231. doi:10.2307/3795702
Takano S (1981) Birds of Japan in photographs (in Japanese). Tokai University Press, Tokyo
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
Traveset A (1994a) Influence of type of avian frugivory on the fitness of Pistacia terebinthus L. Evol Ecol 8:618–627. doi:10.1007/BF01237845
Traveset A (1994b) Cumulative effects on the reproductive output of Pistacia terebinthus (Anacardiaceae). Oikos 71:152–162. doi:10.2307/3546182
Uchida S, Kuzu S (1931) Investigation on the food habits of Oriental Green Finch (in Japanese). Ornithological and Mammalogical Report 5. Bureau of Agriculture and Commerce, Tokyo
van der Pijl L (1982) Principles of dispersal in higher plants, 3rd edn. Springer, Berlin Heidelberg New York
Wada T (2002) Foods and life of Brown-eared Bulbul in winter (in Japanese). Yacho 649:6–9
Walker JS (2007) Dietary specialization and fruit availability among frugivorous birds on Sulawesi. Ibis 149:345–356. doi:10.1111/j.1474-919X.2006.00637.x
Westoby M (1978) What are the biological bases on varied diets? Am Nat 112:627–631. doi:10.1086/283303
Wheelwright NT (1985) Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818. doi:10.2307/1940542
Wheelwright NT (1986) The diet of American robins: an analysis of U.S. biological survey records. Auk 103:710–725
Wheelwright NT, Janson CH (1985) Colors of fruit displays of bird-dispersed plants in two tropical forests. Am Nat 126(6):777–799. doi:10.1086/284453
Yagihashi T (1995) Fruit set, flower and fruit abortion, and fruit removal of Prunus sargentii Rehder. Trans Mtg Hokkaido Br Jpn For Soc 43:183–185
Yagihashi T (2001) Effects of bird ingestion on seed germination of arboreal plants in Hokkaido, Japan (in Japanese). Res Bull Hokkaido Univ For 58:37–59
Yagihashi T, Hayashida M, Miyamoto T (1998) Effect of bird ingestion on seed germination of Sorbus commixta. Oecologia 114:209–212. doi:10.1007/s004420050438
Yoshida M, Arakida A, Arakida N (2001) Seed dispersal of mistletoe Hyphear tanakae Hozakiyadorigi by birds (in Japanese with English summary). Strix 19:115–120
Yoshikawa T (2007) Feeding behaviors of Masked Grosbeak Eophona personata on acorns of fagaceous species (in Japanese with English summary). J Yamashina Inst Ornithol 38:143–146
Yugi Y (1991) The 32 fruits eaten by birds (in Japanese). Yacho 56:10–21
Acknowledgments
We thank the Yamashina Institute for Ornithology and the Forestry and Forest Products Research Institute for letting us measure the gape sizes of their bird specimens. We thank Manabu Kajita for letting us measure gape size in his specimens and for offering information on the pertinent literature. Kouichi Karasawa kindly answered our questions regarding avian gape width. We are grateful to the Kyoto Botanical Garden and the Kamigamo Experimental Forest of Kyoto University for permitting our preliminary fruit observation and sampling. Mari Terakawa and Takahiro Ohta gave us helpful advice on an earlier draft of this paper. We thank Douglas J. Levey and the anonymous reviewers for their very valuable comments and suggestions on our manuscript. We also thank Atsushi Takayanagi, Michimasa Yamasaki, Masae Ishihara, Mizuki Inoue, Kaori Tsujita, and members of the Forest Biology Lab of Kyoto University for their valuable discussions and encouragement on our study.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Yoshikawa, T., Isagi, Y. & Kikuzawa, K. Relationships between bird-dispersed plants and avian fruit consumers with different feeding strategies in Japan. Ecol Res 24, 1301–1311 (2009). https://doi.org/10.1007/s11284-009-0612-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11284-009-0612-7