Environmental Biology of Fishes

, Volume 78, Issue 1, pp 37–55 | Cite as

Reproductive Ecology and Host Utilization of Four Sympatric Bitterling (Acheilognathinae, Cyprinidae) in a Lowland Reach of the Harai River in Mie, Japan

  • Jyun-ichi Kitamura
Original Paper


Bitterling are fishes that use freshwater mussels for oviposition. The reproductive ecology and pattern of mussel utilization of four sympatric species of bitterling, Acheilognathus rhombeus, A. tabira tabira, Tanakia lanceolata, and T. limbata, were investigated in a lowland river with seven sympatric mussel species. Three bitterling species are spring spawners with overlapping spawning seasons. A. rhombeus is an autumn-spawning species and is temporally isolated in its reproduction from the other species. Ovipositor length during oviposition of T. limbata and T. lanceolata was short, while those of A. tabira tabira and A. rhombeus were long. Most T. limbata inhabited near-shore areas, whereas the two other spring-spawning species were distributed across the entire river. All bitterling species used Inversidens brandti, Obovalis omiensis and Inversiunio jokohamensis as spawning hosts, but not the other mussel species available. T. lanceolata, A. tabira tabira and A. rhombeus showed spawning preferences for O. omiensis and I. brandti. However, T. limbata did not show clear preferences for any of the mussel species they used. A. t. tabira showed a significant preference for large I. brandti in offshore areas, while the other spring-spawning bitterling showed a preference for mussels inshore. These results are discussed in the context of reproductive resource partitioning.


Resource utilization Ovipositor Freshwater mussel Host selectivity Habitat segregation Sarcocheilichthys variegates variegates 


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I am grateful to M. Hori, Y. Nagata and T. Kondo, Associate T. Sota and K. Watanabe, A Satoh, H. Nishi and other members of the Laboratory of Animal Ecology, Kyoto University, and members of the Laboratory of Animal Ecology, Osaka Kyoiku University, for their support and assistance in field surveys; K. Kawamura (Faculty of Bioresources, Mie University) for comments and help in bioassays of DNA. I also thank C. Smith of the Department of Biology, University of Leicester for his useful suggestions and assistance with English in the manuscript. This study was partly supported by the Sasakawa Scientific Research Grant from the Japan Science Society and Fujiwara Natural History Foundation.


  1. Aldridge DC (1997) Reproductive ecology of bitterling (Rhodeus sericeus Pallas) and unionid mussels. PhD Thesis, Cambridge University, CambridgeGoogle Scholar
  2. Aldridge DC (1999) Development of European bitterling in the gills of freshwater mussels. J Fish Biol 54:138–151CrossRefGoogle Scholar
  3. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310CrossRefGoogle Scholar
  4. Feinsinger P, Spears EE, Poole RW (1981) A simple measure of niche breadth. Ecology 62:27–32CrossRefGoogle Scholar
  5. Fukuhara S, Maekawa W, Nagata Y (1984) Experimental analysis of the use of mussels by three species of acheilognathine bitterlings (in Japanese). In: Committee for the memorial publication in commemoration of Prof. Mizuno’s retirement, A memorial publication in commemoration of Professor T Mizuno’s retirement. Osaka, pp. 221–226Google Scholar
  6. Fukuhara S, Maekawa W, Nagata Y (1998) Comparison of utilization of freshwater mussels for deposition of the bitterlings in three creeks of northwest Kyushu (in Japanese with English abstract). Memoirs Osaka Kyoiku Univ Ser III 47:27–37Google Scholar
  7. Hirai K (1964) Comparative studies on ecology of four species of bitterlings in the Lake Biwa (in Japanese with English abstract). Physiol Ecol Japan 12:72–81Google Scholar
  8. Hutchinson GE (1965) The ecological theater and the evolutionary play. Yale University Press, New HavenGoogle Scholar
  9. Ivlev VS (1955) Experimental ecology of the feeding of fishes (in Russian). Translated into Japanese by Kodama Y, Yoshihara T (1996) Tatarashobo, Yonago. 261 ppGoogle Scholar
  10. Kamler E (1992) Early life history of fish. Chapman and Hall, LondonGoogle Scholar
  11. Kawamura K, Uehara K (2005) Effects of temperature on free-embryonic diapause in the autumn-spawning bitterling Acheilognathus rhombeus (Teleostei: Cyprinidae). J Fish Biol 67:684–695CrossRefGoogle Scholar
  12. Kitamura J (2005) Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel. Popul Ecol 47:41–51CrossRefGoogle Scholar
  13. Kitamura J (2006) Seasonal change in the spatial utilization of host mussels in relation to ovipositor length by female rosy bitterling, Rhodeus ocellatus kurumeus. J␣Fish Biol 68:594–607CrossRefGoogle Scholar
  14. Kitamura, J (in press) Reproductive ecology of striped bitterling Acheilognathus cyanostigma (Cyprinidae: Acheilognathinae). Ichthyol ResGoogle Scholar
  15. Kondo T (1982) Taxonomic revision of Inversidens (Bivalvia: Unionidae). Venus 41:181–198Google Scholar
  16. Kondo T, Yamashita J, Kano M (1984) Breeding ecology of five species of bitterling (Pisces: Cyprinidae) in a small creek. Physiol Ecol Japan 21:53–62Google Scholar
  17. Liu H, Zhu Y, Smith C, Reichard M (in press) Evidence of host specificity and congruence between phylogenies of bitterlings and freshwater mussels. Zool Studies Google Scholar
  18. Mills SC, Reynolds JD (2002a). Host species preferences by bitterling, Rhodeus sericeus, spawning in freshwater mussels and consequences for offspring survival. Animal Behav 63:1029–1036CrossRefGoogle Scholar
  19. Mills SC, Reynolds JD (2002b). Mussel ventilation rates as a proximate cue for host selection by bitterling Rhodeus sericeus. Oecologia 131:473–478CrossRefGoogle Scholar
  20. Mills SC, Taylor MI, Reynolds JD (2005) Benefits and costs to mussels from ejecting bitterling embryos: a test of the evolutionary equilibrium hypothesis. Animal behav 70:31–37CrossRefGoogle Scholar
  21. Ministry of the environment in Japan (2002) Important wetland 500 selection in Japan (in Japanese). Ministry of the Environment in JapanGoogle Scholar
  22. Nagata Y (1985a). Spawning period and migration of rose bitterling, Rhodeus ocellatus, in a small pond (in Japanese with English abstract). Jpn J Ichthyol 32:79–89Google Scholar
  23. Nagata Y (1985b). The effect of social organization of the bitterling, Rhodeus ocellatus (Kner) and the condition of a bivalve, Anodonta woodiana Lea in a small pond on the number of fish eggs being laid in a bivalve (in Japanese with English abstract). Memoirs Osaka Kyoiku Univ Ser III 34:9–26Google Scholar
  24. Nagata Y, Nakata Y (1988) Distribution of six species of bitterlings in a creek in Fukuoka Prefecture. Jpn J Ichthyol 35:320–331Google Scholar
  25. Nakamura M (1969) Cyprinid fishes of Japan. Studies on the life history of cyprinid fishes of Japan. Research Institute for Natural Resources, Tokyo (in Japanese)Google Scholar
  26. Okazaki M, Naruse K, Shima A, Arai R (2001) Phylogenetic relationships of bitterlings based on mitochondrial 12S ribosomal DNA sequences. J Fish Biol 58:89–106CrossRefGoogle Scholar
  27. Palumbi SR, Martin A, Remano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR, ver 2.0. Zoology Department, University of Hawaii, HonoluluGoogle Scholar
  28. Reichard M, Jurajda P, Smith C (2004) Male-male interference competition decreases spawning rate in the European bitterling (Rhodeus sericeus). Behav Ecol Sociobiol 56:34–41CrossRefGoogle Scholar
  29. Reichard M, Ondračková M, Przybylski M, Liu H, Smith C (2006) The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J␣Evol Biol 19(3):788–796Google Scholar
  30. Shimizu A, Hanyu I (1981) Annual reproductive cycle of a spring-spawning bitterling Acheilognathus tabira (in Japanese with English abstract). Bull Jpn Soc Sci Fish 47:333–339Google Scholar
  31. Shimizu A, Aida K, Hanyu I (1987) Annual reproductive cycle in an autumn-spawning bitterling Acheilognathus rhombea. Bull Jpn Soc Sci Fish 53:529–536Google Scholar
  32. Smith C, Reynolds JD, Sutherland WJ (2000b). The population consequences of reproductive decisions. Proc Royal Soc London B 267:1327–1334CrossRefGoogle Scholar
  33. Smith C, Reynolds JD, Sutherland WJ, Jurajda P (2000a). Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus). Behav Ecol Sociobiol 48:29–35CrossRefGoogle Scholar
  34. Smith C, Reichard M, Jurajda P, Przybylski M (2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool 262:107–124CrossRefGoogle Scholar
  35. Smith C, Rippon K, Douglas A, Jurajda P (2001) A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshw Biol 46:903–911CrossRefGoogle Scholar
  36. Smith C, Wootton RJ (1995) The costs of parental care in teleost fishes. Rev Fish Biol Fish 5:7–22CrossRefGoogle Scholar
  37. Suzuki N, Hibiya T (1985) Minute tubercles on the skin surface of larvae of Acheilognathus and Pseudoperilampus (Cyprinidae) (in Japanese with English abstract). Jpn J Ichthyol 32:335–344CrossRefGoogle Scholar
  38. Webb PW (1998) Swimming. In: Evans DH (eds) The physiology of fishes. 2nd edn. CRC press, Boca Raton, New York, pp 3–24Google Scholar
  39. Winemiller KO, Pianka ER (1990) Organization in natural assemblages of desert lizards and tropical fishes. Ecol Monogr 60:27–55CrossRefGoogle Scholar
  40. Wootton RJ (1998) Ecology of teleost fishes. 2nd edn. Kluwer, DordrechtGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  1. 1.Department of Zoology, Graduate School of ScienceKyoto University Kyoto Japan

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