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Trace elements (Cu, Zn, and Hg) and δ13C/δ15N in seabird subfossils from three islands of the South China Sea and its implications

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Abstract

Seabird subfossils were collected on three islands of the Xisha Archipelago, South China Sea. Via elemental analysis, we identified that bird guano was a significant source for heavy metals Cu, Zn, and Hg. Cu and Zn levels in these guano samples are comparable to their levels in wildbird feces, but guano Hg was lower than previously reported. Trophic positions significantly impacted transfer efficiency of heavy metals by seabirds. Despite of a common source, trace elements, as well as stable isotopes (i.e., guano δ13C and collagen δ15N), showed island-specific characteristics. Bird subfossils on larger island had relatively greater metal concentrations and revealed higher trophic positions. Partition of element and isotope levels among the islands suggested that transfer efficacy of seabirds on different islands was different, and bird species were probably unevenly distributed among the islets. Island area is possibly a driving factor for distributions of seabird species.

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References

  • Administration, H. O. (1999). The professional proceedings of the integrated investigation research on sea islands resource of Hainan province. Beijing: China Ocean Press (in Chinese with English abstract).

    Google Scholar 

  • Anderson, O. R. J., Phillips, R. A., McDonald, R. A., Shore, R. F., McGill, R. A. R., & Bearhop, S. (2009). Influence of trophic position and foraging range on mercury levels within a seabird community. Marine Ecology Progress Series, 375, 277–288.

    Article  CAS  Google Scholar 

  • Azeria, E. T. (2004). Terrestrial bird community patterns on the coralline islands of the Dahlak Archipelago, Red Sea, Eritrea. Glob. Ecol. Biog., 13(2), 177–187.

    Article  Google Scholar 

  • Ballance, L., & Pitman, R. (1999). Foraging ecology of tropical seabirds. In N. J. Adams & R. H. Slotow (Eds.), Proc. 22 Int. Ornithol. Congr., Durban (pp. 2057–2071). Johannesburg: BirdLife South Africa.

    Google Scholar 

  • Bargagli, R., Monaci, F., Sanchez-Hernandez, J. C., & Cateni, D. (1998). Biomagnification of mercury in an Antarctic marine coastal food web. Marine Ecology Progress Series, 169(4), 65–76.

    Article  CAS  Google Scholar 

  • Blais, J. M., Macdonald, R. W., Mackay, D., Webster, E., Harvey, C., & Smol, J. P. (2007). Biologically mediated transport of contaminants to aquatic systems. Environmental Science and Technology, 41(4), 1075–1084.

    Article  CAS  Google Scholar 

  • Brown, T. A., Nelson, D. E., Vogel, J. S., & Southon, J. R. (1988). Improved collagen extraction by modified Longin method. Radiocarbon, 30(2), 171–177.

    CAS  Google Scholar 

  • Burger, J., & Gochfeld, M. (2000). Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. The Science of the Total Environment, 257(1), 37–52.

    Article  CAS  Google Scholar 

  • Cao, L. (2005). Population ecology of the red-footed booby on the Xisha Archipelago. Ph.D. dissertation: University of Science and Technology of China.

    Google Scholar 

  • Cao, L., Pan, Y. L., & Liu, N. F. (2007). Waterbirds of the Xisha Archipelago, South China Sea. Waterbirds, 30(2), 296–300.

    Article  Google Scholar 

  • Chamberlain, C. P., Waldbauer, J. R., Fox-Dobbs, K., Newsome, S. D., Koch, P. L., Smith, D. R., et al. (2005). Pleistocene to recent dietary shifts in California condors. Proc. Nat. Acad. Sci. USA, 102(46), 16707–16711.

    Article  CAS  Google Scholar 

  • Choy, E. S., Kimpe, L. E., Mallory, M. L., Smol, J. P., & Blais, J. M. (2010). Contamination of an arctic terrestrial food web with marine-derived persistent organic pollutants transported by breeding seabirds. Environmental Pollution, 158(11), 3431–3438.

    Article  CAS  Google Scholar 

  • Costa, R. A., Eeva, T., Eira, C., Vaqueiro, J., & Vingada, J. V. (2013). Assessing heavy metal pollution using Great Tits (Parus major): feathers and excrements from nestlings and adults. Environmental Monitoring and Assessment, 185(6), 5339–5344.

    Article  CAS  Google Scholar 

  • Dauwe, T., Bervoets, L., Blust, R., Pinxten, R., & Eens, M. (2000). Can excrement and feathers of nestling songbirds be used as biomonitors for heavy metal pollution? Archives of Environmental Contamination and Toxicology, 39(4), 541–546.

    Article  CAS  Google Scholar 

  • Duffy, D. C. (1983). Competition for nesting space among Peruvian guano birds. Auk, 100(3), 680–688.

    Google Scholar 

  • Duffy, D. C., & La Cock, G. D. (1985). Partitioning of nesting space among seabirds of the Benguela upwelling region. Ostrich, 56(1), 186–201.

    Article  Google Scholar 

  • Emslie, S. D., Coats, L., & Licht, K. (2007). A 45,000 yr record of Adélie penguins and climate change in the Ross Sea, Antarctica. Geology, 35(1), 61–64.

    Article  Google Scholar 

  • Endo, T., Hisamichi, Y., Kimura, O., Kotaki, Y., Kato, Y., Ohta, C., et al. (2009). Contamination levels of mercury in the muscle of female and male spiny dogfishes (Squalus acanthias) caught off the coast of Japan. Chemosphere, 77(10), 1333–1337.

    Article  CAS  Google Scholar 

  • Endo, T., Hisamichi, Y., Kimura, O., Ogasawara, H., Ohta, C., Koga, N., et al. (2013). Levels of mercury in muscle and liver of star-spotted dogfish (Mustelus manazo) from the northern region of Japan: a comparison with spiny dogfish (Squalus acanthias). Archiv. Environ. Contam. Toxicol., 64(3), 467–474.

    Article  CAS  Google Scholar 

  • Endo, T., Kimura, O., Ogasawara, H., Ohta, C., Koga, N., Kato, Y., et al. (2015). Mercury, cadmium, zinc and copper concentrations and stable isotope ratios of carbon and nitrogen in tiger sharks (Galeocerdo cuvier) culled off Ishigaki Island. Japan. Ecol. Indicat., 55, 86–93.

    Article  CAS  Google Scholar 

  • Endo, T., Kimura, O., Ohta, C., Koga, N., Kato, Y., Fujii, Y., et al. (2016). Metal concentrations in the liver and stable isotope ratios of carbon and nitrogen in the muscle of silvertip shark (Carcharhinus albimarginatus) culled off Ishigaki Island, Japan: changes with growth. PloS ONE, 11(2), e0147797. doi:10.1371/journal.pone.0147797.

    Article  Google Scholar 

  • Exploration Group of Xisha Islands of Institute of Soil Science of Chinese Academy of Sciences. (1977). Soil and guano phosphorus mine in Xi-Sha Islands. Beijing: Science Press (in Chinese with English abstract).

    Google Scholar 

  • Exploration Group of Xisha Islands of Plant Institute of Guangdong Province. (1977). Plants and vegetation on Xisha Islands of China. Beijing: Science Press (in Chinese with English abstract).

    Google Scholar 

  • Fry, B. (2007). Stable isotope ecology. New York: Springer Science & Business Media.

    Google Scholar 

  • Fu, X., Feng, X., Zhang, G., Xu, W., Li, X., Yao, H., et al. (2010). Mercury in the marine boundary layer and seawater of the South China Sea: concentrations, sea/air flux, and implication for land outflow. J. Geophy. Res-Atmospheres, 115(D6), 620–631.

    Google Scholar 

  • Gong, Z. T., Huang, B., & Zhou, R. R. (1997). Pedogeochemistry and bioavailability of soils in South China Sea Islands. Acta Pedologica Sin., 34(1), 10–27 (in Chinese with English abstract).

    CAS  Google Scholar 

  • Hawke, D. J. (2006). Soil P in a forested seabird colony: inventories, parent material contributions, and N: P stoichiometry. Soil Res., 43(8), 957–962.

    Article  Google Scholar 

  • Hawke, D. J., Holdaway, R. N., Causer, J. E., & Ogden, S. (1999). Soil indicators of pre-European seabird breeding in New Zealand at sites identified by predator deposits. Austra. J. Soil Res., 37(1), 103–113.

    Article  Google Scholar 

  • Hedges, R. E., & Reynard, L. M. (2007). Nitrogen isotopes and the trophic level of humans in archaeology. Journal of Archaeological Science, 34(8), 1240–1251.

    Article  Google Scholar 

  • Hobson, K. A. (1999). Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia, 120(3), 314–326.

    Article  Google Scholar 

  • Hylander, L. D., & Meili, M. (2003). 500 years of mercury production: global annual inventory by region until 2000 and associated emissions. The Science of the Total Environment, 304(1), 13–27.

    Article  CAS  Google Scholar 

  • Lavoie, R. A., Champoux, L., Rail, J. F., & Lean, D. R. (2010). Organochlorines, brominated flame retardants and mercury levels in six seabird species from the Gulf of St. Lawrence (Canada): relationships with feeding ecology, migration and molt. Environmental Pollution, 158(6), 2189–2199.

    Article  CAS  Google Scholar 

  • Lewis, S., Sherratt, T. N., Hamer, K. C., & Wanless, S. (2001). Evidence of intra-specific competition for food in a pelagic seabird. Nature, 412, 816–819.

    Article  CAS  Google Scholar 

  • Liu, X., Xu, L., Chen, Q., Sun, L., Wang, Y., Yan, H., et al. (2012). Historical change of mercury pollution in remote Yongle Archipelago, South China Sea. Chemosphere, 87(5), 549–556.

    Article  CAS  Google Scholar 

  • Liu, X., Zhao, S., Sun, L., Yin, X., Xie, Z., Honghao, L., et al. (2006). P and trace metal contents in biomaterials, soils, sediments and plants in colony of red-footed booby (Sula sula) in the Dongdao Island of South China Sea. Chemosphere, 65(4), 707–715.

    Article  CAS  Google Scholar 

  • Longin, R. (1971). New method of collagen extraction for radiocarbon dating. Nature, 230, 241.

    Article  CAS  Google Scholar 

  • Lu, Y. C., Yang, X. C., & Jia, R. F. (1979). Quarternary biological sediments in the Xisha Archipelago, China and a discussion on the age of island-formation. Geochimica, 2, 93–102 (in Chinese with English abstract).

    Google Scholar 

  • Metcheva, R., Yurukova, L., & Teodorova, S. E. (2011). Biogenic and toxic elements in feathers, eggs, and excreta of gentoo penguin (Pygoscelis papua ellsworthii) in the Antarctic. Environmental Monitoring and Assessment, 182(1-4), 571–585.

    Article  CAS  Google Scholar 

  • Michelutti, N., Blais, J. M., Mallory, M. L., Brash, J., Thienpont, J., Kimpe, L. E., et al. (2010). Trophic position influences the efficacy of seabirds as metal biovectors. Proc. Nat. Acad. Sci. USA, 107(23), 10543–10548.

    Article  CAS  Google Scholar 

  • Michelutti, N., Keatley, B. E., Brimble, S., Blais, J. M., Liu, H., Douglas, M. S., et al. (2009). Seabird-driven shifts in Arctic pond ecosystems. Proc. Royal Soc. B-Bio. Sci, 276(1656), 591–596.

    Article  Google Scholar 

  • Mizota, C. (2009). Nitrogen isotopic patterns of vegetation as affected by breeding activity of black-tailed gull (Larus crassiostris): a coupled analysis of feces, inorganic soil nitrogen and flora. Appl. Geoche., 24(11), 2027–2033.

    Article  CAS  Google Scholar 

  • Morel, F. M., Kraepiel, A. M., & Amyot, M. (1998). The chemical cycle and bioaccumulation of mercury. Annu. Rev. Ecol. System., 29, 543–566.

    Article  Google Scholar 

  • Morton, B., & Blackmore, G. (2001). South China Sea. Marine Pollution Bulletin, 42(12), 1236–1263.

    Article  CAS  Google Scholar 

  • Nie, Y., Liu, X., Wen, T., Sun, L., & Emslie, S. D. (2014). Environmental implication of nitrogen isotopic composition in ornithogenic sediments from the Ross Sea region, East Antarctica: Δ15N as a new proxy for avian influence. Chemical Geology, 363, 91–100.

    Article  CAS  Google Scholar 

  • Oskam, C. L., Allentoft, M. E., Walter, R., Scofield, R. P., Haile, J., Holdaway, R. N., et al. (2012). Ancient DNA analyses of early archaeological sites in New Zealand reveal extreme exploitation of moa (Aves: Dinornithiformes) at all life stages. Quaternary Science Reviews, 52, 41–48.

    Article  Google Scholar 

  • Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology, 83, 703–718.

    Article  Google Scholar 

  • Rumbold, D., Wasno, R., Hammerschlag, N., & Volety, A. (2014). Mercury accumulation in sharks from the coastal waters of southwest Florida. Archiv. Environ. Contam. Toxicol, 67, 402–412.

    Article  CAS  Google Scholar 

  • Santos, A., Whittaker, R. J., Triantis, K. A., Borges, P. A., Jones, O. R., Quicke, D. L., et al. (2010). Are species–area relationships from entire archipelagos congruent with those of their constituent islands? Glob. Ecol. Biog, 19(4), 527–540.

    Google Scholar 

  • Signa, G., Tramati, C. D., & Vizzini, S. (2013). Contamination by trace metals and their trophic transfer to the biota in a Mediterranean coastal system affected by gull guano. Marine Ecology Progress Series, 479, 13–24.

    Article  CAS  Google Scholar 

  • Stimpson, C. M. (2013). A 48,000 year record of swiftlets (Aves: Apodidae) in North-western Borneo: morphometric identifications and palaeoenvironmental implications. Palaeogeogr. Palaeoclim. Palaeoecol., 374, 132–143.

    Article  Google Scholar 

  • Sun, L., & Xie, Z. (2001). Changes in lead concentration in Antarctic penguin droppings during the past 3,000 years. Environmental Geology, 40(10), 1205–1208.

    Article  CAS  Google Scholar 

  • Sun, L., Xie, Z., & Zhao, J. (2000). A 3,000-year record of penguin populations. Nature, 407, 858.

    Article  CAS  Google Scholar 

  • Tu, N. P. C., Ha, N. N., Haruta, S., & Takeuchi, I. (2014). Trace element concentrations in barramundi (Lates calcarifer) collected along the coast of Vietnam. Marine Pollution Bulletin, 85, 686–695.

    Article  CAS  Google Scholar 

  • Tu, N. P., Ha, N. N., Matsuo, H., Tuyen, B. C., Tanabe, S., & Takeuchi, I. (2012). Biomagnification profiles of trace elements through the food web of an integrated shrimp mangrove farm in Ba Ria Vung Tau, South Vietnam. American Journal of Environmental Sciences, 2, 117–129.

    Google Scholar 

  • Wen, L. S., Jiann, K. T., & Santschi, P. H. (2006). Physicochemical speciation of bioactive trace metals (Cd, Cu, Fe, Ni) in the oligotrophic South China Sea. Marine Chemistry, 101(1), 104–129.

    Article  CAS  Google Scholar 

  • Xu, L. Q. (2015). Impact of climate change and human activity on the eco-environment: an analysis of the Xisha Islands. Berlin: Springer-Verlag.

    Book  Google Scholar 

  • Xu, L. Q., Liu, X. D., Sun, L. G., Chen, Q. Q., Yan, H., Liu, Y., et al. (2011a). A 700-year record of mercury in avian eggshells of Guangjin Island, South China Sea. Environmental Pollution, 159, 889–896.

    Article  CAS  Google Scholar 

  • Xu, L. Q., Liu, X. D., Sun, L. G., Yan, H., Liu, Y., Luo, Y. H., et al. (2011b). Geochemical evidence for the development of coral island ecosystem in the Xisha Archipelago of South China Sea from four ornithogenic sediment profiles. Chemical Geology, 286, 135–145.

    CAS  Google Scholar 

  • Xu, L. Q., Liu, X. D., Sun, L. G., Yan, H., Liu, Y., Luo, Y. H., et al. (2011c). A 2200-year record of seabird population on Ganquan Island, South China Sea. Acta Geol. Sin-Engl., 85(4), 957–967.

    Article  CAS  Google Scholar 

  • Xu, L. Q., Liu, X. D., & Jiang, S. (2014). Late-Holocene seabird palaeodietary record from Ganquan Island, South China Sea. Quat. Internat., 333(3), 139–145.

    Article  Google Scholar 

  • Yan, H., Sun, L., Wang, Y., Liu, X., Qiu, S., & Cheng, W. (2010). A 2000-year record of copper pollution in South China Sea derived from seabird excrements: a potential indicator for copper production and civilization of China. Journal of Paleolimnology, 44(2), 431–442.

    Article  Google Scholar 

  • Yan, H., Wang, Y. H., Cheng, W. H., & Sun, L. G. (2011). Millennial mercury records derived from ornithogenic sediment on Dongdao Island, South China Sea. Journal of Environmental Sciences, 23(9), 1415–1423.

    Article  CAS  Google Scholar 

  • Yin, X. B., Xia, L. J., Sun, L. G., Luo, H. H., & Wang, Y. H. (2008). Animal excrement: a potential biomonitor of heavy metal contamination in the marine environment. The Science of the Total Environment, 399, 179–185.

    Article  CAS  Google Scholar 

  • Zeng, Y., Huang, X., Gu, B., Zhang, D., Zhang, X., & Ye, F. (2015). Analyzing biomagnification of heavy metals in food web from the Pearl River Estuary, South China by stable carbon and nitrogen isotopes. Fresenius Environmental Bulletin, 22(6), 1652–1658.

    Google Scholar 

  • Zhu, A., Zhang, W., Xu, Z., Huang, L., & Wang, W. X. (2013). Methylmercury in fish from the South China Sea: geographical distribution and biomagnification. Marine Pollution Bulletin, 77(1-2), 437–444.

    Article  CAS  Google Scholar 

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Nos. 41402148 and 41376124), China Postdoctoral Science Foundation (No. 2014M550338), and Fundamental Research Funds for the Central Universities (No. 2013bh2x0026). All members of the field study team, including Yan Hong, Liu Yi, Luo Yuhan, Huang Jing, and the Chinese People’s Liberation Army, are acknowledged for their help in sample collection.

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Xu, L., Liu, X. & Nie, Y. Trace elements (Cu, Zn, and Hg) and δ13C/δ15N in seabird subfossils from three islands of the South China Sea and its implications. Environ Monit Assess 188, 274 (2016). https://doi.org/10.1007/s10661-016-5274-7

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