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Spawning and Adaptation Characteristics Inside the Mussel, Unio douglasiae of Autumn Spawning Bitterling, Acheilognathus rhombeus (Pisces: Acheilognathinae)

추계산란종 납지리, Acheilognathus rhombeus (Pisces: Acheilognathinae)의 말조개, Unio douglasiae 내 산란과 적응특성

  • Kim, Hyeongsu (Inland aquaculture research, National Institute of Fisheries Science) ;
  • Park, Jongsung (Research center for endangered species, National Institute of Ecology) ;
  • Kim, Hyuntae (Faculty of Biological Science and Institute for Biodiversity, College of Natural Science, Jeonbuk National University)
  • 김형수 (국립수산과학원 내수면양식연구센터) ;
  • 박종성 (국립생태원 멸종위기종복원센터) ;
  • 김현태 (전북대학교 자연과학대학 생물다양성연구소)
  • Received : 2020.06.30
  • Accepted : 2020.08.06
  • Published : 2020.08.31

Abstract

This study aimed to investigate the autumn spawning by bitterling (A. rhombeus) inside mussel (Unio douglasiae) and the adaptation characteristics at the Bongseocheon Stream of Mankyeonggang River. The survey was carried out between August 2015 and July 2016. The spawning season was from September to November, and 17-75 (36.2 ± 16.44) eggs were found from mature females. During the survey period, 476 mussels were collected, 129 (27.1%) of spawned A. rhombeus. Mussels that spawned eggs, embryos, and larva of A. rhombeus (46.3 ± 4.55 mm, n = 129) were larger than than those that did not spawn (42.6 ± 8.51 mm, n = 347). The appearance frequency of A. rhombeus larva before and after the formation of lens was 99.8% (n = 597) vs. 0.2% (n = 1) from October 2015 to March 2016, 25.6% (n = 23) vs. 74.4% (n = 67) in April 2016, 0% (n = 0) vs. 100% (n = 40) on May 2016. The number of eggs, embryos, and larvae of A. rhombeus inside the mussels were 1-18 (5.6 ± 3.81). The number and appearance frequency of A. rhombeus eggs, embryos, and larvae inside the mussel according to mussel gill demibranchs position were 1 (0.01 ± 0.09, n = 1) and 0.78% in the left outer demibranch, 1-18 (2.33 ± 3.31, n = 63) and 48.84% in the left inner demibranch, 1-15 (2.97 ± 3.79, n = 76) and 58.91% in the right inner demibransh, and 1-12 (0.33 ± 1.71, n = 7) and 5.43% in the right outer demibransh. The highest frequency of the developmental position of eggs, embryos, and larvae occurred 71.8% (n = 445) in lower part 3 (L3) before formation lens and 94.4% (n = 102) in L3 after formation lens, indicating that L3 was dominating position for eggs, embryos, and larvae. More eggs, embryos, and larvae of A. rhombeus were found more often in the inner demibranshs than outer demibranchs. Since A. rhombeus is a species that spawn in the autumn and thus avoids the competition with interspecific and glochidia. However, they have to spend the winter in low water temperature. Consequently, we assume that A. rhombeus have evolved toward embryonic diapause under the low water temperature before the formation of lens and spawning inside the supracranchial cavity to save the transit energy from the water space to the suprabranchial cavity after the achieving movement ability with the formation of lens.

본 연구는 2015년 8월부터 2016년 7월까지 납지리의 말조개 내 산란과 적응특성을 조사하기 위해서 만경강 봉서천 일대에서 수행하였다. 납지리의 산란기는 9-11월까지로 추정되었고 성숙한 암컷에서 확인된 알수는 17-75개(36.2 ± 16.44)였다. 조사기간 동안 확인된 조개는 476개체이었고 납지리의 산란이 확인된 조개는 129개체(27.1%)였다. 납지리의 알과 자어가 산란된 조개(46.3 ± 4.55 mm, n = 129)가 산란되지 않은 조개(42.6 ± 8.51 mm, n = 347)보다 더 큰 것으로 나타났다. 안구가 형성되기 전 납지리 자어와 형성된 후 자어의 출현 비율은 2015년 10월부터 2016년 3월까지는 99.8% (n = 597) vs. 0.2% (n = 1)이었고, 4월에는 25.6% (n = 23) vs. 74.4% (n = 67), 5월에는 0% (n = 0) vs. 100% (n = 40)로 확인되었다. 말조개 안에서 확인된 납지리 알과 자어수는 1-18개(5.6 ± 3.81)로 나타났다. 아가미 위치에 따른 납지리 알과 자어수 및 출현빈도는 왼쪽 외반새 1개(0.01 ± 0.09, n = 1), 0.78%, 왼쪽 내반새 1-18개(2.33 ± 3.31, n = 63), 48.84%, 오른쪽 내반새 1-15개(2.97 ± 3.79, n = 76), 58.91%, 오른쪽 외반새 1-12개(0.33 ± 1.71, n = 7), 5.43%로 나타났다. 납지리 알과 자어의 아가미에서 발생위치는 안구 형성 전에는 lower part 3 (L3)에서 71.8% (n = 445), 안구 형성 후에는 L3에서 94.4% (n = 102)로 다른 부위보다 L3에서 모두 높게 나타났다. 납지리의 알과 자어수 및 출현빈도는 조개의 내반새가 외반새보다 높게 나타났다. 납지리는 추계산란종으로 다른 납자루아과 어류나 글로키디아 조개 유생과의 조개 안에서의 경쟁은 피하는 장점이 있지만 낮은 수온의 겨울을 보내야 한다. 이에 납지리는 안구형성 전인 낮은 수온에서는 배아적 휴면(embryonic diapause)을, 안구형성 후에는 수관에서 상새방으로의 이동에너지 절약을 위한 상새방 내 산란이라는 방향으로 적응해 온 것으로 판단된다.

Keywords

References

  1. Aldridge, D.(1999) Development of European bitterling in the gills of freshwater mussels. J. Fish. Biol. 54: 138-151. https://doi.org/10.1111/j.1095-8649.1999.tb00618.x
  2. Aldridge, D.C.(1997) Reproductive ecology of bitterling (Rhodeus sericeus Pallas) and Unionid mussels. Ph. D. Dissertation, Cambridge University, UK.
  3. Back, H.M. and H.B. Song(2005) Spawning in mussel and adaptation strategy of Acheilognathus signifer (Cyprinidae: Acheilognathinae). Korean J. Ichthyol. 17: 105-111. (in Korean with English abstract)
  4. Damme, V.D., N. Bogutskaya, R.C. Hoffimann and C. Smith(2007) The introduction of the European bitterling (Rhodeus amarus) to west and central Europe. Fish. Fish. 8: 79-106. https://doi.org/10.1111/j.1467-2679.2007.00239.x
  5. Denlinger, D.L. and P.A. Armbruster(2014) Mosquito diapause. Annu. Rev. Entomol. 59: 73-93. https://doi.org/10.1146/annurev-ento-011613-162023
  6. Denlinger, D.L.(2002) Regulation of diapause. Annu. Rev. Entomol. 47: 73-122. https://doi.org/10.1146/annurev.ento.47.091201.145137
  7. Kawamura, K. and K. Uehara(2005) Effects of temperature on free embryonic diapause in the autumn-spawning bitterling Acheilognathus rhombeus (Teleostei: Cyprinidae). J. Fish. Biol. 67: 684-695. https://doi.org/10.1111/j.0022-1112.2005.00769.x
  8. Ki, S.U., K.H. Kho and W.K. Lee(2019) Annual reproductive cycle of Acheilognathus rhombeus, in Korea. Dev. Reprod. 23: 323-331. https://doi.org/10.12717/DR.2019.23.4.323
  9. Kim, C.H., W.O. Lee, J.H. Lee and J.M. Beak(2011) Reproduction study of Korean endemic species Acheilognathus koreensis. Korean J. Ichthyol. 23: 150-157. (in Korean with English abstract)
  10. Kim, H.S., H. Yang, J.G. Ko and J.Y. Park(2014) Spawning pattern in the freshwater mussel Lamprotula leai and Unio douglasiae sinuolatus of Acheilognathus signifer (Pisces: Acheilognathinae). Korean J. Ichthyol. 26: 83-88. (in Korean with English abstract)
  11. Kim, H.S., H.S. Choi and Y.J. Park(2018) Embryonic development characteristics and host mussel utilization of flat bitterling Acheilognathus rhombeus (Cyprinidae) during winter in Korea. Environ. Biol. Fish. 101: 55-66. https://doi.org/10.1007/s10641-017-0680-4
  12. Kim, H.S., J.D. Yoon, H. Yang, H.S. Choi and J.H. Lee(2017) Reproductive characteristics of Rhodeus pseudosericeus (Pisces: Acheilognathinae) in the Heukcheon, Namhangang (River), Korea. Korean J. Ichthyol. 29: 235-243. (in Korean with English abstract)
  13. Kim, H.S., J.G. Ko, W.S. Choi and J.Y. Park(2015) Population ecology of Korean rose bitterling, Rhodeus uyekii (Pisces: Acheilognathinae) in the Bongseocheon, Mankyeonggang (river), Korea. Korean J. Ichthyol. 27: 78-85. (in Korean with English abstract)
  14. Kim, I.S. and J.Y. Park(2002) Freshwater Fishes of Korea. Kyohak Publishing, Seoul. 467pp. (in Korean)
  15. Kim, I.S.(1997) Illustrated encyclopedia of fauna and flora of Korea. Vol. 37. Freshwater fishes. Ministry of Education, Seoul. (in Korean)
  16. Kitamura, J.(2006a) Seasonal change in the spatial utilization of host mussels in relation to ovipositor length by female rosy bitterling Rhodeus ocellatus kurumeus. J. Fish. Biol. 65: 597-607. https://doi.org/10.1111/j.0022-1112.2004.00511.x
  17. Kitamura, J.(2006b) Reproductive ecology of the striped bitterling Acheilognathus cyanostigma (Cyprinidae: Acheilognathinae). Ichthyol. Res. 53: 216-222. https://doi.org/10.1007/s10228-006-0336-4
  18. Kitamura, J., T. Abe and J. Nakjima(2009) The reproductive ecology of two subspecies of the bitterling Rhodeus atremius (Cyprinidae, Acheilognathinae). Ichthyol. Res. 56: 156-161. https://doi.org/10.1007/s10228-008-0079-5
  19. Ko, M.H., I.S. Kim, J.Y. Park and Y.J. Lee(2007) Distribution and ecology of a land-locked ayu, Plecoglossus altivelis (Pisces: Osmeridae) in lake Okjeong, Korea. Korean J. Ichthyol. 19: 24-34. (in Korean with English abstract)
  20. Kwon, O.K, G.M. Park and J.S. Lee(1993) Coloured shells of Korea. Academy Publishing Company, Seoul. (in Korean)
  21. Love, D.C. and T.C. Shirley(1993) Parasitism of the golden king crab, Lithodes Aequispinus Benedict, 1895 (Decapoda, Anomura, Lithodidae) by a liparid fish. Crustaceana 65: 97-104. https://doi.org/10.1163/156854093X00414
  22. Mills, S.C. and J.D. Reynolds(2002) Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131: 473-478. https://doi.org/10.1007/s00442-002-0895-7
  23. Mills, S.C. and J.D. Reynolds(2003) The bitterling-mussel interaction as a test case for co-evolution. J. Fish. Biol. 63: 84-104. https://doi.org/10.1111/j.1095-8649.2003.00209.x
  24. Mills, S.C., M.I. Taylor and J.D. Reynolds(2005) Benefits and costs to mussels from ejecting bitterling embryos: A test of the evolutionary equilibrium hypothesis. Anim. Behav. 70: 30-37.
  25. Nakamura, M.(1969) Cyprinid fishes of Japan. Special publications of the research institute for natural resources, No. 4. Tokyo: Research Institute for Natural Resources. (in Japanese)
  26. Refsnider, J.M. and F.J. Janzen(2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu. Rev. Ecol. Evol. Syst. 41: 39-57. https://doi.org/10.1146/annurev-ecolsys-102209-144712
  27. Reichard, M., J. Bryja, M. Polacik and C. Smith(2001) No evidence for host specialization or host-race formation in the European bitterling (Rhoseus amarus), a fish that parasitizes freshwater mussels. Mol. Ecol. 20: 3631-3643. https://doi.org/10.1111/j.1365-294X.2011.05198.x
  28. Reichard, M., M. Polacik, A.S. Tarkan, R. Spence, O. Gaygusuz, E. Ercan, O. Ondrackova and C. Smith(2010) The bitterlingmussel coevoluionary relationship in areas of recent and ancient sympatry. Evolution 64: 3047-3056.
  29. Shimizu, A. and I. Hanyu(1981) Annual reproductive cycle of a spring-spawning bittering, Acheilognathus tabira. Bull. Jpn. Soc. Sci. Fish. 48: 1563-1568. https://doi.org/10.2331/suisan.48.1563
  30. Shimizu, A. and I. Hanyu(1993) Factors involved in the development of and decline in photoperiodism as it relates to the gonadal activity of spring-spawning bitterling, Acheilognathus tabira. J. Exp. Zool. 265: 134-143. https://doi.org/10.1002/jez.1402650205
  31. Shimizu, A., K. Aida and I. Hanyu(1987) Annual reproductive cycle in an autumn-spawning bitterling Acheilognathus rhombea. Bull. Jpn. Soc. Sci. Fish. 53:529-536. https://doi.org/10.2331/suisan.53.529
  32. Shimizu, A., K. Aida and I. Hanyu(1994) Effects of photoperiod and temperature on gonadal activity and plasma steroid levels in an autumn-spawning bitterling, Acheilognathus rhombea, during different phase of its annual reproductive cycle. Gen. Comp. Endocrinol. 93: 137-150. https://doi.org/10.1006/gcen.1994.1016
  33. Smith, C., M. Reichard, P. Jurajda and M. Przybylski(2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J. Zool. Lond. 262: 107-124. https://doi.org/10.1017/S0952836903004497
  34. Somerton, D.A. and W. Donaldson(1998) Parasitism of the golden king crab, Lithodes aequispinus, by two species of snailfish, genus Careproctus. Fish. Bull. 96: 871-884.
  35. Song, H.B. and O.K. Kwon(1994) Spawning of the bitterling, Acheilognathus yamatsutae (Cyprinidae) into the mussel. Korean J. Ichthyol. 6: 39-50. (in Korean with English abstract)
  36. Spence, R. and C. Smith(2013) Rose bitterling (Rhodeus ocellatus) embryos parasitize freshwater mussels by competing for nutrients and oxygen, Acta Zool. 94: 113-118. https://doi.org/10.1111/j.1463-6395.2011.00532.x
  37. Suzuki, N. and S.R. Jeon(1989) Development of the bitterling, Acanthorhodeus asmussi (Cyprinidae) with note on minute tubercles on the skin surface. Korean J. Ichthyol. 1: 73-82.
  38. Suzuki, N. and S.R. Jeon(1990a) Development of the bitterling, Acanthorhodeus (=Acheilognathus) gracilis (Cyprinidae), with a note on minute tubercles on the skin surface. Korean J. Ichthyol. 2: 169-181.
  39. Suzuki, N. and S.R. Jeon(1990b) Development of the bitterling, Acheilognathus lanceolatus from Ungchonriver. Korean J. Ichthyol. 2: 77-87.
  40. Suzuki, N. and S.R. Jeon(1991) Development of the bitterling, Acheilognathus rhombeus (Cyprinidae), from Korea. J. Basic. Sci. 5: 53-62.