Journal of Oceanography

, Volume 69, Issue 5, pp 601–618

Impacts of elevated CO2 on particulate and dissolved organic matter production: microcosm experiments using iron-deficient plankton communities in open subarctic waters

  • Takeshi Yoshimura
  • Koji Suzuki
  • Hiroshi Kiyosawa
  • Tsuneo Ono
  • Hiroshi Hattori
  • Kenshi Kuma
  • Jun Nishioka
Original Article

Abstract

Response of phytoplankton to increasing CO2 in seawater in terms of physiology and ecology is key to predicting changes in marine ecosystems. However, responses of natural plankton communities especially in the open ocean to higher CO2 levels have not been fully examined. We conducted CO2 manipulation experiments in the Bering Sea and the central subarctic Pacific, known as high nutrient and low chlorophyll regions, in summer 2007 to investigate the response of organic matter production in iron-deficient plankton communities to CO2 increases. During the 14-day incubations of surface waters with natural plankton assemblages in microcosms under multiple pCO2 levels, the dynamics of particulate organic carbon (POC) and nitrogen (PN), and dissolved organic carbon (DOC) and phosphorus (DOP) were examined with the plankton community compositions. In the Bering site, net production of POC, PN, and DOP relative to net chlorophyll-a production decreased with increasing pCO2. While net produced POC:PN did not show any CO2-related variations, net produced DOC:DOP increased with increasing pCO2. On the other hand, no apparent trends for these parameters were observed in the Pacific site. The contrasting results observed were probably due to the different plankton community compositions between the two sites, with plankton biomass dominated by large-sized diatoms in the Bering Sea versus ultra-eukaryotes in the Pacific Ocean. We conclude that the quantity and quality of the production of particulate and dissolved organic matter may be altered under future elevated CO2 environments in some iron-deficient ecosystems, while the impacts may be negligible in some systems.

Keywords

CO2 Ocean acidification Phytoplankton response Organic matter production Elemental stoichiometry Iron availability Bering Sea North Pacific 

Supplementary material

10872_2013_196_MOESM1_ESM.ppt (466 kb)
Supplementary material (PPT 466 kb)

References

  1. Aguilar-Islas A, Hurst M, Buck K, Sohst B, Smith G, Lohan M, Bruland K (2007) Micro- and macronutrients in the southeastern Bering Sea: insight into iron-replete and iron-depleted regimes. Prog Oceanogr 73(2):99–126. doi:10.1016/j.pocean.2006.12.002 CrossRefGoogle Scholar
  2. Aoyama M, Becker S, Dai M, Daimon H, Gordon LI, Kasai H, Kerouel R, Kress N, Masten D, Murata A, Nagai N, Ogawa H, Ota H, Saito H, Saito K, Shimizu T, Takano H, Tsuda A, Yokouchi K, Youenou A (2007) Recent comparability of oceanographic nutrients data: results of a 2003 intercomparison exercise using reference materials. Anal Sci 23(9):1151–1154CrossRefGoogle Scholar
  3. Biswas H, Gadi S, Ramana V, Bharathi M, Priyan R, Manjari D, Kumar M (2012) Enhanced abundance of tintinnids under elevated CO2 level from coastal Bay of Bengal. Biodivers Conserv 21(5):1309–1326. doi:10.1007/s10531-011-0209-7 CrossRefGoogle Scholar
  4. Boyd PW, Jickells T, Law CS, Blain S, Boyle EA, Buesseler KO, Coale KH, Cullen JJ, de Baar HJ, Follows M, Harvey M, Lancelot C, Levasseur M, Owens NP, Pollard R, Rivkin RB, Sarmiento J, Schoemann V, Smetacek V, Takeda S, Tsuda A, Turner S, Watson AJ (2007) Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315(5812):612–617. doi:10.1126/science.1131669 CrossRefGoogle Scholar
  5. Breitbarth E, Bellerby RJ, Neill CC, Ardelan MV, Meyerh’Ufer M, Z’Ullner E, Croot PL, Riebesell U (2010) Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences 7(3):1065–1073. doi:10.5194/bg-7-1065-2010 CrossRefGoogle Scholar
  6. Brzezinski MA (1985) The Si: C: N ratio of marine diatoms: interspecific variability and the effect of some environmental variables. J Phycol 21(3):347–357. doi:10.1111/j.0022-3646.1985.00347.x CrossRefGoogle Scholar
  7. Bucciarelli E, Pondaven P, Sarthou G (2010) Effects of an iron-light co-limitation on the elemental composition (Si, C, N) of the marine diatoms Thalassiosira oceanica and Ditylum brightwellii. Biogeosciences 7(2):657–669. doi:10.5194/bg-7-657-2010 CrossRefGoogle Scholar
  8. Buitenhuis ET, Geider RJ (2010) A model of phytoplankton acclimation to iron-light colimitation. Limnol Oceanogr 55(2):714–724CrossRefGoogle Scholar
  9. Chierici M, Fransson A, Nojiri Y (2006) Biogeochemical processes as drivers of surface fCO2 in contrasting provinces in the subarctic North Pacific Ocean. Glob Biogeochem Cycles 20: GB1009. doi:10.1029/2004GB002356
  10. Culberson CH, Pytkowicz RM, Hawley JE (1970) Seawater alkalinity determination by the pH method. J Mar Res 28:15–21Google Scholar
  11. Dickson AG (1990) Standard potential of the reaction: AgCl(s) + 1/2H2(g) = Ag(s) + HCl(aq), and and the standard acidity constant of the ion HSO4 in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodynamics 22(2):113–127. doi:10.1016/0021-9614(90)90074-z CrossRefGoogle Scholar
  12. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res 34(10):1733–1743CrossRefGoogle Scholar
  13. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Res 1(1):169–192. doi:10.1146/annurev.marine.010908.163834 CrossRefGoogle Scholar
  14. Endo H, Yoshimura T, Kataoka T, Suzuki K (2013) Effects of CO2 and iron availability on phytoplankton and eubacterial community compositions in the northwest subarctic Pacific. J Exp Mar Biol Ecol 439:160–175. doi:10.1016/j.jembe.2012.11.003 CrossRefGoogle Scholar
  15. Feng Y, Hare CE, Leblanc K, Rose JM, Zhang Y, DiTullio GR, Lee PA, Wilhelm SW, Rowe JM, Sun J, Nemcek N, Gueguen C, Passow U, Benner I, Brown C, Hutchins DA (2009) Effects of increased pCO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response. Mar Ecol Prog Ser 388:13–25CrossRefGoogle Scholar
  16. Feng Y, Hare CE, Rose JM, Handy SM, DiTullio GR, Lee PA, Smith WO Jr, Peloquin J, Tozzi S, Sun J, Zhang Y, Dunbar RB, Long MC, Sohst B, Lohan M, Hutchins DA (2010) Interactive effects of iron, irradiance and CO2 on Ross Sea phytoplankton. Deep Sea Res I 57(3):368–383CrossRefGoogle Scholar
  17. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281(5374):237–240. doi:10.1126/science.281.5374.237 CrossRefGoogle Scholar
  18. Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64(9):3352–3358Google Scholar
  19. Gao K, Xu J, Gao G, Li Y, Hutchins DA, Huang B, Wang L, Zheng Y, Jin P, Cai X, Hader D-P, Li W, Xu K, Liu N, Riebesell U (2012) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nature Clim Change 2(7):519–523. doi:10.1038/nclimate1507 Google Scholar
  20. Geider RJ (1987) Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol 106:1–34CrossRefGoogle Scholar
  21. Geider RJ, La Roche J (1994) The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynth Res 39(3):275–301. doi:10.1007/bf00014588 CrossRefGoogle Scholar
  22. Gifford DJ, Caron DA (2000) Sampling, preservation, enumeration and biomass of marine protozooplankton. In: Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M (eds) ICES Zooplankton Methodology Manual. Academic, London, pp 193–221. doi:10.1016/b978-012327645-2/50006-2
  23. Grossart HP, Allgaier M, Passow U, Riebesell U (2006) Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol Oceanogr 51(1):1–11CrossRefGoogle Scholar
  24. Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of Seawater Analysis, 3rd edn. Wiley-VCH, Weinheim, pp 159–228. doi:10.1002/9783527613984.ch10
  25. Hare CE, Leblanc K, DiTullio GR, Kudela RM, Zhang Y, Lee PA, Riseman S, Hutchins DA (2007) Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Mar Ecol Prog Ser 352:9–16CrossRefGoogle Scholar
  26. Harrison PJ, Whitney FA, Tsuda A, Saito H, Tadokoro K (2004) Nutrient and plankton dynamics in the NE and NW gyres of the subarctic Pacific Ocean. J Oceanogr 60(1):93–117CrossRefGoogle Scholar
  27. Holmes RM, Aminot A, Kerouel R, Hooker BA, Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56(10):1801–1808Google Scholar
  28. Hopkinson BM, Xu Y, Shi D, McGinn PJ, Morel FMM (2010) The effect of CO2 on the photosynthetic physiology of phytoplankton in the Gulf of Alaska. Limnol Oceanogr 55(5):2011–2024CrossRefGoogle Scholar
  29. Hopkinson BM, Dupont CL, Allen AE, Morel FMM (2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proc Natl Acad Sci USA 108(10):3830–3837. doi:10.1073/pnas.1018062108 CrossRefGoogle Scholar
  30. Hutchins DA, Mulholland MR, Fu F (2009) Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22(4):128–145CrossRefGoogle Scholar
  31. Johnson KM, King AE, Sieburth JM (1985) Coulometric TCO2 analyses for marine studies; an introduction. Mar Chem 16(1):61–82. doi:10.1016/0304-4203(85)90028-3 CrossRefGoogle Scholar
  32. Kim JM, Lee K, Shin K, Kang JH, Lee HW, Kim M, Jang PG, Jang MC (2006) The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnol Oceanogr 51(4):1629–1636CrossRefGoogle Scholar
  33. Langer G, Nehrke G, Probert I, Ly J, Ziveri P (2009) Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6(11):2637–2646CrossRefGoogle Scholar
  34. Lee K, Tong LT, Millero FJ, Sabine CL, Dickson AG, Goyet C, Park GH, Wanninkhof R, Feely RA, Key RM (2006) Global relationships of total alkalinity with salinity and temperature in surface waters of the world’s oceans. Geophys Res Lett 33(19):L19605. doi:10.1029/2006GL027207 CrossRefGoogle Scholar
  35. Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10(12):1170–1181. doi:10.1111/j.1461-0248.2007.01117.x CrossRefGoogle Scholar
  36. Liu H, Suzuki K, Saino T (2002) Phytoplankton growth and microzooplankton grazing in the subarctic Pacific Ocean and the Bering Sea during summer 1999. Deep Sea Res I 49(2):363–375. doi:10.1016/s0967-0637(01)00056-5 CrossRefGoogle Scholar
  37. Mahowald NM, Engelstaedter S, Luo C, Sealy A, Artaxo P, Benitez-Nelson C, Bonnet S, Chen Y, Chuang PY, Cohen DD, Dulac F, Herut B, Johansen AM, Kubilay N, Losno R, Maenhaut W, Paytan A, Prospero JM, Shank LM, Siefert RL (2009) Atmospheric iron deposition: global distribution, variability, and human perturbations. Annu Rev Mar Res 1(1):245–278. doi:10.1146/annurev.marine.010908.163727 CrossRefGoogle Scholar
  38. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18(6):897–907CrossRefGoogle Scholar
  39. Millero FJ, Woosley R, DiTrolio B, Waters J (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22(4):72–85CrossRefGoogle Scholar
  40. Mochizuki M, Shiga N, Saito M, Imai K, Nojiri Y (2002) Seasonal changes in nutrients, chlorophyll a and the phytoplankton assemblage of the western subarctic gyre in the Pacific Ocean. Deep-Sea Res II 49(24–25):5421–5439. doi:10.1016/s0967-0645(02)00209-6 CrossRefGoogle Scholar
  41. Moore JK, Lindsay K, Doney SC, Long MC, Misumi K (2013) Marine ecosystem dynamics and biogeochemical cycling in the community earth system model [CESM1(BGC)]: comparison of the 1990s with the 2090s under the RCP4.5 and RCP8.5 Scenarios. J Clim. doi:10.1175/JCLI-D-12-00566.1
  42. Nagata T (2000) Production mechanisms of dissolved organic matter. In: Kirchmann DL (ed) Microbial Ecology of the Oceans. Wiley-Liss, New York, pp 121–152Google Scholar
  43. Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanogr 55(3–4):287–333. doi:10.1016/s0079-6611(02)00138-6 CrossRefGoogle Scholar
  44. Pierrot D, Lewis E, Wallace DWR (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, TennesseeGoogle Scholar
  45. Price NM (2005) The elemental stoichiometry and composition of an iron-limited diatom. Limnol Oceanogr 50(4):1159–1171CrossRefGoogle Scholar
  46. Putt M, Stoecker DK (1989) An experimentally determined carbon: volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34(6):1097–1103CrossRefGoogle Scholar
  47. Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms on the composition of seawater. In: Hill MN (ed) The Sea, vol 2. Wiley, New York, pp 26–77Google Scholar
  48. Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Res 3:291–315CrossRefGoogle Scholar
  49. Ridal JJ, Moore RM (1990) A re-examination of the measurement of dissolved organic phosphorus in seawater. Mar Chem 29:19–31. doi:10.1016/0304-4203(90)90003-u CrossRefGoogle Scholar
  50. Riebesell U, Wolf-Gladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361(6409):249–251CrossRefGoogle Scholar
  51. Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, Meyerhofer M, Neill C, Nondal G, Oschlies A, Wohlers J, Zollner E (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450(7169):545–548. doi:10.1038/nature06267 CrossRefGoogle Scholar
  52. Roberts K, Granum E, Leegood R, Raven J (2007) Carbon acquisition by diatoms. Photosynth Res 93(1–3):79–88. doi:10.1007/s11120-007-9172-2 CrossRefGoogle Scholar
  53. Rose JM, Feng Y, Gobler CJ, Gutierrez R, Hare CE, Leblanc K, Hutchins DA (2009) Effects of increased pCO2 and temperature on the North Atlantic spring bloom. II. Microzooplankton abundance and grazing. Mar Ecol Prog Ser 388:27–40CrossRefGoogle Scholar
  54. Shi D, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron availability to marine phytoplankton. Science 327(5966):676–679CrossRefGoogle Scholar
  55. Strathmann RR (1967) Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol Oceanogr 12:411–418CrossRefGoogle Scholar
  56. Strickland JDH (1960) Measuring the production of marine phytoplankton. Fish Res Bd Can Bull 122:1–172Google Scholar
  57. Sugie K, Yoshimura T (2013) Effects of pCO2 and iron on the elemental composition and cell geometry of the marine diatom Pseudo-nitzschia pseudodelicatissima (Bacillariophyceae). J Phycol 49(3):475–488. doi:10.1111/jpy.12054
  58. Sunda WG (2010) Iron and the carbon pump. Science 327(5966):654–655. doi:10.1126/science.1186151 CrossRefGoogle Scholar
  59. Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N. N-dimethylformamide. J Oceanogr 46(4):190–194Google Scholar
  60. Suzuki K, Handa N, Nishida T, Wong CS (1997) Estimation of phytoplankton succession in a fertilized mesocosm during summer using high-performance liquid chromatographic analysis of pigments. J Exp Mar Biol Ecol 214(1–2):1–17. doi:10.1016/s0022-0981(97)00003-8 CrossRefGoogle Scholar
  61. Suzuki K, Liu H, Saino T, Obata H, Takano M, Okamura K, Sohrin Y, Fujishima Y (2002) East-west gradients in the photosynthetic potential of phytoplankton and iron concentration in the subarctic Pacific Ocean during early summer. Limnol Oceanogr 47(6):1581–1594CrossRefGoogle Scholar
  62. Suzuki K, Hinuma A, Saito H, Kiyosawa H, Liu H, Saino T, Tsuda A (2005) Responses of phytoplankton and heterotrophic bacteria in the northwest subarctic Pacific to in situ iron fertilization as estimated by HPLC pigment analysis and flow cytometry. Prog Oceanogr 64(2–4):167–187. doi:10.1016/j.pocean.2005.02.007 CrossRefGoogle Scholar
  63. Takata H, Kuma K, Iwade S, Isoda Y, Kuroda H, Senjyu T (2005) Comparative vertical distributions of iron in the Japan Sea, the Bering Sea, and the western North Pacific Ocean. J Geophys Res 110(7):1–10Google Scholar
  64. Takeda S (1998) Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters. Nature 393(6687):774–777CrossRefGoogle Scholar
  65. Takeda S (2011) Iron and phytoplankton growth in the subarctic North Pacific. Aqua-BioSci Monogr 4(2):41–93. doi:10.5047/absm.2011.00402.0041 CrossRefGoogle Scholar
  66. Taucher J, Schulz KG, Dittmar T, Sommer U, Oschlies A, Riebesell U (2012) Enhanced carbon overconsumption in response to increasing temperatures during a mesocosm experiment. Biogeosciences 9:3531–3545. doi:10.5194/bg-9-3531-2012 CrossRefGoogle Scholar
  67. Taylor AH, Geider RJ, Gilbert FJH (1997) Seasonal and latitudinal dependencies of phytoplankton carbon-to-chlorophyll a ratios: results of a modelling study. Mar Ecol Prog Ser 152:51–66CrossRefGoogle Scholar
  68. Taylor BW, Keep CF, Hall RO, Koch BJ, Tronstad LM, Flecker AS, Ulseth AJ (2007) Improving the fluorometric ammonium method: matrix effects, background fluorescence, and standard additions. J North Am Benthol Soc 26(2):167–177. doi:10.1899/0887-3593 CrossRefGoogle Scholar
  69. Thingstad TF, Bellerby RGJ, Bratbak G, Borsheim KY, Egge JK, Heldal M, Larsen A, Neill C, Nejstgaard J, Norland S, Sandaa RA, Skjoldal EF, Tanaka T, Thyrhaug R, Topper B (2008) Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455(7211):387–390. doi:10.1038/nature07235 CrossRefGoogle Scholar
  70. Tomas CR (1997) Identifying Marine Phytoplankton. Academic, San DiegoGoogle Scholar
  71. Tortell PD, Payne CD, Li Y, Trimborn S, Rost B, Smith WO, Riesselman C, Dunbar RB, Sedwick P, DiTullio GR (2008) CO2 sensitivity of Southern Ocean phytoplankton. Geophys Res Lett 35 (L04605). doi:10.1029/2007GL032583
  72. Trimborn S, Wolf-Gladrow D, Richter KU, Rost B (2009) The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms. J Exp Mar Biol Ecol 376(1):26–36CrossRefGoogle Scholar
  73. Uye S-I, Nagano N, Tamaki H (1996) Geographical and seasonal variations in abundance, biomass and estimated production rates of microzooplankton in the Inland Sea of Japan. J Oceanogr 52(6):689–703. doi:10.1007/bf02239460 CrossRefGoogle Scholar
  74. Verity PG, Lagdon C (1984) Relationships between lorica volume, carbon, nitrogen, and ATP content of tintinnids in Narragansett Bay. J Plank Res 6(5):859–868. doi:10.1093/plankt/6.5.859 CrossRefGoogle Scholar
  75. Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39(8):1985–1992CrossRefGoogle Scholar
  76. Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7(9):2915–2923. doi:10.5194/bg-7-2915-2010 CrossRefGoogle Scholar
  77. Yamada N, Suzumura M (2010) Effects of seawater acidification on hydrolytic enzyme activities. J Oceanogr 66(2):233–241. doi:10.1007/s10872-010-0021-0 CrossRefGoogle Scholar
  78. Yoshimura T, Nishioka J, Nakatsuka T (2010a) Iron nutritional status of the phytoplankton assemblage in the Okhotsk Sea during summer. Deep-Sea Res I 57(11):1454–1464. doi:10.1016/j.dsr.2010.08.003 CrossRefGoogle Scholar
  79. Yoshimura T, Nishioka J, Suzuki K, Hattori H, Kiyosawa H, Watanabe YW (2010b) Impacts of elevated CO2 on organic carbon dynamics in nutrient depleted Okhotsk Sea surface waters. J Exp Mar Biol Ecol 395(1–2):191–198. doi:10.1016/j.jembe.2010.09.001 CrossRefGoogle Scholar
  80. Zubkov MV, Sleigh MA, Tarran GA, Burkill PH, Leakey RJG (1998) Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S. Deep-Sea Res I 45(8):1339–1355. doi:10.1016/s0967-0637(98)00015-6 CrossRefGoogle Scholar

Copyright information

© The Oceanographic Society of Japan and Springer Japan 2013

Authors and Affiliations

  • Takeshi Yoshimura
    • 1
  • Koji Suzuki
    • 2
  • Hiroshi Kiyosawa
    • 3
  • Tsuneo Ono
    • 4
  • Hiroshi Hattori
    • 5
  • Kenshi Kuma
    • 6
  • Jun Nishioka
    • 7
  1. 1.Central Research Institute of Electric Power IndustryAbikoJapan
  2. 2.Faculty of Environmental Earth ScienceHokkaido UniversitySapporoJapan
  3. 3.Marine Biological Research Institute of JapanShinagawaJapan
  4. 4.Hokkaido National Fisheries Research InstituteFisheries Research AgencyKushiroJapan
  5. 5.Department of Marine Biology and SciencesTokai UniversitySapporoJapan
  6. 6.Graduate School of Fisheries Sciences and Faculty of FisheriesHokkaido UniversityHakodateJapan
  7. 7.Institute of Low Temperature ScienceHokkaido UniversitySapporoJapan

Personalised recommendations