Population Ecology

, Volume 47, Issue 1, pp 41–51 | Cite as

Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel

  • Jyun-ichi KitamuraEmail author
Original Article


I investigated the seasonal change in factors affecting embryonic mortality in the rosy bitterling, Rhodeus ocellatus kurumeus, a freshwater fish that spawns on the gills of living unionid mussels. Research was conducted in a small pond during 1999 and 2001 in which bitterling were provided with Anodonta sp. mussels for spawning. Bitterling spawned between April and July, peaking mid–late May. Seasonal survival rate of bitterling embryos in their mussel hosts was unimodal, with a peak between late April and mid May (about 70% of total spawnings). In mid April, survival was about 50%. The lowest survival was from late May to July (0%). Losses of bitterling embryos from mussels were identified by ejections from the mussel host. Ejections were categorized as either ejections of live embryos, or ejections of embryos that died in the mussel and were subsequently expelled from the mussel. Ejection rates of live embryos were higher in the earlier part of the spawning period (early–mid April) and dead embryo ejections in the later period (after June). The ejection rate of live embryos was higher among younger embryos earlier in the season, probably because of the incomplete development of morphological and behavioural traits associated with maintaining the embryo inside the mussel gill chambers, and as a consequence of a more protracted developmental period at low temperatures making them more susceptible to ejection. The ejection rate of dead embryos was higher in older embryos later in the season, and in larger mussels and at high embryo densities. The survival of embryos in mussels was probably related to oxygen availability, with mortalities probably caused by asphyxiation. Increased embryo mortalities may arise through competition among embryos, between embryos and mussel, and ambient dissolved oxygen levels. The optimal period for bitterling to spawn may represent a balance between two opposing factors; with positive and negative effects of a seasonal rise in temperature directly affecting embryonic growth rate and oxygen availability.


Freshwater mussel Oxygen availability Adaptation Oviposition Density dependence Egg size 



I am grateful to E. Tanaka, S. Kitagishi and F. Wakano (Section of Biology Higashiosaka City), and Dr. Y. Kanoh (Section of Biology, Seifu High School) for help with the field survey; Professors Y. Nagata and I. Maki, H. Yamane, K. Tani, Y. Iokura and other members of the Laboratory of Animal Ecology, Osaka Kyoiku University, for their support and useful advice; Professor M. Hori, Associate Professors T. Sota and K. Watanabe and other members of the Laboratory of Animal Ecology, Kyoto University, for useful suggestions and discussion; Dr. K. Kawamura (Division of Genetics, National Research Institute of Aquaculture) for comments. I also thank Dr. C. Smith (Department of Biology, University of Leicester) for useful suggestions and help with English corrections. This study was partly supported by the Sasakawa Scientific Research Grant from the Japan Science Society.


  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. Bayne BL, Newell RC (1983) Physiological energetics of marine mollusks. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca. Academic, London, pp 407–515Google Scholar
  4. Chambers RC (1997) Environmental influences on egg and propagule sizes in marine fishes. In: Chambers RC, Trippel EA (eds) Early life history and recruitment in fish populations. Chapman and Hall, London, pp 63–102Google Scholar
  5. Coleman RM (1991) Measuring parental investment in nonspherical eggs. Copeia 1991:1092–1098Google Scholar
  6. Fujikura K, Segawa S, Okutani T (1988) Respiration rate and ammonia excretion rate of freshwater mussel, Unio douglasiae (Griffith et Pidgeon) (in Japanese). Venus 47:207–211Google Scholar
  7. Higashi S (1965a) The respiration of principal mollusks in Lake Biwa-ko (in Japanese). Venus 23:229–237Google Scholar
  8. Higashi S (1965b) Basal metabolism of principal mollusks in Lake Biwa-ko (in Japanese). Venus 24:152–155Google Scholar
  9. Huebner JD (1982) Seasonal variation in two species of unionid clams from Manitoba, Canada: respiration. Can J Zool 60:560–564Google Scholar
  10. Hunter MD, McNeil JH (1997) Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology 78:977–987Google Scholar
  11. Imai C, Tanaka S (1987) Effect of sea water temperature on egg size of Japanese anchovy. Nippon Suisan Gakkaishi 53:2169–2178Google Scholar
  12. Kamler E (1992) Early life history of fish. Chapman and Hall, LondonGoogle Scholar
  13. Kanoh Y (1996) Pre-oviposition ejaculation in externally fertilizing fish: how sneaker male rose bitterlings contrive to mate. Ethology 102:883–899Google Scholar
  14. Kanoh Y (2000) Reproductive success associated with territoriality, sneaking, and grouping in male rose bitterlings, Rhodeus ocellatus (Pisces: Cyprinidae). Env Biol Fish 57:143–154CrossRefGoogle Scholar
  15. Kawamura K (2003) Rhodeus ocellatus kurumeus In: Ministry of the environment in Japan. Threatened wildlife of Japan, Red data book, 2nd edn, vol 4. Pisces, brackish and freshwater fishes (in Japanese). Japan Wildlife Research Center, Tokyo, pp 44–45Google Scholar
  16. Kawamura K, Nagata Y, Ohtaka H, Kanoh Y, Kitamura J (2001) Genetic diversity in the Japanese rosy bitterling, Rhodeus ocellatus kurumeus (Cyprinidae). Ichthyol Res 48:369–378CrossRefGoogle Scholar
  17. Kondo T (2002) Unionid mussels of Japan (in Japanese). Osaka Kyoiku University, Kashiwara CityGoogle Scholar
  18. Ministry of the Environment in Japan (2002) Important wetland 500 selection in Japan (in Japanese). Ministry of the Environment in Japan, pp186–229Google Scholar
  19. Nagata Y (1985) Estimation of population fecundity of the bitterling, Rhodeus ocellatus, and ecological significance of its spawning habit into bivalves (in Japanese). Jpn J Ichthyol 32:324–334Google Scholar
  20. Nagata Y, Miyabe H (1978) Developmental stages of the bitterling, Rhodeus ocellatus ocellatus (Cyprinidae). Mem Osaka Kyoiku Univ Ser III 26:171–181Google Scholar
  21. Nakamura M (1969) Cyprinid fishes of Japan. Studies on the life history of cyprinid fishes of Japan (in Japanese). Research Institute for Natural Resources, TokyoGoogle Scholar
  22. Nikolsky G V (1963) The ecology of fishes (in Russian). Japanese translation by K. Kamei, published 1970. Takara-shobo, YonagoGoogle Scholar
  23. Pusch M, Siefert J, Walz N (2001) Filtration and respiration rates of two unionid species and their impact on the water quality of a lowland river. In: Bauer G, Wachtler K (eds) Ecology and evolution of the freshwater mussels unionoide. Springer, Berlin Heidelberg New York, pp 317–326Google Scholar
  24. Reynolds JD, Guillaume H (1998) Effects of phosphate on the reproductive symbiosis between bitterlings and freshwater mussels: implications for conservation. J Appl Ecol 35:575–581CrossRefGoogle Scholar
  25. Saijyo Y, Mitamura O (1995) New book, study method of lake and pond (in Japanese). Koudansya, TokyoGoogle Scholar
  26. 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
  27. Smith C, Reynolds JD, Sutherland WJ (2000b) The population consequences of reproductive decisions. Proc R Soc Lond B 267:1327–1334CrossRefPubMedGoogle Scholar
  28. 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
  29. Smith C, Reichard M, Jurajda P, Przybylski M (2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool Lond 262:107–124Google Scholar
  30. Suzuki N (1988) Development and incubation method of Rhodeus ocellatus smith in the laboratory. In: Nagata Y (eds) Research club of Japanese rosy bitterling, Rhodeusocellatus kurumeus (in Japanese). Shinseisha, Tokyo, pp 42–51Google Scholar
  31. Suzuki M (2002) Individual flowering schedule, fruit set, and flower and seed predation in Vaccinium hirtum Thumb (Ericaceae). Can J Bot 80:82–92CrossRefGoogle Scholar
  32. Suzuki M (2003) Effects of flower and seed predators and pollinators on fruit production in two sequentially flowering congeners. Plant Ecol 166:37–48CrossRefGoogle Scholar
  33. Suzuki N, Hibiya T (1984) Minute tubercles on the skin surface of larvae of Rhodeus (Cyprinidae) (in Japanese). Jpn J Ichthyol 31:198–202Google Scholar
  34. Suzuki N, Hibiya T (1985) Minute tubercles on the skin surface of larvae of Acheilognathus and Pseudoperilampus (Cyprinidae) (in Japanese). Jpn J Ichthyol 32:335–344Google Scholar
  35. Tankersley RA, Dimock RV (1993) The effect of larval brooding on the respiratory physiology of the freshwater unionid mussel Pyganodon cataracta. Am Mid Nat 130:146–163Google Scholar
  36. Tesch, FW (1971) Age and growth. In: Ricker WE (ed) Methods for assessment of fish production in fresh waters. IBP Handbook 3. Blackwell, Oxford, pp 98–130Google Scholar

Copyright information

© The Society of Population Ecology and Springer-Verlag Tokyo 2004

Authors and Affiliations

  1. 1.Department of Zoology, Faculty of ScienceKyoto UniversityKyotoJapan

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