Abstract
Based on three ornithogenic sediment profiles and seabird subfossils therein from the **sha Islands, South China Sea, the relative population size of seabirds over the past 1000 years was reconstructed using reflectance spectrum. Here we present an apparent increase and subsequent decline of seabirds on these islands in the South China Sea. Seabird populations peaked during the Little Ice Age (LIA, 1400–1850 AD), implying that the cool climate during the LIA appears to have been more favorable to seabirds on the **sha Islands in the South China Sea. Climate change partly explains the recent decrease in seabird populations over the past 150 years, but the significant decline and almost complete disappearance thereof on most of the **sha Islands is probably attributable to human disturbance. Our study reveals the increasing impact of anthropogenic activities on seabird population in recent times.
Similar content being viewed by others
Introduction
Seabirds forage at sea and breed on land, delivering significant quantities of marine-derived nutrients and contaminants to terrestrial ecosystems1. Activities of seabirds such as Little Auks and Northern Fulmars in the Arctic resulted in the accumulation of guano, and significantly impacted on the properties of soil and lacustrine sediments, as well as plant communities2,3,4. Similar processes have also been observed in coastal areas and islands worldwide5. Moreover, seabirds are quite sensitive to environmental changes and thus are an ideal indicator for variability in climatic systems6,7,8.
The **s in the **sha Archipelago, and thus may be used to estimate changes in seabird populations11. The down-core distributions of the elements P, Cu, Cd, Zn, As and Se were determined for the profile ZS2. The concentrations of As, Se, Cu, Cd and Zn in the sediments were determined by inductively coupled plasma-mass spectrometry (ICP-MS) after digestion with multi-acids at ALS Chemex (Guangzhou) Co. Ltd., while the P level was determined by inductively coupled plasma-atomic emission spectrometry (ICP-AES) at the Institute of Polar Environment, University of Science and Technology of China.
Dating
The chronology of each profile was established by both 210Pb dating and radiocarbon analysis. For 210Pb analysis, the upper sediments of all the cores were dated using 210Pb activity measured by HPGE gamma spectrometry (manufactured by Ortec, USA), and the lower parts of the ZS2, BD1 and CH cores were dated using AMS 14C ages obtained from seabird bones. Specifics of the 210Pb test were reported in our earlier study22. Radiocarbon analyses of several bird bone samples in each profile were performed at Beta Analytic Inc., or the University of Georgia. The AMS 14C dates were then calibrated into Calendar Year Before Present (Cal BP), where the “present” is defined as 1950 AD. In the current study, we established the age models of the three cores using Bayesian analysis.
Additional Information
How to cite this article: Xu, L. et al. Decline of recent seabirds inferred from a composite 1000-year record of population dynamics. Sci. Rep. 6, 35191; doi: 10.1038/srep35191 (2016).
References
Anderson, W. B. & Polis, G. A. Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands. Oecologia 118, 324–332 (1999).
Blais, J. M. et al. Arctic seabirds transport marine-derived contaminants. Science 309, 445 (2005).
Stempniewicz, L., Błachowiak-Samołyk, K. & Węsławski, J. M. Impact of climate change on zooplankton communities, seabird populations and arctic terrestrial ecosystem-a scenario. Deep-Sea Res. Part II 54, 2934–2945 (2007).
Michelutti, N. et al. Trophic position influences the efficacy of seabirds as metal biovectors. Proc. Natl. Acad. Sci. 107, 10543–10548 (2010).
Ellis, J. C. Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecol. 181, 227–241 (2005).
Devney, C. A., Short, M. & Congdon, B. C. Sensitivity of tropical seabirds to El-Niño precursors. Ecology 90, 1175–1183 (2009).
Sun, L. G. et al. Vertebrate records in polar sediments: biological responses to past climate change and human activities. Earth-Sci. Rev. 126, 147–155 (2013).
Nie, Y., Sun, L., Liu X. & Emslie, S. D. From warm to cold: migration of Adélie penguins within Cape Bird, Ross Island. Sci. Rep. 5, 11530, doi: 10.1038/srep11530 (2015).
Lu, Y. C., Yang, X. C. & Jia, R. F., 1979. Quaternary biological sediments in the **sha Archipelago, China and a discussion on the age of island-formation. Geochimica 2, 93–102 (in Chinese with English abstract) (2002).
Hainan Ocean Administration. The professional proceedings of the integrated investigation research on sea islands resource of Hainan province. (China Ocean Press, 1999) (in Chinese with English abstract).
Xu, L. Q. et al. Geochemical evidence for the development of coral island ecosystem in the **sha Archipelago of South China Sea from three ornithogenic sediment profiles. Chem. Geol. 286, 135–145 (2011).
Braje, T. J. & Erlandson, J. M. Human acceleration of animal and plant extinctions: A late Pleistocene, Holocene, and Anthropocene continuum. Anthropocene 4, 14–23 (2013).
Seddon, A. W. et al. Looking forward through the past: identification of 50 priority research questions in palaeoecology. J. Ecol. 102, 256–267 (2014).
Exploration Group of **sha Islands of Institute of Soil Science of Chinese Academy of Sciences (CAS). Soil and guano phosphorus mine in **-Sha. (Science Press, 1977). (in Chinese).
Cao, L., Pan, Y. L. & Liu, N. F. Waterbirds of the **sha Archipelago, South China Sea. Waterbirds 30, 296–300 (2007).
Cao, L. Population ecology of the red-footed booby on the **sha Archipelago. PhD dissertation. Lanzhou University (2005).
Tang, S. The biodiversity research on a tropical coral archipelago in the South China Sea. Master dissertation. University of Science and Technology of China (2009).
Zhao, H. T. et al. Nature and development of Yongxing island and Shi island of **sha islands. Mar. Sci. Bull. 12, 44–56, (in Chinese with English abstract) (1994).
Blaauw, M. & Christen, J. A. Flexible paleoclimate age-depth models using an autoregressive gamma process. Bayesian Anal. 6, 457–474 (2011).
Appleby, P. G. Three decades of dating recent sediments by fallout radionuclides: a review. Holocene 18, 83–93 (2008).
Reimer, P. J. et al. IntCal13 and Marine13 radiocarbon age calibration curves 0-50,000 yr cal BP. Radiocarbon 55, 1869–1887 (2013).
Xu, L. Q. et al. Distribution of radionuclides in the guano sediments of **sha Islands, South China Sea and its implication. J. Environ. Radioact. 101, 362–368 (2010).
Liu, X. D., Sun, J., Sun, L. G., Liu, W. Q. & Wang, Y. H. Reflectance spectroscopy: a new approach for reconstructing penguin population size from Antarctic ornithogenic sediments. J. Paleoliminol. 45, 213–222 (2011).
Xu, L. Q., Liu, X. D., Sun, L. G. & Liu, W. Q. Rapid identification of source material levels in coral sand ornithogenic sediments by reflectance spectroscopy. Ecol. Indicat. 23, 517–523 (2012).
Sun, L. G., **e, Z. Q. & Zhao, J. L. A 3,000-year record of penguin populations. Nature 407, 858 (2000).
Wu, L. B. et al. Dietary change in seabirds on Guang** Island, South China Sea, over the past 1200 years inferred from stable isotope analysis. Holocene, doi: 10.1177/0959683616660163 (2016).
Cao, L., Pang, Y. L. & Liu, N. F. Status of the red-footed booby on the **sha Archipelago, South China Sea. Waterbirds 28, 411–419 (2005).
Moberg, A., Sonechldn, D. M., Holmgren, K., Datsenko, N. M. & Karlen, W. Highly variable Northern Hemisphere temperatures reconstructed from low- and high-resolution proxy data. Nature 433, 613–617 (2005).
Yang, B., Braeuning, A. & Shi, Y. A. General characteristics of temperature variation in China during the last two millennia. Geophys. Res. Lett. 29, 1324, doi: 10.1029/2001GL014485 (2002).
Huang, T., Sun, L. G., Wang, Y. H., Liu, X. D. & Zhu, R. B. Penguin population dynamics for the past 8500 years at Gardener Island, Vestfold Hills. Antarct. Sci. 21, 571–578 (2009).
Emslie, S. D., Coats, L. & Licht, K. A 45,000 yr record of Adélie penguins and climate change in the Ross Sea, Antarctica. Geology 35, 61–64 (2007).
Clucas, G. V. et al. A reversal of fortunes: climate change ‘winners’ and ‘losers’ in Antarctic Peninsula penguins. Sci. Rep. 4, 5024, doi: 10.1038/srep05024 (2014).
Younger, J. L. et al. Too much of a good thing: Sea ice extent may have forced emperor penguins into refugia during the last glacial maximum. Glob. Change Boil. 21, 2215–2226 (2015).
Ropert-Coudert, Y. et al. A complete breeding failure in an Adélie penguin colony correlates with unusual and extreme environmental events. Ecography 38, 111–113 (2015).
Liu, K. K. et al. Monsoon-forced chlorophyll distribution and primary production in the South China Sea: observations and a numerical study. Dddp-Sea Res. Pt I 49, 1387–1412 (2002).
Shiozaki, T. & Chen, Y. L. Different mechanisms controlling interannual phytoplankton variation in the South China Sea and the western North Pacific subtropical gyre: A satellite study. Adv. Space Res. 52, 668–676 (2013).
Wei, G. J. et al. Coralline Sr/Ca and Mg/Ca thermometer for the northern South China Sea: calibration and primary application on high resolution SST reconstructing. Quaternary Sci. 24, 325–331 (2004).
Song, S. H. et al. Variation of the winter monsoon in South China Sea over the past 183 years: Evidence from oxygen isotopes in coral. Global Planet. Change 98, 131–138 (2012).
Zhao, H. & Tang, D. L. Effect of 1998 El Niño on the distribution of phytoplankton in the South China Sea. J. Geophy. Res. 112, doi: 10.1029/2006JC003536 (2007).
Meeker, L. D. & Mayewski, P. A. A 1400-year high-resolution record of atmospheric circulation over the North Atlantic and Asia. Holocene 12, 257–266 (2002).
Zhang, P. Z. et al. A test of climate, sun and culture relationships from an 1810-year Chinese cave record. Science 322, 940–942 (2008).
Yan, H. et al. South China Sea hydrological changes and Pacific Walker Circulation variations over the last millennium. Nat. Commun. 2, 293, doi: 10.1038/ncomms1297 (2011).
Yan, H. et al. A record of the Southern Oscillation Index for the past 2,000 years from precipitation proxies. Nat. Geosci. 4, 611–614 (2011).
Mann, M. E., Cane, M. A., Zebiak, S. E. & Clement, A. Volcanic and solar forcing of the tropical pacific over the past 1000 years. J. Climate 18, 447–456 (2005).
Zhao, H. T. History of expeditions to **sha Islands. Geographical Research 15, 55–65 (in Chinese with English abstract) (1996).
Sun, Y. et al. Strontium contents of a Porites coral from **sha Island, South China Sea: A proxy for sea-surface temperature of the 20th century. Paleoceanography 19, PA2004, doi: 10.1029/2003PA000959 (2004).
Peng, Z. C. et al. Coral δ18O records as an indicator of winter monsoon intensity in the South China Sea. Quaternary Res. 59, 285–292 (2003).
Liu, Y. et al. The decline of winter monsoon velocity in the South China Sea through 20th centrry: evidence from the Sr/Ca records in corals. Global Planet. Change 63, 79–85 (2008).
Chiu, H. & Park, C. H. Legal status of the Paracel and Spratly Islands. Ocean Dev. Int. Law 3, 1–28 (1975).
Wang, Y., Ma, Y. J., Yang, Z. Z., Zheng, J. Q. & Yu, T. F. Identification of rodents and blood-sucking insects in **sha Islands of China and the first report of Anopheles mosquitoes and midges. Acad. J. Second Mil. Med. Univ. 35, 581–585 (in Chinese with English abstract) (2014).
Yu, K. F. Coral reefs in the South China Sea: Their response to and records on past environmental changes. Sci. China Ser. D-Earth Sci. 55, 1217–1229 (2012).
Wang, D. R., Wu, Z. J., Li, Y. C., Chen, J. R. & Chen, M. Analysis on variation trend of coral reef in **sha. Acta Ecol. Sin. 31, 254–258 (2011).
Myers, R. A. & Worm, B. Rapid worldwide depletion of predatory fish communities. Nature 423, 280–283 (2003).
Stobutzki, I. C., Silvestre, G. T. & Garces, L. R. Key issues in coastal fisheries in South and Southeast Asia outcomes of a regional initiative. Fish. Res. 78, 109–118 (2006).
Christensen, V., Garces, L. R., Silvestre, G. T. & Pauly, D. Fisheries impact on the South China Sea Large Marine Ecosystem: a preliminary analysis using spatially explicit methodology. Assessment, Management and Future Directions for Coastal Fisheries in Asian Countries [ Silvestre, G. T. et al. (eds.)] 51–62 (World Fish Center Conference Proceedings 67, 2003).
**e, Z. Q. et al. Preliminary geochemical evidence of groundwater contamination in coral islands of **-Sha, South China Sea. Appl. Geochem. 20, 1848–1856 (2005).
Liu, X. D. et al. Historical change of mercury pollution in remote Yongle archipelago, South China Sea. Chemosphere 87, 549–556 (2012).
Xu, L. Q. et al. A 700-year record of mercury in avian eggshells of Guang** Island, South China Sea. Environ. Pollut. 159, 889–896 (2011).
Rawlence, N. J. et al. Geographically contrasting biodiversity reductions in a widespread New Zealand seabird. Mol. Ecol. 24, 4605–4616 (2015).
Acknowledgements
This work was funded by the National Natural Science Foundation of China (Grant Nos 41402148, 41376124) and China Postdoctoral Science Foundation (Grant No. 2014M550338). All members of field study team including the Chinese People’s Liberation Army are acknowledged for their help in sample collection. We are grateful to **sha Deep Sea Marine Environment Observation and Research Station, South China Sea Institute, Chinese Academy of Sciences for field study support.
Author information
Authors and Affiliations
Contributions
L.X., X.L. and L.S designed the study and prepared the manuscript. L.X., X.L., L.W. and L.C. collected the samples. L.X. and J.Z. performed the experiments. All author contributed to discussion of the results.
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Electronic supplementary material
Rights and permissions
This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
About this article
Cite this article
Xu, L., Liu, X., Wu, L. et al. Decline of recent seabirds inferred from a composite 1000-year record of population dynamics. Sci Rep 6, 35191 (2016). https://doi.org/10.1038/srep35191
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/srep35191
- Springer Nature Limited