Journal of Oceanography

, Volume 69, Issue 5, pp 511–526 | Cite as

Relationships of interannual variability in SST and phytoplankton blooms with giant jellyfish (Nemopilema nomurai) outbreaks in the Yellow Sea and East China Sea

  • Yongjiu Xu
  • Joji Ishizaka
  • Hisashi Yamaguchi
  • Eko Siswanto
  • Shengqiang Wang
Original Article
First Online:
Received:
Revised:
Accepted:

Abstract

Giant jellyfish (Nemopilema nomurai) outbreaks in relation to satellite sea surface temperature (SST) and chlorophyll-a concentrations (Chl-a) were investigated in the Yellow Sea and East China Sea (YECS) from 1998 to 2010. Temperature, eutrophication, and match–mismatch hypotheses were examined to explain long-term increases and recent reductions of N. nomurai outbreaks. We focused on the timing of SST reaching 15 °C, a critical temperature enabling polyps to induce strobilation and enabling released ephyra to grow. We analyzed the relationship of the timing with interannual variability of SST, Chl-a, and the timing of phytoplankton blooms. Different environmental characteristics among pre-jellyfish years (1998–2001), jellyfish years (2002–2007, 2009), and non-jellyfish years (2008, 2010) were assessed on this basis. The SST during late spring and early summer increased significantly from 1985 to 2007. This indicated that high SST is beneficial to the long-term increases in jellyfish outbreaks. SST was significantly lower in non-jellyfish years than in jellyfish years, suggesting that low SST might reduce the proliferation of N. nomurai. We identified three (winter, spring, and summer) major phytoplankton bloom regions and one summer decline region. Both Chl-a during non-blooming periods and the peak increased significantly from 1998 to 2010 in most of the YECS. This result indicates that eutrophication is beneficial to the long-term increases in jellyfish outbreaks. Timing of phytoplankton blooms varied interannually and spatially, and their match and mismatch to the timing of SST reaching 15 °C did not correspond to long-term increases in N. nomurai outbreaks and the recent absence.

Keywords

Interannual variability SST Satellite chlorophyll Jellyfish Outbreak 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank NASA/DAAC for providing AVHRR, SeaWiFS, and MODIS data. We also thank Professor Shin-ichi Uye for providing valuable information about the ecology and biology of giant jellyfish. We thank Professor Egil Sakshaug for scientific and writing support. Two anonymous reviewers and the editor also provided valuable comments on the manuscript. This work was funded by the Fisheries Agency of Japan as the “International Cooperative Study of Giant Jellyfish.”

Supplementary material

10872_2013_189_MOESM1_ESM.doc (120 kb)
Supplementary material 1 (DOC 120 kb)

References

  1. Ahn YH, Shanmugam P (2006) Detecting the red tide algal blooms from satellite ocean color observations in optically complex Northeast-Asia Coastal waters. Remote Sens Environ 103(4):419–437. doi: 10.1016/j.rse.2006.04.007 CrossRefGoogle Scholar
  2. Båmstedt U, Wild B, Martinussen M (2001) Significance of food type for growth of ephyrae Aurelia aurita (Scyphozoa). Mar Biol 139(4):641–650. doi: 10.1007/s002270100623 CrossRefGoogle Scholar
  3. Beardsley RC, Limeburner R, Yu H, Cannon GA (1985) Discharge of the Changjiang (Yangtze River) into the East China Sea. Cont Shelf Res 4(1–2):57–76CrossRefGoogle Scholar
  4. Chai CZ, Yu M, Song XX, Cao XH (2006) The Status and Characteristics of Eutrophication in the Yangtze River (Changjiang) Estuary and the Adjacent East China Sea China. Hydrobiologia 563(1):313–328. doi: 10.1007/s10750-006-0021-7 CrossRefGoogle Scholar
  5. Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–294. doi: 10.1016/S0065-2881(08)60202-3 CrossRefGoogle Scholar
  6. Durant JM, Hjermann DO, Anker-Nilssen T, Beaugrand G, Mysterud A, Pettorelli N, Stenseth NC (2005) Timing and abundance as key mechanisms affecting trophic interactions in variable environments. Ecol Lett 8:952–958. doi: 10.1111/j.1461-0248.2005.00798.x CrossRefGoogle Scholar
  7. Frank KT, Petrie B, Shackell NL (2007) The ups and downs of trophic control in continental shelf ecosystems. Trends Ecol Evol 22(5):236–242. doi: 10.1016/j.tree.2007.03.002 CrossRefGoogle Scholar
  8. Furuya K, Hayashi M, Yabushita Y (2003) Phytoplankton dynamics in the East China Sea in spring and summer as revealed by HPLC-derived pigment signatures. Deep Sea Res Part II 50:367–387. doi: 10.1016/S0967-0645(02)00460-5 CrossRefGoogle Scholar
  9. Gao XL, Song JM (2005) Phytoplankton distributions and their relationship with the environment in the Changjiang Estuary China. Mar Pollut Bull 50(3):327–335. doi: 10.1016/j.marpolbul.2004.11.004 CrossRefGoogle Scholar
  10. Gao C, Zhang T (2010) Eutrophication in a Chinese context: understanding various physical and socio-economic aspects. Ambio 39(5–6):385–393. doi: 10.1007/s13280-010-0040-5 CrossRefGoogle Scholar
  11. Gremillet D, Lewis S, Drapeau L, van Der Lingen CD, Huggett JA, Coetzee JC, Verheye HM, Daunt F, Wanless S, Ryan PG (2008) Spatial match-mismatch in the Benguela upwelling zone: should we expect chlorophyll and sea-surface temperature to predict marine predator distributions? J Appl Ecol 45(2):610–621. doi: 10.1111/j.1365-2664.2007.01447.x CrossRefGoogle Scholar
  12. Henson SA, Thomas AC (2007) Interannual variability in timing of bloom initiation in the California Current System. J Geophys Res 112(C08007):1–12. doi: 10.1029/2006JC003960 Google Scholar
  13. Hickox R (2000) Climatology and seasonal variability of ocean fronts in the East China, Yellow and Bohai seas from satellite SST data. Geophys Res Lett 27:2945–2948. doi: 10.1029/1999GL011223 CrossRefGoogle Scholar
  14. Hu C, Li D, Chen CS, Ge JZ, Muller-Karger FE, Liu JP, Yu F, He MX (2010) On the recurrent Ulva prolifera blooms in the Yellow Sea and East China Sea. J Geophys Res 115:C05017. doi: 10.1029/2009JC005561 CrossRefGoogle Scholar
  15. Jiao N, Zhang Y, Zeng Y (2007) Ecological anomalies in the East China Sea: impacts of the Three Gorges Dam? Water Res 41(41):1287–1293. doi: 10.1016/j.watres.2006.11.053 CrossRefGoogle Scholar
  16. Kang YS, Jung S, Zuenko Y, Choi I, Dolganova N (2012) Regional differences in the response of mesozooplankton to oceanographic regime shifts in the northeast Asian marginal seas. Prog Oceanogr 97:120–134. doi: 10.1016/j.pocean.2011.11.012 CrossRefGoogle Scholar
  17. Kaufman L, Rousseeuw PJ (1990) Finding Groups In Data: An Introduction to Cluster Analysis, John Wiley & Sons, p 368Google Scholar
  18. Kawahara MS, Uye S, Ohtsu K, Izumi H (2006) Unusual population explosion of the giant jellyfish Nemopilemia nomurai (Scyphozoa : Rhizostomeae) in East Asian waters. Mar Ecol Prog Ser 307:161–173. doi: 10.3354/meps307161 CrossRefGoogle Scholar
  19. Kawahara M, Ohtsu K, Uye S (2013) Bloom or non-bloom in the giant jellyfish Nemopilema nomurai (Schphozoa: Rhizostomeae): roles of dormant podocysts. J Plankton Res 35(1):213–217. doi: 10.1093/plankt/fbs074 CrossRefGoogle Scholar
  20. Kim HC, Yamaguchi H, Yoo S, Zhu JR, Okamura K, Kiyomoto YK, Tanaka K, Kim SW, Park T, Oh IS, Ishizaka J (2009) Distribution of Changjiang diluted water detected by satellite chlorophyll-a and its interannual variation during 1998–2007. J Oceanogr 65:129–135. doi: 10.1007/s10872-009-0013-0 CrossRefGoogle Scholar
  21. Kiorboe T, Nielsen TG (1994) Regulation of Zooplankton Biomass and Production in a Temperate, Coastal Ecosystem1 Copepods. Limnol Oceanogr 39(3):493–507CrossRefGoogle Scholar
  22. Lee HE, Yoon WD, Lim D (2008) Description of feeding apparatus and mechanism in nemopilema nomurai kishinouye (scyphozoa: rhizostomeae). Ocean Sci J 43(1):61–65. doi: 10.1007/BF03022432 CrossRefGoogle Scholar
  23. Li MT, Xu K, Watanabe M, Chen Z (2007) Long-term variations in dissolved silicate, nitrogen, and phosphorus flux from the Yangtze River into the East China Sea and impacts on estuarine ecosystem. Estuar Coast Shelf S 71(1–2):3–12. doi: 10.1016/j.ecss.2006.08.013 CrossRefGoogle Scholar
  24. Lin C, Ning X, Su J, Lin Y, Xu B (2005) Environmental changes and the responses of the ecosystem of the Yellow Sea during 1976–2000. J Mar Sys 55(3–4):223–234. doi: 10.1016/j.jmarsys.2004.08.001 CrossRefGoogle Scholar
  25. Lynam CP, Hay SJ, Brierley AS (2004) Interannual variability in abundance of North Sea jellyfish and links to the North Atlantic Oscillation. Limnol Oceanogr 49(3):637–643. doi: 10.4319/lo.2004.49.3.0637 CrossRefGoogle Scholar
  26. Lynam CP, Hay SJ, Brierley AS (2005) Jellyfish abundance and climatic variation: contrasting responses in oceanographically distinct regions of the North Sea, and possible implications for fisheries. J Mar Bio Assoc UK 85:435–450. doi: 10.1017/S0025315405011380 CrossRefGoogle Scholar
  27. Michael PF, Proschan MA (2010) Wilcoxon-Mann-Whitney or t-test? On assumptions for hypothesis tests and multiple interpretations of decision rules. Stat Surv 4:1–39. doi: 10.1214/09-SS051 CrossRefGoogle Scholar
  28. Minnett PJ, Evans RH, Kearns EJ, Brown OB (2002) Sea-surface temperature measured by the Moderate Resolution Imaging Spectroradiometer (MODIS). In: IEEE International Geosciences and Remote Sensing Symposium. Toronto, CanadaGoogle Scholar
  29. Platt T, Sathyendranath S, Fuentes-Yaco C (2007) Biological oceanography and fisheries management: perspective after 10 years. ICES J Mar Sci 64:863–869. doi: 10.1093/icesjms/fsm072 CrossRefGoogle Scholar
  30. Purcell JE (2012) Jellyfish and Ctenophore Blooms Coincide with Human Proliferations and Environmental Perturbations. Annu Rev Marine Sci 4:209–235. doi: 10.1146/annurev-marine-120709-142751 CrossRefGoogle Scholar
  31. Purcell JE, Uye S, Lo WT (2007) Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Mar Ecol Prog Ser 350:153–174. doi: 10.3354/meps07093 CrossRefGoogle Scholar
  32. Purcell JE, Hoover RA, Schwarck NT (2009) Interannual variation of strobilation by the scyphozoan Aurelia labiata in relation to polyp density, temperature, salinity, and light conditions in situ. Mar Ecol Prog Ser 375:139–149. doi: 10.3354/meps07785 CrossRefGoogle Scholar
  33. Richardson AJ, Andrew B, Hays GC, Gibbons MJ (2009) The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol 24(6):312–322. doi: 10.1016/j.tree.2009.01.010 CrossRefGoogle Scholar
  34. Siswanto E, Nakata H, Matsuoka Y, Tanaka K, Kiyomoto Y, Okamura K, Zhu JR, Ishizaka J (2008) The long-term freshening and nutrient increases in summer surface water in the northern East China Sea in relation to Changjiang discharge variation. J Geophys Res 113:C10030. doi: 10.1029/2008JC004812 CrossRefGoogle Scholar
  35. Siswanto E, Tang J, Yamaguchi H, Ahn YH, Ishizaka J, Yoo S, Kim SW, Kiyomoto Y, Yamada K, Chiang C, Kawamura H (2011) Empirical ocean-color algorithms to retrieve chlorophyll-a, total suspended matter, and colored dissolved organic matter absorption coefficient in the Yellow and East China Seas. J Oceanogr 67(5):627–650. doi: 10.1007/s10872-011-0062-z CrossRefGoogle Scholar
  36. Sommer U, Lengfellner K (2008) Climate change and the timing, magnitude, and composition of the phytoplankton spring bloom. Global Change Biol 14(6):1199–1208. doi: 10.1111/j.1365-2486.2008.01571.x CrossRefGoogle Scholar
  37. Tang DL, Di BP, Wei GF, Ni IH, Oh IS, Wang SF (2006) Spatial, seasonal and species variations of harmful algal blooms in the South Yellow Sea and East China Sea. Hydrobiologia 568(1):245–253. doi: 10.1007/s10750-006-0108-1 CrossRefGoogle Scholar
  38. Toyokawa M, Shibata M, Cheng JH, Li HY, Ling JZ, Lin N, Liu ZL, Zhang Y, Shimizu M, Akiyama H (2012) First record of wild ephyrae of the giant jellyfish Nemopilema nomurai. Fisheries Sci 78(6):1213–1218. doi: 10.1007/s12562-012-0550-0 CrossRefGoogle Scholar
  39. Uye S (2008) Blooms of the giant jellyfish Nemopilema nomurai: a threat to the fisheries sustainability of the East Asian Marginal Seas. Plankton Benthos Res 3(Suppl):125–131CrossRefGoogle Scholar
  40. Uye S (2011) Human forcing of the copepod-fish-jellyfish triangular trophic relationship. Hydrobiologia 666(1):71–83. doi: 10.1007/s10750-010-0208-9 CrossRefGoogle Scholar
  41. Vantrepotte V, Melin F (2009) Temporal variability of 10-year global SeaWiFS time-series of phytoplankton chlorophyll a concentration. ICES J Mar Sci 66:1547–1556. doi: 10.1093/icesjms/fsp107 CrossRefGoogle Scholar
  42. Wang B (2006) Cultural eutrophication in the Changjiang (Yangtze River) plume: history and perspective. Estuar Coast Shelf S 69:471–477. doi: 10.1016/j.ecss.2006.05.010 CrossRefGoogle Scholar
  43. Wang JJ, Tang DL, Su Y (2010) Winter phytoplankton bloom induced by subsurface upwelling and mixed layer entrainment southwest of Luzon Strait. J Mar Sys 83(3–4):141–149. doi: 10.1016/j.jmarsys.2010.05.006 CrossRefGoogle Scholar
  44. Yamada K, Ishizaka J (2006) Estimation of interdecadal change of spring bloom timing, in the case of the Japan Sea. Geophys Res Lett 33:L02608. doi: 10.1029/2005GL024792 CrossRefGoogle Scholar
  45. Yamaguchi H, Kim HC, Son YB, Kim SW, Okamura K, Kiyomoto Y, Ishizaka J (2012) Seasonal and summer interannual variations of SeaWiFS chlorophyll a in the Yellow Sea and East China Sea. Prog Oceanogr 105:22–29. doi: 10.1016/j.pocean.2012.04.004 CrossRefGoogle Scholar
  46. Yamaguchi H, Ishizaka J, Siswanto E, Son YB, Yoo S, Kiyomoto Y (2013) Seasonal and spring interannual variations in satellite-observed chlorophyll-a in the Yellow and East China Seas: new datasets with reduced interference from high concentration of resuspended sediment. Cont Shelf Res 59:1–9. doi: 10.1016/j.csr.2013.03.009 CrossRefGoogle Scholar
  47. Yasuda T (2004) On the unusual occurrence of the giant medusa Nemopilema nomurai in Japanese waters. Nippon Suisan Gakkaishi 70:380–386 (in Japanese with English abstract)Google Scholar
  48. Zervoudaki S, Nielsen TG, Carstensen J (2009) Seasonal succession and composition of the zooplankton community along an eutrophication and salinity gradient exemplified by Danish waters. J Plankton Res 31(12):1475–1492. doi: 10.1093/plankt/fbp084 CrossRefGoogle Scholar
  49. Zhai L, Platt T, Tang C, Sathyendranath S, Walls RH (2011) Phytoplankton phenology on the Scotian Shelf. ICES J Mar Sci 68(4):781–791. doi: 10.1093/icesjms/fsq175 CrossRefGoogle Scholar
  50. Zhang J, Liu SM, Ren JL, Wu Y, Zhang GL (2007) Nutrient gradients from the eutrophic Changjiang (Yangtze River) Estuary to the oligotrophic Kuroshio waters and reevaluation of budgets for the East China Sea Shelf. Prog Oceanogr 74(4):449–478. doi: 10.1016/j.pocean.2007.04.019 CrossRefGoogle Scholar
  51. Zhou M, Shen Z, Yu R (2008) Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Cont Shelf Res 28:1483–1489. doi: 10.1016/j.csr.2007.02.009 CrossRefGoogle Scholar

Copyright information

© The Oceanographic Society of Japan and Springer Japan 2013

Authors and Affiliations

  • Yongjiu Xu
    • 1
  • Joji Ishizaka
    • 2
  • Hisashi Yamaguchi
    • 3
  • Eko Siswanto
    • 4
  • Shengqiang Wang
    • 1
  1. 1.Graduate School of Environmental StudiesNagoya UniversityNagoyaJapan
  2. 2.Hydrospheric Atmospheric Research CenterNagoya UniversityNagoyaJapan
  3. 3.Earth Observation Research Center, Japan Aerospace Exploration AgencyTsukubaJapan
  4. 4.Research Institute for Global Change, Japan Agency for Marine-Earth Science and TechnologyYokosukaJapan

Personalised recommendations