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Effect of Water Temperature on Infectivity of the Parasitoid Amoebophrya sp. Infecting the Harmful Bloom-forming Dinoflagellate Akashiwo sanguinea

유해 적조생물 Akashiwo sanguinea를 감염시키는 포식성 기생생물 Amoebophrya sp.의 감염력에 대한 수온의 영향

YOUNGGYO JUNG1
,
SUNJU KIM1*
정 영교1
,
김 선주1*
1Department of Oceanography, Pukyong National University
1부경대학교 해양학과
*교신저자. *Corresponding Author. 
February 2018. pp. 20-31
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Abstract

포식 기생생물 Amoebophrya spp.는 적조를 유발하는 다양한 와편모류 종들을 감염시켜 적조를 제어하는 생물학적 요인으로 잘 알 려져 있다. 본 연구는 전 세계 연안에서 유해 적조를 유발하는 와편모류 Akashiwo sanguinea를 감염시키는 포식성 기생생물 Amoebophrya sp.의 감염력에 대해 물리적 환경요인으로서 수온이 미치는 영향에 대해 살펴보았다. 연구 결과, 적조생물 A. sanguinea에 대한 Amoebophrya의 감염력과 세대시간은 수온의 변화에 따라 크게 영향을 받는 것으로 나타났으며, 수온이 낮을수 록 숙주 세포내 발달이 급격하게 느려져서 기생생물의 총 세대시간이 25°C에서는 약 58 ± 0.1 h과 20°C에서는 83 ± 0.1 h, 15°C에 서는 115 ± 0.1 h의 범위를 나타내어 각 온도 조건에서 유의한 차이를 보였으며(p< > = >0.001), 온도가 낮을수록 포식성 기생생물의 총 세대시간이 크게 길어지는 것으로 나타났다. 또한 감염율은 25°C에서 71.5 ± 0.30%의 범위로 가장 높게 나타났고, 20°C와 15°C에 서는 각각 54.3 ± 1.68%와 29.6 ± 1.42%의 범위를 나타내어 온도가 낮아질수록 감염율이 크게 감소하는 것으로 나타났다. 이러한 연구결과는 저수온기에 발생한 A. sanguinea의 적조에는 포식 기생생물의 감염으로 인한 생물학적 제어 효과가 크게 감소하는 것 으로 판단된다. 뿐만 아니라, 숙주개체군의 거동과 관련하여 포식 기생생물의 감염력에 영향을 주는 요인으로서 수온이 하나의 주 요 변수로서 작용할 것으로 판단된다.

Marine parasitoid Amoebophrya infects and kills various bloom-forming dinoflagellates and strongly influences the harmful algal bloom dynamics. We investigated the effect of temperature on survival, infectivity, generation time of the parasite from the parasitoid Amoebophrya sp. and the harmful dinoflagellate host Akashiwo sanguinea system. Temperature had a significant effect on the parasite generation time and infectivity. While the lower temperature (15°C) arrested parasite intracellular development and infectivity, resulting in the longer generation time (115 ± 0.1 h), the higher temperatures (25°C and 20°C) accelerated the parasite development, with the generation times of 58 ± 0.1h and 83 ± 0.1h, respectively. Parasite prevalence (percent of host infected) was 71.5 ± 0.30%, 54.3 ± 1.68%, and 29.6 ± 1.42% at 25°C, 20°C, and 15°C, respectively. These results suggest that biological control by parasitism on A. sanguinea bloom would not be highly effective during low water temperature season. Further, water temperature would be an important factor of bottom-up controls for the host-parasite population dynamics.

Keywords
Akashiwo sanguinea
Amoebophrya
Infectivity
Parasitoid
Red tide

References
1
Bockstahler, K.R. and D.W. Coats, 1993. Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. J. Euk. Microbiol., 40: 49-60.
2
Botes, L., A.J. Smit, A.J. and P.A. Cook, 2003. The potential threat of algal blooms to the abalone (Haliotis midae) mariculture industry situated around the South African coast. Harmful Algae, 2: 247-259.
3
Cardwell, R.D., S. Olsen, M.I. Carr and E.W. Sanborn, 1979. Causes of oyster mortality in South Puget Sound. NOAA Tech. Mem. ERL MESA-39. Washington Department of Fisheries, Salmon Research and Development, Brinnan, Washington.
4
Chambouvet, A., P. Morin, D. Marie and L. Guillou, 2008. Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science, 322: 1254-1257.
5
Cleary, A.C. and E.G. Durbin, 2016. Unexpected prevalence of parasite 18SrDNA sequences in winter among Antarctic marine protists. J. Plankton Res., 38: 401-417.
6
Coats, D.W. and K.R. Bockstahler, 1994. Occurrence of the parasitic dinoflagellate Amoebophrya ceratii in Chesapeake Bay populations of Gymnodinium sanguineum. J. Eukaryot. Microbiol., 41: 586-593.
7
Coats, D.W. and M.G. Park, 2002. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): parasite survival, infectivity, generation time, and host specificity. J. Phycol., 38: 520-528.
8
Coats, D.W., E.J. Adam, C.L. Gallegos and S. Hedrick, 1996. Parasitism of photosynthetic dinoflagellates in a shallow subestuary of Chesapeake Bay, USA. Aquat. Microb. Ecol., 11: 1-9.
9
De Vargas, C., S. Audic, N. Henry, J. Decelle, F. Mahé, R. Logares et al., 2015. Eukaryotic plankton diversity in the sunlit ocean. Science, 348: 1261605.
10
Gomez, F. and F. Boicenco, 2004. An annotated checklist of dinoflagellates in the Black Sea. Hydrobiologia, 517: 43-759.
11
Gomez, F. and S. Souissi, 2008. The impact of the 2003 summer heat wave and the 2005 late cold wave on the phytoplankton in the north-eastern English Channel. C.R. Biol., 331: 678-685.
12
Guillard, R.R.L. and J.H. Ryther, 1962. Studies of marine planktonic diatom. Part I. Cyclotella nana Hustedt and Detonula confervadea (Cleve) Gran. Can. J. Microbiol., 8: 229-239.
13
Guillou, L., M. Viprey, A. Chambouvet, R.M. Welsh, A.R. Kirkham, R. Massana et al., 2008. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ. Microbiol., 10: 3349-3365.
14
Hallegraeff, G.M., 1991. Aquaculturists guide to harmful Australian microalgae. Fishing Industry training board of Tasmania/CSIRO division of fisheries, Hobart.
15
Hirasaka, K., 1922. On a case of discoloured sea water. Annot. Zool., Japan, 10: 161-164.
16
Jessup, D.A., M.A. Miller, J.P. Ryan, H.M. Nevins, H.A. Kerkering, A. Mekebri, D.B. Crane, T.A. Johnson and R.M. Kudela, 2009. Mass stranding of marine birds caused by a surfactant-producing red tide. PLoS ONE, 4: e4550.
17
Kiefer, D.A. and R. Lasker, 1975. Two blooms of Gymnodinium splendens, an unarmored dinoflagellate. Fish. Bull., 73: 675-678.
18
Kim, J.S., H.J. Jeong, Y.D. Yoo, N.S. Kang, S.K. Kim, J.Y. Song, M.J. Lee, S.T. Kim, J.H. Kang, K.A. Seong and W. Yih, 2013. Red tides in Masan Bay, Korea, in 2004-2005: III. Daily variation in the abundance of mesozooplankton and their grazing impacts on red-tide organisms. Harmful Algae, 30S: S102-S113.
19
Kim, S. and M.G. Park, 2014. Amoebophrya spp. from the bloom-forming dinoflagellate Cochlodinium polykrikoides: parasites not nested in the “Amoebophrya ceratii complex”. J. Eukaryot. Microbiol., 61: 173-181.
20
Kim, S., 2006. Patterns in host range for two strains of Amoebophrya (Dinophyta) infecting thecate dinoflagellates: Amoebophrya spp. ex Alexandrium affine and ex Gonyaulax polygramma. J. Phycol., 42: 1170-1173.
21
Kim, S., M.G. Park, W. Yih and D.W. Coats, 2004. Infection of the bloom-forming, thecate dinoflagellates Alexandrium affine and Gonyaulax spinifera by two strains of Amoebophrya (Dinophyta). J. Phycol., 40: 815-822.
22
Kim, Y.G., M.G. Park and W. Yih, 2002 Host-parasite system in a red tide dinoflagellate Prorocentrum minimum: (1) life cycle stages of the parasitic dinoflagellate Amoebophrya sp. J. Kor. Soc. Oceanogr., 7: 221-225.
23
Lee, C.K., O.H. Lee and S.M. Lee, 2005. Impacts of temperature, salinity and irradiance on the growth of ten harmful algal bloom-forming microalgae isolated in Korean coastal waters. J. Korean Soc. Oceanogr., 10: 79-91.
24
Lu, S.H. and I..J. Hodgkiss, 2004. Harmful algal bloom causative collected from Hong Kong waters. Hydrobiologia, 512: 231-28.
25
Luo, Z., W. Yang, C.P. Leaw, V. Pospelova, G. Bilien, G.R. Liow, P.T. Lim and H. Gu, 2017. Cryptic diversity within the harmful dinoflagellate Akashiwo sanguinea in coastal Chinese waters is related to differentiated ecological niches. Harmful Algae, 66: 88-96.
26
Martin, G.W., 1929. Dinoflagellates from marine and brackish waters of New Jersey. University of Iowa Studies in Natural History, 12: 1-32.
27
Matsubara, T., S. Nagasoe, T. Yamasaki, T. Shikata, Y. Shimasaki, Y. Oshima and T. Honjo, 2007. Effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea. J. Exp. Mar. Biol. Ecol., 342: 226-230.
28
Mazzillo, F.F.M., J.P. Ryan and M.W Silver, 2011. Parasitism as a biological control agent of dinoflagellate blooms in the California Current System. Harmful Algae, 10: 763-73.
29
Montagnes, D.J.S., A. Chambouvet, L. Guillou and A. Fenton, 2008 Can microzooplankton and parasite pressure be responsible for the demise of toxic dinoflagellate blooms? Aquatic. Microb. Ecol., 53: 201-210.
30
Nakamura, Y., M. Watanabe and M. Watanabe, 1982. The effect of various environmental factors on the growth yield of red tide algae. III. Gymnodinium splendens. Res. Rep. Natl. Inst. Environ. Stud., 30: 87-93.
31
NFRDI (National Fisheries Research and Development Institute), 2017. Harmful Algal Blooms in Korean Coastal Waters in 2016, 71pp.
32
Nishitani, L., R. Hood, J. Wakeman and K.K. Chew, 1984. Potential importance of an endoparasite of Gonyaulax in paralytic shellfish poisoning outbreaks. In: Seafood toxins, edited by Ragelis, E.P., ACS Symposium Ser., 262: 139-149.
33
Park, J.-G., H.-J. Hur, D. W. Coats, W. Yih and H. Na, 2007. Endoparasitic dinoflagellate, Amoebophrya spp. and their host dinoflagellates in Jinhae Bay, Korea. The Sea, 12: 359-369.
34
Park, M.G., S. Kim, E.-Y. Shin, W. Yih and D.W. Coats, 2013. Parasitism of harmful dinoflagellates in Korean coastal waters. Harmful Algae, 30: S62-S74.
35
Robinson, M.G. and L.N. Brown, 1983. A recurrent red tide in a British Columbian coastal lagoon. Can. J. Fish Aquat. Sci., 40: 2135-2143.
36
Son M.H. and S.H. Baek, 2012. Short-term dynamics of the red-tide dinoflagellate Akashiwo sanguinea. In: Preceedings of annual conference of the Society of Naval Architects of Korea, Daegu, 233p.
37
Taylor, F.J.R., 1968. Parasitism of the toxin-producing dinoflagellate Gonyaulax catenella by the endoparasitic dinoflagellate Amoebophrya ceratii. J. Fish. Res. Bd. Canada, 25: 2241-2245.
38
Velo-Suάrez, L., M.L. Brosnahan, D.M. Anderson and Jr., D.J McGillicuddy, 2013. A quantitative assessment of the role of the parasite Amoebophrya in the termination of Alexandrium fundyense blooms within a small coastal embayment. PLoS One, 8: e81150.
39
Worden, A.Z., M.J. Follows, S.J. Giovannoni, S. Wilken, A.E. Zimmerman, P.J. Keeling, 2015. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science, 347: 1257594-7.
40
Yih, W. and D.W. Coats, 2000. Infection of Gymnodinium sanguineum by the dinoflagellate Amoebophrya sp.: effect of nutrient environment on parasite generation time, reproduction, and infectivity. J. Eukaryot. Microbiol., 47: 504-510.
Information
  • Publisher :The Korean Society of Oceanography
  • Publisher(Ko) :한국해양학회
  • Journal Title :The Sea Journal of the Korean Society of Oceanography
  • Journal Title(Ko) :한국해양학회지 바다
  • Volume : 23
  • No :1
  • Pages :20-31
  • Received Date : 2018-01-25
  • Accepted Date : 2018-02-22
  • DOI :https://doi.org/10.7850/jkso.2017.23.1.020
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