DOI QR코드

DOI QR Code

Seasonal Whole-plant Carbon Balance of Phyllospadix iwatensis on the Coast of the Korean Peninsula

한반도 연안에 분포하는 새우말의 탄소수지 계절적 변동

  • SEUNG HYEON KIM (Department of Biological Sciences, Institute of Systems Biology, Education/Research Group of Longevity and Marine Biotechnology for innovative Talent, Pusan National University) ;
  • JONG-HYEOB KIM (Korea Ocean Research) ;
  • HYEGWANG KIM (Department of Biological Sciences, Pusan National University) ;
  • JIN WOO KU (Department of Biological Sciences, Pusan National University) ;
  • KI YOUNG KIM (Department of Biological Sciences, Pusan National University) ;
  • KUN-SEOP LEE (Department of Biological Sciences, Institute of Systems Biology, Education/Research Group of Longevity and Marine Biotechnology for innovative Talent, Pusan National University)
  • 김승현 (부산대학교 생명과학과, 생명시스템연구소, 장수.해양바이오 혁신인력 양성 교육연구단 ) ;
  • 김종협 ((주)코리아오션리서치 ) ;
  • 김혜광 (부산대학교 생명과학과 ) ;
  • 구진우 (부산대학교 생명과학과 ) ;
  • 김기영 (부산대학교 생명과학과 ) ;
  • 이근섭 (부산대학교 생명과학과, 생명시스템연구소, 장수.해양바이오 혁신인력 양성 교육연구단 )
  • Received : 2023.10.12
  • Accepted : 2024.01.15
  • Published : 2024.02.29

Abstract

The carbon balance serves as a valuable indicator of a plant's physiological status under diverse environmental conditions. We investigated the photosynthetic and respiratory responses of the Asian surfgrass Phyllospadix iwatensis along the northeast coast of the Korean peninsula in response to changing water temperature (ranging from 5℃ to 30℃) to estimate the seasonal whole-plant carbon balance through a series of incubation experiments. The maximum gross photosynthetic rate (Pmax) showed a significant difference among the temperature treatments, while there was no significant difference in photosynthetic efficiency (α). The maximum gross photosynthetic rate of P. iwatensis reached its peaks at 20℃ treatment (101.65 μmol O2 g-1 DW h-1) but decreased rapidly at 30℃. The saturation irradiance (Ik), compensation irradiance (Ic), and respiration rate (R) of P. iwatensis exhibited significant differences among the temperature treatments. The saturation irradiance increased up to 20-25℃ (121.59-124.50 μmol photons m-2 s-1) and sharply decreased at 30℃. The compensation irradiance and respiration rate increased steadily with rising water temperature. The ratio of Pmax to R (Pmax:R ratio) was the highest at 5℃ but dramatically decreased at 30℃. The whole-plant carbon balance, calculated based on photosynthetic parameters, respiration rates, and biomass, exhibited distinct seasonal variation, increasing during winter and spring and decreasing during summer and fall, which is consistent with the highest in situ growth in spring and severely limited growth at the highest water temperature conditions. Phyllospadix iwatensis displayed a negative carbon balance during late summer, fall, and winter, but demonstrated a positive carbon balance during spring and early summer. Our findings suggest that the rising seawater temperatures associated with climate change may lead to significant alterations in the seagrass ecosystem functioning along the rocky shores of the Korean east coast.

탄소수지는 다양한 환경조건에서 식물의 생리적 상태를 평가할 수 있는 중요한 지표 중 하나이다. 우리 동해 연안에 분포하는 새우말의 수온 변화(5-30℃)에 따른 광합성률과 호흡률을 측정하여, 전체 식물 탄소수지의 계절적 변동을 추정하였다. 수온 처리에 따라 최대총광합성률은 유의한 차이를 보였지만, 광합성 효율은 유의한 차이를 보이지 않았다. 새우말의 최대총광합성률은 수온이 상승함에 따라 증가하여 20℃에서 최대값(101.65 μmol O2 g-1 DW h-1)을 보인 후 30℃에서 급격히 감소하였다. 수온 변화에 따른 새우말의 포화광도, 보상광도와 호흡률은 모두 유의한 차이를 보였다. 새우말의 포화광도는 20-25℃까지(121.59-124.50 μmol photons m-2 s-1) 증가하다가 30℃에서 급격히 감소하였다. 보상광도와 호흡률은 수온이 증가할수록 점차 증가하였다. 최대총광합성률과 호흡률의 비율은 5℃에서 가장 높았고, 30℃에서 급격히 감소하였다. 광합성 매개변수, 호흡률 및 생체량을 통해서 추정된 새우말 전체 식물의 탄소수지는 겨울과 봄에 증가하고, 여름과 가을에 감소하는 뚜렷한 계절적 경향을 보였으며, 봄에 생장이 가장 활발하고, 수온이 가장 높은 시기에 급격히 감소하는 새우말의 생장 패턴과 일치하였다. 새우말은 늦여름부터 겨울까지 음의 탄소수지를, 봄에서 초여름까지 양의 탄소수지를 보였다. 기후 변화에 의한 지속적인 수온 상승은 우리 동해 연안 암반생태계에 분포하는 잘피생육지의 구조와 기능에 영향을 미칠 것으로 판단된다.

Keywords

Acknowledgement

본 연구는 부산대학교 기본연구지원사업(2년)에 의하여 수행되었습니다.

References

  1. Alcoverro, T., M. Manzanera and J. Romero, 2001. Annual metabolic carbon balance of the seagrass Posidonia oceanica: the importance of carbohydrate reserves. Mar. Ecol. Prog. Ser., 211: 105-116. https://doi.org/10.3354/meps211105
  2. Arias-Ortiz, A., O. Serrano, P. Masque, P.S. Lavery, U. Mueller, G.A. Kendrick, M. Rozaimi, A. Esteban, J.W. Fourqurean, N. Marba, M.A. Mateo, K. Murray, M.J. Rule and C.M. Duarte, 2018. A marine heatwave drives massive losses from the world's largest seagrass carbon stocks. Nature Climate Change, 8: 338-344. https://doi.org/10.1038/s41558-018-0096-y
  3. Beca-Carretero, P., B. Olesen, N. Marba and D. Krause-Jensen, 2018. Response to experimental warming in northern eelgrass populations: comparison across a range of temperature adaptations. Mar. Ecol. Prog. Ser., 589: 59-72. https://doi.org/10.3354/meps12439
  4. Belkin, I.M., 2009. Rapid warming of large marine ecosystems. Prog. Oceanogr., 81(1-4): 207-213. https://doi.org/10.1016/j.pocean.2009.04.011
  5. Birchenough, S.N.R., H. Reiss, S. Degraer, N. Mieszkowska, A. Borja, L. Buhl-Mortensen, U. Braeckman, J. Craeymeersch, I. De Mesel, F. Kerckhof, I. Kroncke, S. Parra, M. Rabaut, A. Schroder, C. Van Colen, G. Van Hoey, M. Vincx and K. Watjen, 2015. Climate change and marine benthos: a review of existing research and future directions in the North Atlantic. Wiley Interdisciplinary Reviews-Climate Change, 6(2): 203-223. https://doi.org/10.1002/wcc.330
  6. Collier, C.J., Y.X. Ow, L. Langlois, S. Uthicke, C.L. Johansson, K.R. O'Brien, V. Hrebien and M.P. Adams, 2017. Optimum temperatures for net primary productivity of three tropical seagrass species. Front. Plant Sci., 8: 1446.
  7. Doney, S.C., M. Ruckelshaus, J.E. Duffy, J.P. Barry, F. Chan, C.A. English, H.M. Galindo, J.M. Grebmeier, A.B. Hollowed, N. Knowlton, J. Polovina, N.N. Rabalais, W.J. Sydeman and L.D. Talley, 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science, 4: 11-37. https://doi.org/10.1146/annurev-marine-041911-111611
  8. Dunton, K.H. and D.A. Tomasko, 1994. In situ photosynthesis in the seagrass Halodule wrightii in a hypersaline subtropical lagoon Mar. Ecol. Prog. Ser., 107(3): 281-293. https://doi.org/10.3354/meps107281
  9. George, R., M. Gullstrom, M.M. Mangora, M.S.P. Mtolera and M. Bjork, 2018. High midday temperature stress has stronger effects on biomass than on photosynthesis: A mesocosm experiment on four tropical seagrass species. Ecol. Evol., 8(9): 4508-4517. https://doi.org/10.1002/ece3.3952
  10. Georgiou, D., A. Alexandre, J. Luis and R. Santos, 2016. Temperature is not a limiting factor for the expansion of Halophila stipulacea throughout the Mediterranean Sea. Mar. Ecol. Prog. Ser., 544: 159-167. https://doi.org/10.3354/meps11582
  11. Hammer, K.J., J. Borum, H. Hasler-Sheetal, E.C. Shields, K. Sand-Jensen and K.A. Moore, 2018. High temperatures cause reduced growth, plant death and metabolic changes in eelgrass Zostera marina. Mar. Ecol. Prog. Ser., 604: 121-132. https://doi.org/10.3354/meps12740
  12. Hansen, A.B., A.S. Pedersen, M. Kuhl and K.E. Brodersen, 2022. Temperature effects on leaf and epiphyte photosynthesis, bicarbonate use and diel O2 budgets of the seagrass Zostera marina L. Front. Mar. Sci., 9: 822485.
  13. Hyun, J.-H., K.-S. Choi, K.-S. Lee, S.H. Lee, Y.K. Kim and C.-K. Kang, 2020. Climate Change and anthropogenic impact around the Korean coastal ecosystems: Korean Long-term Marine Ecological Research (K-LTMER). Estuar. Coast., 43: 441-448. https://doi.org/10.1007/s12237-020-00711-6
  14. Intergovernmental Panel on Climate Change (IPCC), 2021. Summary for Policymakers. In: Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, edited by Masson-Delmotte, V., P. Zhai, A. Pirani, S.L. Connors, C. Pean, S. Berger, N. Caud, Y. Chen, L. Goldfarb, M.I. Gomis, M. Huang, K. Leitzell, E. Lonnoy, J.B.R. Matthews, T.K. Maycock, T. Waterfield, O. Yelekci, R. Yu and B. Zhou. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, pp. 3-32.
  15. Jassby, A.D. and T. Platt, 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr., 21: 540-547. https://doi.org/10.4319/lo.1976.21.4.0540
  16. Jorda, G., N. Marba and C.M. Duarte, 2012. Mediterranean seagrass vulnerable to regional climate warming. Nature Climate Change, 2: 821-824. https://doi.org/10.1038/nclimate1533
  17. Kim, H., J.-H. Kim, S.H. Kim, Z. Suonan and K.-S. Lee, 2022. Photosynthetis and respiratory responses of the surfgrass, Phyllospadix japonicus, to the rising water temperature. Korean J. Environ. Biol., 40(3): 352-362. https://doi.org/10.11626/KJEB.2022.40.3.352
  18. Kim, J.-H., J.H. Kim, G.Y. Kim and J.-I. Park, 2018. Growth dynamics of the surfgrass, Phyllospadix iwatensis on the eastern coast of Korea. The Sea, 23(4): 192-203. https://doi.org/10.7850/JKSO.2018.23.4.192
  19. Kim, S.H., H. Kim, Z. Suonan, F. Zhang and K.-S. Lee, 2023. Photosynthesis and whole-plant carbon balances of warm affinity Halophila nipponica and cold affinity Zostera marina in relation to water temperature rise: implication for future geographic distribution. Front. Mar. Sci., 10: 1203809.
  20. Kim, S.H., J.-H. Kim, S.R. Park and K.-S. Lee, 2014. Annual and perennial life history strategies of Zostera marina populations under different light regimes. Mar. Ecol. Prog. Ser., 509: 1-13. https://doi.org/10.3354/meps10899
  21. Kim, S.H., Y.K. Kim, S.R. Park, W.-T. Li and K.-S. Lee, 2012. Growth dynamics of the seagrass Halophila nipponica, recently discovered in temperate coastal waters of the Korean peninsula. Mar. Biol., 159: 255-267. https://doi.org/10.1007/s00227-011-1804-6
  22. Kim, T.H., S.R. Rark, Y.K. Kim, J.-H. Kim, S.H. Kim, J.H. Kim, I.K. Chung and K.-S. Lee, 2008. Growth dynamics and carbon incorporation of the seagrass, Zostera marina L. in Jindong Bay and Gamak Bay on the southern coast of Korea. Algae, 23(3): 241-250. https://doi.org/10.4490/ALGAE.2008.23.3.241
  23. Lee, K.-S., S.H. Kim and Y.K. Kim, 2018. Current status of seagrass habitat in Korea. In: The Wetland Book: II: Distribution, Description, and Conservation, edited by Finlayson, C.M., G.R. Milton, R.C. Prentice and N.C. Davidson. Springer Netherlands, Dordrecht, pp. 1589-1596.
  24. Lee, K.-S., S.R. Park and Y.K. Kim, 2005. Production dynamics of the eelgrass, Zostera marina in two bay systems on the south coast of the Korean peninsula. Mar. Biol., 147: 1091-1108. https://doi.org/10.1007/s00227-005-0011-8
  25. Lee, K.-S., S.R. Park and Y.K. Kim, 2007. Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: A review. J. Exp. Mar. Biol. Ecol., 350(1-2): 144-175. https://doi.org/10.1016/j.jembe.2007.06.016
  26. Marsh Jr, J.A., W.C. Dennison and R.S. Alberte, 1986. Effects of temperature on photosynthesis and respiration in eelgrass (Zostera marina L.). J. Exp. Mar. Biol. Ecol., 101(3): 257-267. https://doi.org/10.1016/0022-0981(86)90267-4
  27. McKenzie, L.J., L.M. Nordlund, B.L. Jones, L.C. Cullen-Unsworth, C. Roelfsema and R.K.F. Unsworth, 2020. The global distribution of seagrass meadows. Environ. Res. Lett., 15: 074041.
  28. Moreno-Marin, F., F.G. Brun and M.F. Pedersen, 2018. Additive response to multiple environmental stressors in the seagrass Zostera marina L. Limnol. Oceanogr., 63(4): 1528-1544. https://doi.org/10.1002/lno.10789
  29. Nguyen, H.M., P.J. Ralph, L. Marin-Guirao, M. Pernice and G. Procaccini, 2021. Seagrasses in an era of ocean warming: a review. Biological Reviews, 96(5): 2009-2030. https://doi.org/10.1111/brv.12736
  30. Oczkowski, A., R. McKinney, S. Ayvazian, A. Hanson, C. Wigand and E. Markham, 2015. Preliminary evidence for the amplification of global warming in shallow, intertidal estuarine waters. Plos one, 10: e0141529.
  31. Olive, I., J.J. Vergara and J.L. Perez-Llorens, 2013. Photosynthetic and morphological photoacclimation of the seagrass Cymodocea nodosa to season, depth and leaf position. Mar. Biol., 160: 285-297. https://doi.org/10.1007/s00227-012-2087-2
  32. Park, J.-I. and K.-S. Lee, 2009. Peculiar growth dynamics of the surfgrass Phyllospadix japonicus on the southeastern coast of Korea. Mar. Biol., 156: 2221-2233. https://doi.org/10.1007/s00227-009-1250-x
  33. Park, J.-I., J.H. Kim, J.-H. Kim and M.S. Kim, 2019. Growth dynamics of the surfgrass, Phyllospadix japonicus on the southeastern coast of Korea. The Sea, 24(4): 548-561. https://doi.org/10.7850/JKSO.2019.24.4.548
  34. Poloczanska, E.S., C.J. Brown, W.J. Sydeman, W. Kiessling, D.S. Schoeman, P.J. Moore, K. Brander, J.F. Bruno, L.B. Buckley, M.T. Burrows, C.M. Duarte, B.S. Halpern, J. Holding, C.V. Kappel, M.I. O'Connor, J.M. Pandolfi, C. Parmesan, F. Schwing, S.A. Thompson and A.J. Richardson, 2013. Global imprint of climate change on marine life. Nat. Clim. Chang., 3: 919-925. https://doi.org/10.1038/nclimate1958
  35. Qin, L.-Z., S.H. Kim, H.-J. Song, H.G. Kim, Z. Suonan, O. Kwon, Y.K. Kim, S.R. Park, J.-I. Park and K.-S. Lee, 2020. Long-term variability in the flowering phenology and intensity of the temperate seagrass Zostera marina in response to regional sea warming. Ecol. Indic., 119: 106821.
  36. Rasmusson, L.M., M. Gullstrom, P.C.B. Gunnarsson, R. George and M. Bjork, 2019. Estimation of a whole plant Q10 to assess seagrass productivity during temperature shifts. Sci. Rep., 9: 12667.
  37. Rasmusson, L.M., P. Buapet, R. George, M. Gullstrom, P.C.B. Gunnarsson and M. Bjork, 2020. Effects of temperature and hypoxia on respiration, photorespiration, and photosynthesis of seagrass leaves from contrasting temperature regimes. ICES J. Mar. Sci., 77(6): 2056-2065. https://doi.org/10.1093/icesjms/fsaa093
  38. Said, N.E., K. McMahon and P.S. Lavery, 2021. Accounting for the influence of temperature and location when predicting seagrass (Halophila ovalis) photosynthetic performance. Estuar. Coast. Shelf Sci., 257: 107414.
  39. Staehr, P.A. and J. Borum, 2011. Seasonal acclimation in metabolism reduces light requirements of eelgrass (Zostera marina). J. Exp. Mar. Biol. Ecol., 407(2): 139-146. https://doi.org/10.1016/j.jembe.2011.05.031
  40. Strydom, S., R. McCallum, A. Lafratta, C.L. Webster, C.M. O'Dea, N.E. Said, N. Dunham, K. Inostroza, C. Salinas, S. Billinghurst, C.M. Phelps, C. Campbell, C. Gorham, R. Bernasconi, A.M. Frouws, A. Werner, F. Vitelli, V. Puigcorbe, A. D'Cruz, K.M. McMahon, J. Robinson, M.J. Huggett, S. McNamara, G.A. Hyndes and O. Serrano, 2023. Global dataset on seagrass meadow structure, biomass and production. Earth Syst. Sci. Data, 15(1): 511-519. https://doi.org/10.5194/essd-15-511-2023
  41. Tanaka, Y. and M. Nakaoka, 2007. Interspecific variation in photosynthesis and respiration balance of three seagrasses in relation to light availability. Mar. Ecol. Prog. Ser., 350: 63-70. https://doi.org/10.3354/meps07103
  42. Torquemada, Y.F., M.J. Durako and J.L.S. Lizaso, 2005. Effects of salinity and possible interactions with temperature and pH on growth and photosynthesis of Halophila johnsonii Eiseman. Mar. Biol., 148: 251-260. https://doi.org/10.1007/s00227-005-0075-5
  43. Vivanco-Bercovich, M., M.D. Belando-Torrentes, M.F. Figueroa-Burgos, A. Ferreira-Arrieta, V. Macias-Carranza, J.A. Garcia-Pantoja, A. Cabello-Pasini, G. Samperio-Ramos, R. Cruz-Lopez and J.M. Sandoval-Gil, 2022. Combined effects of marine heatwaves and reduced light on the physiology and growth of the surfgrass Phyllospadix torreyi from Baja California, Mexico. Aquat. Bot., 178: 103488.
  44. Wernberg, T., S. Bennett, R.C. Babcock, T. de Bettignies, K. Cure, M. Depczynski, F. Dufois, J. Fromont, C.J. Fulton, R.K. Hovey, E.S. Harvey, T.H. Holmes, G.A. Kendrick, B. Radford, J. Santana-Garcon, B.J. Saunders, D.A. Smale, M.S. Thomsen, C.A. Tuckett, F. Tuya, M.A. Vanderklift and S. Wilson, 2016. Climate-driven regime shift of a temperate marine ecosystem. Science, 353: 169-172. https://doi.org/10.1126/science.aad8745