Abstract
Quantitative identification of long-term changes in the abundance of Japanese anchovy (Engraulis japonicus) in the Yellow Sea is particularly important for understanding evolutionary processes of the Yellow Sea ecosystem. Unfortunately, the driving mechanisms of climate variability on the anchovy are still unclear due to the lack of long-term observational data. In this study, we used the fish scale deposition rate in the central Yellow Sea to reconstruct the time series of the anchovy stock over the past 400 a. On this basis, we further explored the impacts of the Pacific Decadal Oscillation (PDO) on the anchovy. Our results show that the anchovy stock is positively correlated with the PDO on a decadal time scale. In addition, anchovy abundance was relatively high during 1620–1860 AD (the Little Ice Age, LIA), though in a state of constant fluctuation; anchovy abundance maintained at a relatively low level after ∼1860 AD. In particular, followed by overfishing since the 1980s, the anchovy stock has declined sharply. Based on these findings, we infer that fluctuations of the anchovy stock may be regulated by basin-scale “atmosphere-ocean” interactions. Nevertheless, the role of overfishing should not be ignored.
Similar content being viewed by others
References
Alheit J, Niquen M. 2004. Regime shifts in the Humboldt Current ecosystem. Progress in Oceanography, 60(2–4): 201–222, doi: https://doi.org/10.1016/j.pocean.2004.02.006
Alheit J, Pohlmann T, Casini M, et al. 2012. Climate variability drives anchovies and sardines into the North and Baltic Seas. Progress in Oceanography, 96(1): 128–139, doi: https://doi.org/10.1016/j.pocean.2011.11.015
Baumgartner T R, Soutar A, Ferreira-Bartrina V. 1992. Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara Basin, California. CalCOFI Reports, 33: 24–40
Behrenfeld M J, O’Malley R T, Siegel D A, et al. 2006. Climate-driven trends in contemporary ocean productivity. Nature, 444(7120): 752–755, doi: https://doi.org/10.1038/nature05317
Britten G L, Dowd M, Worm B. 2016. Changing recruitment capacity in global fish stocks. Proceedings of the National Academy of Sciences of the United States of America, 113(1): 134–139, doi: https://doi.org/10.1073/pnas.1504709112
Capuzzo E, Lynam C P, Barry J, et al. 2018. A decline in primary production in the North Sea over 25 years, associated with reductions in zooplankton abundance and fish stock recruitment. Global Change Biology, 24(1): e352–e364, doi: https://doi.org/10.1111/gcb.13916
Chavez F P, Ryan J, Lluch-Cota S E, et al. 2003. From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science, 299(5604): 217–221, doi: https://doi.org/10.1126/science.1075880
Checkley D M, Asch R G, Rykaczewski R R. 2017. Climate, anchovy, and sardine. Annual Review of Marine Science, 9: 469–493, doi: https://doi.org/10.1146/annurev-marine-122414-033819
Cury P, Shannon L. 2004. Regime shifts in upwelling ecosystems: observed changes and possible mechanisms in the northern and southern Benguela. Progress in Oceanography, 60(2–4): 223–243, doi: https://doi.org/10.1016/j.pocean.2004.02.007
Deyle E R, Fogarty M, Hsieh C H, et al. 2013. Predicting climate effects on Pacific sardine. Proceedings of the National Academy of Sciences of the United States of America, 110(16): 6430–6435, doi: https://doi.org/10.1073/pnas.1215506110
Doney S C, Ruckelshaus M, Duffy J E, et al. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science, 4: 11–37, doi: https://doi.org/10.1146/annurev-marine-041911-111611
Frank K T, Petrie B, Choi J S, et al. 2005. Trophic cascades in a formerly cod-dominated ecosystem. Science, 308(5728): 1621–1623, doi: https://doi.org/10.1126/science.1113075
Greene C H, Pershing A J. 2007. Climate drives sea change. Science, 315(5815): 1084–1085, doi: https://doi.org/10.1126/science.1136495
Guiñez M, Valdés J, Sifeddine A, et al. 2014. Anchovy population and ocean-climatic fluctuations in the Humboldt Current System during the last 700 years and their implications. Palaeogeography, Palaeoclimatology, Palaeoecology, 415: 210–224
Gutiérrez D, Sifeddine A, Field D B, et al. 2009. Rapid reorganization in ocean biogeochemistry off Peru towards the end of the Little Ice Age. Biogeosciences, 6(5): 835–848, doi: https://doi.org/10.5194/bg-6-835-2009
Holmgren D. 2001. Decadal-centennial variability in marine ecosystems of the Northeast Pacific Ocean: the use of fish scales de-positions in sediments [dissertation]. Washington: University of Washington
Holmgren-Urba D, Baumgartner T R. 1993. A 250-year history of pelagic fish abundances from the anaerobic sediments of the central Gulf of California. CalCOFI Reports, 34: 60–68
Hsieh C H, Reiss C S, Hunter J R, et al. 2006. Fishing elevates variability in the abundance of exploited species. Nature, 443(7113): 859–862, doi: https://doi.org/10.1038/nature05232
Hu Bangqi, Yang Zuosheng, Zhao Meixun, et al. 2012. Grain size records reveal variability of the East Asian Winter Monsoon since the Middle Holocene in the Central Yellow Sea mud area, China. Science China: Earth Sciences, 55(10): 1656–1668, doi: https://doi.org/10.1007/s11430-012-4447-7
Huang Jiansheng, 2015. Sedimentary record of anchovy population dynamics in the Yellow Sea and its response to climate changes (in Chinese) [dissertation]. Xiamen: Xiamen University
Huang Jiansheng, Sun Yao, Jia Haibo, et al. 2014. Spatial distribution and reconstruction potential of Japanese anchovy (Engraulis japonicus) based on scale deposition records in recent anaerobic sediment of the Yellow Sea and East China Sea. Acta Oceanologica Sinica, 33(12): 138–144, doi: https://doi.org/10.1007/s13131-014-0573-8
Huang Jiansheng, Sun Yao, Jia Haibo, et al. 2016. Last 150-year variability in Japanese anchovy (Engraulis japonicus) abundance based on the anaerobic sediments of the Yellow Sea Basin in the western North Pacific. Journal of Ocean University of China, 15(1): 131–136, doi: https://doi.org/10.1007/s11802-016-2605-9
Izquierdo-Peña V, Lluch-Cota S E, Hernandez-Rivas M E, et al. 2019. Revisiting the regime problem hypothesis: 25 years later. Deep-Sea Research Part II: Topical Studies in Oceanography, 159: 4–10, doi: https://doi.org/10.1016/j.dsr2.2018.11.003
Jacox M G, Bograd S J, Hazen E L, et al. 2015. Sensitivity of the California Current nutrient supply to wind, heat, and remote ocean forcing. Geophysical Research Letters, 42(14): 5950–5957, doi: https://doi.org/10.1002/2015GL065147
Jang C J, Park J, Park T, et al. 2011. Response of the ocean mixed layer depth to global warming and its impact on primary production: a case for the North Pacific Ocean. ICES Journal of Marine Science, 68(6): 996–1007, doi: https://doi.org/10.1093/icesjms/fsr064
Jia Haibo, Sun Yao, Zhao Meixun, et al. 2008. Fish-scale-deposition information and spatial distribution in typical fishery area of the Yellow Sea and East China Sea. Journal of Fisheries of China, 32(4): 584–591
Jin Xianshi, Hamre J, Zhao Xianyong, et al. 2001. Study on the quota management of anchovy (Engraulis japonicus) in the Yellow Sea. Journal of Fishery Sciences of China, 8(3): 27–30
Jin Xianshi, Zhang Bo, Xue Ying. 2010. The response of the diets of four carnivorous fishes to variations in the Yellow Sea ecosystem. Deep-Sea Research Part II: Topical Studies in Oceanography, 57(11–12): 996–1000, doi: https://doi.org/10.1016/j.dsr2.2010.02.001
Kawasaki T. 2002. Climate change, regime shift and stock management. Fisheries Science, 68(S1): 148–153
Kim D, Park B K, Shin I C. 1998. Paleoenvironmental changes of the Yellow Sea during the Late Quaternary. Geo-Marine Letters, 18(3): 189–194, doi: https://doi.org/10.1007/s003670050067
Kuparinen A, Boit A, Valdovinos F S, et al. 2016. Fishing-induced life-history changes degrade and destabilize harvested ecosystems. Scientific Reports, 6(1): 22245, doi: https://doi.org/10.1038/srep22245
Kuwae M, Yamamoto M, Sagawa T, et al. 2017. Multidecadal, centennial, and millennial variability in sardine and anchovy abundances in the western North Pacific and climate-fish linkages during the late Holocene. Progress in Oceanography, 159: 86–98, doi: https://doi.org/10.1016/j.pocean.2017.09.011
Li Haoyu, Yang Shu, Tang Qisheng, et al. 2020. Long-term variation in the abundance of Pacific herring (Clupea pallasii) from the Yellow Sea in the western North Pacific and its relation to climate over the past 590 years. Fisheries Oceanography, 29(1): 56–65, doi: https://doi.org/10.1111/fog.12449
Lindegren M, CheckleyJr D M, Rouyer T, et al. 2013. Climate, fishing, and fluctuations of sardine and anchovy in the California Current. Proceedings of the National Academy of Sciences of the United States of America, 110(33): 13672–13677, doi: https://doi.org/10.1073/pnas.1305733110
Lindegren M, Van Deurs M, MacKenzie B R, et al. 2018. Productivity and recovery of forage fish under climate change and fishing: North Sea sandeel as a case study. Fisheries Oceanography, 27(3): 212–221, doi: https://doi.org/10.1111/fog.12246
Litzow M A, Malick M J, Bond N A, et al. 2020. Quantifying a novel climate through changes in PDO-climate and PDO-salmon relationships. Geophysical Research Letters, 47(16): e2020GL087972
Liu Yi, Zhou Xin, Huang Wen, et al. 2013. Responses of primary productivity to current and climate changes in the mud area to the Southwest of Cheju Island during the past 800 years. Journal of Ocean University of China, 12(4): 605–610, doi: https://doi.org/10.1007/s11802-013-2205-x
Ma Shuyang, Liu Yang, Li Jianchao, et al. 2019. Climate-induced long-term variations in ecosystem structure and atmosphere-ocean-ecosystem processes in the Yellow Sea and East China Sea. Progress in Oceanography, 175: 183–197, doi: https://doi.org/10.1016/j.pocean.2019.04.008
Mantua N J, Hare S R. 2002. The Pacific Decadal Oscillation. Journal of Oceanography, 58(1): 35–44, doi: https://doi.org/10.1023/A:1015820616384
Mantua N J, Hare R S, Zhang Yuan, et al. 1997. A Pacific interdecadal climate oscillation with impacts on salmon production. Bulletin of the American Meteorological Society, 78(6): 1069–1080, doi: https://doi.org/10.1175/1520-0477(1997)078<1069:APICOW7gt;2.0.CO;2
McClatchie S, Hendy I L, Thompson A R, et al. 2017. Collapse and recovery of forage fish populations prior to commercial exploitation. Geophysical Research Letters, 44(4): 1877–1885, doi: https://doi.org/10.1002/2016GL071751
Mcowen C J, Cheung W W L, Rykaczewski R R, et al. 2015. Is fisheries production within large marine ecosystems determined by bottom-up or top-down forcing?. Fish and Fisheries, 16(4): 623–632, doi: https://doi.org/10.1111/faf.12082
Möllmann C, Müller-Karulis B, Kornilovs G, et al. 2008. Effects of climate and overfishing on zooplankton dynamics and ecosystem structure: regime shifts, trophic cascade, and feedback loops in a simple ecosystem. ICES Journal of Marine Science, 65(3): 302–310, doi: https://doi.org/10.1093/icesjms/fsm197
Newman M, Alexander M A, Ault T R, et al. 2016. The Pacific Decadal Oscillation, revisited. Journal of Climate, 29(12): 4399–4427, doi: https://doi.org/10.1175/JCLI-D-15-0508.1
Oozeki Y, Ñiquen Carranza M, Takasuka A, et al. 2019. Synchronous multi-species alternations between the northern Humboldt and Kuroshio Current systems. Deep-Sea Research Part II: Topical Studies in Oceanography, 159: 11–21, doi: https://doi.org/10.1016/j.dsr2.2018.11.018
Patterson R T, Prokoph A, Kumar A, et al. 2005. Late Holocene variability in pelagic fish scales and dinoflagellate cysts along the west coast of Vancouver Island, NE Pacific Ocean. Marine Micropaleontology, 55(3–4): 183–204, doi: https://doi.org/10.1016/j.marmicro.2005.02.006
Pikitch E K, Rountos K J, Essington T E, et al. 2014. The global contribution of forage fish to marine fisheries and ecosystems. Fish and Fisheries, 15(1): 43–64, doi: https://doi.org/10.1111/faf.12004
Pinsky M L, Byler D. 2015. Fishing, fast growth and climate variability increase the risk of collapse. Proceedings of the Royal Society B:Biological Sciences, 282(1813): 20151053, doi: https://doi.org/10.1098/rspb.2015.1053
Pitois S G, Lynam C P, Jansen T, et al. 2012. Bottom-up effects of climate on fish populations: data from the Continuous Plankton Recorder. Marine Ecology Progress Series, 456: 169–186, doi: https://doi.org/10.3354/meps09710
Planque B, Fromentin J M, Cury P, et al. 2010. How does fishing alter marine populations and ecosystems sensitivity to climate?. Journal of Marine Systems, 79(3–4): 403–417, doi: https://doi.org/10.1016/j.jmarsys.2008.12.018
Qiao Shuqing, Shi Xuefa, Wang Guoqing, et al. 2017. Sediment accumulation and budget in the Bohai Sea, Yellow Sea and East China Sea. Marine Geology, 390: 270–281, doi: https://doi.org/10.1016/j.margeo.2017.06.004
Rayner N A, Brohan P, Parker D E, et al. 2006. Improved analyses of changes and uncertainties in sea surface temperature measured in situ since the mid-nineteenth century: The HadSST2 dataset. Journal of Climate, 19(3): 446–469, doi: https://doi.org/10.1175/JCLI3637.1
Roemmich D, McGowan J. 1995. Climatic warming and the decline of zooplankton in the California Current. Science, 267(5202): 1324–1326, doi: https://doi.org/10.1126/science.267.5202.1324
Rykaczewski R R, Dunne J P. 2010. Enhanced nutrient supply to the California Current Ecosystem with global warming and increased stratification in an earth system model. Geophysical Research Letters, 37(21): L21606
Salvatteci R, Field D, Baumgartner T, et al. 2012. Evaluating fish scale preservation in sediment records from the oxygen minimum zone off Peru. Paleobiology, 38(1): 52–78, doi: https://doi.org/10.1666/10045.1
Salvatteci R, Field D, Gutiérrez D, et al. 2018. Multifarious anchovy and sardine regimes in the Humboldt Current System during the last 150 years. Global Change Biology, 24(3): 1055–1068, doi: https://doi.org/10.1111/gcb.13991
Salvatteci R, Gutierrez D, Field D, et al. 2019. Fish debris in sediments from the last 25 kyr in the Humboldt Current reveal the role of productivity and oxygen on small pelagic fishes. Progress in Oceanography, 176: 102114, doi: https://doi.org/10.1016/j.pocean.2019.05.006
Shen Gongming, Heino M. 2014. An overview of marine fisheries management in China. Marine Policy, 44: 265–272, doi: https://doi.org/10.1016/j.marpol.2013.09.012
Shen Caiming, Wang W C, Gong Wei, et al. 2006. A Pacific Decadal Oscillation record since 1470 AD reconstructed from proxy data of summer rainfall over eastern China. Geophysical Research Letters, 33(3): L03702
Soutar A, Isaacs J D. 1969. History of fish populations inferred from fish scales in anaerobic sediments off California. California Committee on the Fishing Industry Reports, 13: 63–70
Stenseth N C, Mysterud A, Ottersen G, et al. 2002. Ecological effects of climate fluctuations. Science, 297(5585): 1292–1296, doi: https://doi.org/10.1126/science.1071281
Surry A M, King J R. 2015. A New Method for Calculating ALPI: The Aleutian Low Pressure Index. Nanaimo: Fisheries and Oceans Canada, 1–31
Tang Qisheng, Ying Yiping, Wu Qiang. 2016. The biomass yields and management challenges for the Yellow Sea large marine ecosystem. Environmental Development, 17(S1): 175–181
Valdés J, Ortlieb L, Gutierrez D, et al. 2008. 250 years of sardine and anchovy scale deposition record in Mejillones Bay, northern Chile. Progress in Oceanography, 79(2–4): 198–207, doi: https://doi.org/10.1016/j.pocean.2008.10.002
Ware D M, Thomson R E. 2005. Bottom-up ecosystem trophic dynamics determine fish production in the Northeast Pacific. Science, 308(5726): 1280–1284, doi: https://doi.org/10.1126/science.1109049
Worm B, Myers R A. 2003. Meta-analysis of cod-shrimp interactions reveals top-down control in oceanic food webs. Ecology, 84(1): 162–173, doi: https://doi.org/10.1890/0012-9658(2003)084[0162:MAOCSI]2.0.CO;2
Wu Zhaohua, Huang N E. 2009. Ensemble empirical mode decomposition: a noise-assisted data analysis method. Advances in Adaptive Data Analysis, 1(1): 1–41, doi: https://doi.org/10.1142/S1793536909000047
Xing Lei, Zhao Meixun, Zhang Hailong, et al. 2009. Biomarker records of phytoplankton community structure changes in the Yellow Sea over the last 200 years. Periodical of Ocean University of China, 39(2): 317–322
Yang Qian, Song Xianli, Sun Yao, et al. 2012. Application of biologic silicon in modern sedimentary section to reconstruction of phytoplankton changes in the East China Sea and the Huang-hai Sea during last 200 years. Acta Oceanologica Sinica, 31(2): 70–77, doi: https://doi.org/10.1007/s13131-012-0193-0
Yasuda I, Sugisaki H, Watanabe Y, et al. 1999. Interdecadal variations in Japanese sardine and ocean/climate. Fisheries Oceanography, 8(1): 18–24, doi: https://doi.org/10.1046/j.1365-2419.1999.00089.x
Yuan Dongliang, Hsueh Y. 2010. Dynamics of the cross-shelf circulation in the Yellow and East China Seas in winter. Deep-Sea Research Part II: Topical Studies in Oceanography, 57(19–20): 1745–1761, doi: https://doi.org/10.1016/j.dsr2.2010.04.002
Zhang Ziyin, Guo Wenli, Gong Daoyi, et al. 2013. Evaluation of the twentieth century reanalysis dataset in describing East Asian winter monsoon variability. Advances in Atmospheric Sciences, 30(6): 1645–1652, doi: https://doi.org/10.1007/s00376-012-2226-1
Zhang Zhaohui, Qu Fangyuan, Wang Shouqiang. 2019. Sustainable development of the Yellow Sea Large Marine Ecosystem. Deep-Sea Research Part II: Topical Studies in Oceanography, 163: 102–107, doi: https://doi.org/10.1016/j.dsr2.2018.08.009
Zhao Xianyong. 2006. Population dynamic characteristics and sustainable utilization of the anchovy stock in the Yellow Sea (in Chinese) [dissertation]. Qingdao: Ocean University of China
Zhou Xin, Sun Yao, Huang Wen, et al. 2015. The Pacific Decadal Oscillation and changes in anchovy populations in the Northwest Pacific. Journal of Asian Earth Sciences, 114: 504–511, doi: https://doi.org/10.1016/j.jseaes.2015.06.027
Acknowledgements
We thank Hongxia Qiu for her help in subsampling the cores. We would like to express our sincere appreciation to the two anonymous reviewers for their insightful comments that have greatly improved the quality of the manuscript. The captain and crew aboard the R/V Beidou are thanked for their excellent cooperation during sample collection.
Author information
Authors and Affiliations
Corresponding author
Additional information
Foundation item: The National Natural Science Foundation of China under contract No. 31600397.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Li, H., Tang, Q. & Sun, Y. Response of Japanese anchovy (Engraulis japonicus) to the Pacific Decadal Oscillation in the Yellow Sea over the past 400 a. Acta Oceanol. Sin. 41, 31–40 (2022). https://doi.org/10.1007/s13131-021-1914-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13131-021-1914-z