The Impact of Penguins on the Content of Trace Elements and Nutrients in Coastal Soils of North Western Chile and the Antarctic Peninsula Area

  • Winfred Espejo
  • José E. Celis
  • Marco Sandoval
  • Daniel González-Acuña
  • Ricardo Barra
  • Juan Capulín
Article
First Online:
Received:
Accepted:

Abstract

In isolated areas without direct human impact where several species of seabirds nest, transformations affecting the soil come mainly from natural processes, such as chemical enrichment caused by seabirds. Penguins constitute an important bird biomass in the Southern Hemisphere, where they breed in colonies on different sites from 100 to thousands of individuals. The accumulation of trace elements and nutrients in soils within two perennial colonies of Humboldt penguins (Spheniscus humboldti) located in north western Chile and three colonies of Adélie penguins (Pygoscelis adeliae) in the Antarctic Peninsula area were investigated here. Surface soil samples were collected directly from nesting sites. Control samples were taken outside the colonies within sites adjacent to the nesting areas, but not affected by bird excrement. The contents of Cd, Co, Cr, Cu, Mo, Ni, Sr, V and Zn were determined by inductively coupled plasma optical emission spectrometry. Ammonium (NH4) and nitrate (NO3) ions were determined colorimetrically. Extractable potassium (K) was determined by flame emission spectrometry, and available phosphorus (Olsen-P) was determined by spectrophotometry. The highest concentrations of trace metals (Cd, Co, Cr, Cu, Mo, V and Zn) and macronutrients (available N, K and P), along with an increase in salinity and acidity levels, were found directly below the seabird colony, a situation occurring in northern Chile as well as in the Antarctic Peninsula area, highlighting the role that penguins have as bio-vectors on generating geochemical changes in different ecosystems. Some terrestrial plants and animals that live near those penguin colonies might be affected at a greater level than the organisms that live in sites similar but distant from colonies of birds. New data about the role of these species of seabirds as bio-vectors of chemical contaminants are added.

Keywords

Trace metals Heavy metals Nutrients Seabirds Soil Biotransport Penguins 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We thank the Instituto Antártico Chileno (INACH) for providing logistical support. This study was financially supported by the project INACH RG 09–14 granted to J. Celis, project VRID 214.074.051-1.0 granted to M. Sandoval and project FONDAP-CONICYT CRHIAM 15-13-0015 granted to R. Barra. Also, many thanks are due to Dr. Mario Briones for all the statistical analyses. We finally thank Diane Haughney and Jeff Elhai for their useful contributions of the English revision.

References

  1. Aislabie, J. M., Balks, M. R., Foght, J. M., & Waterhouse, E. J. (2004). Hydrocarbon spills on Antarctic soils: effects and management. Environmental Science and Technology, 38, 1265–1274.CrossRefGoogle Scholar
  2. Anderson, W. B., & Polis, G. A. (1999). Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands. Oecologia, 118, 324–332.CrossRefGoogle Scholar
  3. ATSDR. (2016). Agency for toxic substances and disease registry. http://www.atsdr.cdc.gov. Accessed 9 Sept 2016
  4. Barałkiewicz, D., & Siepak, J. (1999). Chromium, nickel and cobalt in environmental samples and existing legal norms. Polish Journal of Environmental Studies, 8, 201–208.Google Scholar
  5. Barbosa, A., De Mas, E., Benzal, J., Diaz, J., Motas, M., Jerez, S., Pertierra, L., Benayas, J., Justel, A., Lauzurica, P., Garcia-Peña, F., & Serrano, T. (2013). Pollution and physiological variability in Gentoo penguins at two rookeries with different levels of human visitation. Antarctic Science, 25, 329–338.CrossRefGoogle Scholar
  6. Bettinelli, M., Beone, G. M., Spezia, S., & Baffi, C. (2000). Determination of heavy metals in soils and sediments by microwave-assisted digestion and inductively cupled plasma optical emission spectrometry analysis. Analytica Chimica Acta, 424, 289–296.CrossRefGoogle Scholar
  7. Blais, J. M., Kimpe, L. E., McMahon, D., Keatley, B. E., Mallory, M. L., Douglas, M. S. V., & Smol, J. P. (2005). Arctic seabirds transport marine-derived contaminants. Science, 309, 445. doi: 10.1126/science.1112658.CrossRefGoogle Scholar
  8. Bockheim, J. G. (1997). Properties and classification of cold desert soils. Soil Science Society of America Journal, 61, 224–231.CrossRefGoogle Scholar
  9. Boersma, P. D. (2008). Penguins as marine sentinels. Bioscience, 58, 597–607.CrossRefGoogle Scholar
  10. Brimble, S. K., Foster, K. L., Mallory, M. L., MacDonald, R. W., Smol, J. P., & Blais, J. M. (2009). High arctic ponds receiving biotransported nutrients from a nearby seabird colony are also subject to potentially toxic loadings of arsenic, cadmium, and zinc. Environmental Toxicology and Chemistry, 28, 2426–2433.CrossRefGoogle Scholar
  11. Bueno, M. B., Schaefer, G. R., De Freitas, P., Simas, F. N., Pereira, T. C., & Rodrigues, E. (2011). Heavy metals contamination in century-old manmade technosols of Hope Bay, Antarctic Peninsula. Water, Air, and Soil Pollution, 222, 91–102.CrossRefGoogle Scholar
  12. Burton, G. A. (2002). Sediment quality criteria in use around the world. Limnology, 3, 65–75.CrossRefGoogle Scholar
  13. Celis, J., Espejo, W., González-Acuña, D., Jara, S., & Barra, R. (2014). Assessment of trace metals and porphyrins in excreta of Humboldt penguins (Spheniscus humboldti) in different locations of the northern coast of Chile. Environmental Monitoring and Assessment, 186, 1815–1824. doi: 10.1007/s10661-013-3495-6.CrossRefGoogle Scholar
  14. Celis, J. E., Barra, R., Espejo, W., González-Acuña, D., & Jara, S. (2015). Trace element concentrations in biotic matrices of Gentoo penguins (Pygoscelis papua) and coastal soils from different locations of the Antarctic Peninsula. Water, Air, and Soil Pollution, 226, 2266. doi: 10.1007/s11270-014-2266-5.CrossRefGoogle Scholar
  15. Choy, E. S., Gauthier, M., Mallory, M. L., Smol, J. P., Lean, D., & Blais, J. M. (2010). An isotopic investigation of mercury accumulation in terrestrial food webs adjacent to an Arctic seabird colony. Science of the Total Environment, 408, 1858–1867.CrossRefGoogle Scholar
  16. CQG. (1999). Canadian soil quality guidelines for the protection of environmental and human health. http://ceqg-rcqe.ccme.ca/en/index.html#void. Accessed 10 Sept 2016.
  17. Ellis, J. C. (2005). Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecology, 181, 227–241.Google Scholar
  18. Ellis, J. C., Farina, J. M., & Witman, J. D. (2006). Nutrient transfer from sea to land: the case of gulls and cormorants in the Gulf of Maine. Journal of Animal Ecology, 75, 565–574.CrossRefGoogle Scholar
  19. Gabler, H. E., Gluh, K., Bahr, A., & Utermann, J. (2009). Quantification of vanadium adsorption by German soils. Journal of Geochemical Exploration, 103, 37–44.CrossRefGoogle Scholar
  20. García, L. V., Marañón, T., Ojeda, F., Clemente, L., & Redondo, R. (2002). Seagull influence on soil properties, chenopod shrub distribution, and leaf nutrient status in semi-arid Mediterranean islands. OIKOS, 98, 75–86.CrossRefGoogle Scholar
  21. 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. Australian Journal of Soil Research, 37, 103–113.CrossRefGoogle Scholar
  22. He, Z. L. L., Yang, X. E., & Stoffella, P. J. (2005). Trace elements in agroecosystems and impacts on the environment. Journal of Trace Elements in Medicine and Biology, 19, 25–140.CrossRefGoogle Scholar
  23. Headley, A. D. (1996). Heavy metals concentrations in peat profiles from the high Arctic. Science of the Total Environment, 177, 105–111.CrossRefGoogle Scholar
  24. Hutchinson, G. E. (1950). Survey of existing knowledge of biogeochemistry. III. The biogeochemistry of vertebrate excretion. Bulletin of the American Museum of Natural History, 96, 1–554.Google Scholar
  25. Jerez, S., Motas, M., Benzal, J., Díaz, J., Vidal, V., D’Amico, V., & Barbosa, A. (2013). Distribution of metals and trace elements in adult and juvenile penguins from the Antarctic Peninsula area. Environmental Science and Pollution Research, 20, 3300–3311.CrossRefGoogle Scholar
  26. Kobus, J., & Kurek, E. (1990). Effect of cadmium contained in plant residues on their microbial decomposition. Zentralblatt für Mikrobiologie, 145, 283–291.Google Scholar
  27. Li, H. F., Gray, C., Micó, C., Zhao, F. J., & McGrath, S. P. (2009). Phytotoxicity and bioavailability of cobalt to plants in a range of soils. Chemosphere, 75, 979–986.CrossRefGoogle Scholar
  28. Liang, C. N., & Tabatabai, M. A. (1977). Effects of trace elements on nitrification in soils. Journal of Environmental Quality, 7, 291–293.CrossRefGoogle Scholar
  29. Ligeza, S., & Smal, H. (2003). Accumulation of nutrients in soil affected by perennial colonies of piscivorous birds with reference to biogeochemical cycles of elements. Chemosphere, 52, 595–602.CrossRefGoogle Scholar
  30. Liu, X. D., Sun, L. G., & Yin, X. B. (2004). Textural and geochemical characteristics of proglacial sediments: a case study in the foreland of Nelson Ice Cap, Antarctica. Acta Geologica Sinica, 78, 970–981.Google Scholar
  31. Liu, X., Zhao, S., Sun, L., Yin, X., Xie, Z., Honghao, L., & Wang, Y. (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, 707–715.CrossRefGoogle Scholar
  32. Lynch, H. J., Crosbie, K., Fagan, W. F., & Naveen, R. (2010). Spatial patterns of tour ship traffic in the Antarctic Peninsula region. Antarctic Science, 22, 123–130.CrossRefGoogle Scholar
  33. Madrid, F., Díaz-Barrientos, E., & Madrid, L. (2005). Elementos traza y nutrientes en suelos y herbáceas de parques y zonas verdes de Sevilla. Edafología, 12, 29–42 [In Spanish with English summary].Google Scholar
  34. Mallory, M. L., Mahon, L., Tomlik, M. D., White, C., Milton, G. R., & Spooner, I. (2015). Colonial marine birds influence island soil chemistry through biotransport of trace elements. Water, Air, and Soil Pollution, 226, 31. doi: 10.1007/s11270-015-2314-9.CrossRefGoogle Scholar
  35. Margon, A., Mondini, C., Valentini, M., Ritota, M., & Leita, L. (2013). Soil microbial biomass influence on strontium availability in mine soil. Chemical Speciation and Bioavailability, 25, 119–124.CrossRefGoogle Scholar
  36. McGrath, S. P., Micó, C., Zhao, F. J., Stroud, J. L., Zhang, H., & Fozard, S. (2010). Predicting molybdenum toxicity to higher plants: estimation of toxicity threshold values. Environmental Pollution, 158, 3085–3094.CrossRefGoogle Scholar
  37. Michelutti, N., Keatley, B., Brimble, S., Blais, J. M., Liu, H., Douglas, M., Mallory, M. L., Macdonald, R. W., & Smol, J. P. (2009). Seabird-driven shifts in Arctic pond ecosystems. Proceedings of the Royal Society B-Biological Sciences, 276, 591–596.CrossRefGoogle Scholar
  38. Micó, C., Li, H. F., Zhao, F. J., & McGrath, S. P. (2008). Use of Co speciation and soil properties to explain variation in Co toxicity to root growth of barley (Hordeum vulgare L.) in different soils. Environmental Pollution, 156, 883–890.CrossRefGoogle Scholar
  39. Moral, R., Pérez-Murcia, M. D., Pérez-Espinosa, A., Moreno-Caselles, J., Paredes, C., & Rufete, B. (2008). Salinity, organic content, micronutrients and heavy metals in pig slurries from South-eastern Spain. Waste Management, 28, 367–371.CrossRefGoogle Scholar
  40. Motavalli, P. P., Palm, C. A., Parton, W. J., Elliott, E. T., & Frey, S. D. (1995). Soil pH and organic C dynamics in tropical forest soils: evidence from laboratory and simulation studies. Soil Biology and Biochemistry, 27, 1589–1599.CrossRefGoogle Scholar
  41. Nygard, T., Lie, E., Rov, N., & Steinnes, E. (2001). Metal dynamics in an Antarctic food chain. Marine Pollution Bulletin, 42, 598–602.CrossRefGoogle Scholar
  42. Polis, G. A., Anderson, W. B., & Holt, R. D. (1997). Towards an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics, 29, 289–316.CrossRefGoogle Scholar
  43. Ribeiro, A. P., Figueira, R. C. L., Martins, C. C., Silva, C. R. A., França, E. J., Bícego, M. C., Mahiques, M. M., & Montone, R. C. (2011). Arsenic and trace metal contents in sediment profiles from the Admiralty Bay, King George Island, Antarctica. Marine Pollution Bulletin, 62, 192–196.CrossRefGoogle Scholar
  44. Rooney, C. P., Zhao, F. J., & McGrath, S. P. (2006). Soil factors controlling the expression of copper toxicity to plants in a wide range of European soils. Environmental Toxicology and Chemistry, 25, 726–732.CrossRefGoogle Scholar
  45. Rooney, C. P., Zhao, F. J., & McGrath, S. P. (2007). Phytotoxicity of nickel in a range of European soils: influence of soil properties, Ni solubility and speciation. Environmental Pollution, 145, 596–605.CrossRefGoogle Scholar
  46. Rundel, P. W., Dillon, M. O., & Palma, B. (1996). Flora and vegetation of Pan de Azucar National Park in the Atacama desert of northern Chile. Gayana Botanica, 53, 295–315.Google Scholar
  47. Sadzawka, A., M. Carrasco, R. Grez, M. Mora, H. Flores y A. Neaman. (2006). Methods of analysis recommended for soils of Chile: 2006 review. [In Spanish]. http://www.inia.cl/medios/biblioteca/serieactas/NR33998.pdf. Accessed 12 March 2016.
  48. Santos, I. R., Silva-Filho, E. V., Schaefer, C. E., Albuquerque-Filho, M. R., & Campos, L. S. (2005). Heavy metal contamination in coastal sediments and soils near the Brazilian Antarctic Station, King George Island. Marine Pollution Bulletin, 50, 185–194.CrossRefGoogle Scholar
  49. Singh, B. R. (1990). Cadmium and fluoride uptake by oats and rape from phosphate fertilizers in two different soils: Cadmium and fluoride uptake by plants from phosphorus fertilizers. Norwegian Journal of Agricultural Sciences, 4, 239–250.Google Scholar
  50. Smith, V. R. (1979). The influence of seabird manuring on the phosphorus status of Marion Island (Subantarctic) soils. Oecologia, 41, 123–126.CrossRefGoogle Scholar
  51. Srivastava, O. P., & Sethi, B. C. (1981). Contribution of farm yard manure on the build up of available zinc in an aridisol. Communications in Soil Science and Plant Analysis, 12, 355–361.CrossRefGoogle Scholar
  52. Sun, L. G., & Xie, Z. Q. (2001). Changes in lead concentration in Antarctic penguin droppings during the past 3000 years. Environmental Geology, 40, 1205–1208.CrossRefGoogle Scholar
  53. Tatur, A., & Myrcha, A. (1984). Ornithogenic soils on King George Island, South Shetland Islands (Maritime Antarctic Zone). Polish Polar Research, 5, 31–60.Google Scholar
  54. Tin, T., Fleming, Z. L., Hughes, K. A., Ainley, D. G., Convey, P., Moreno, C. A., Pfeiffer, S., Scott, J., & Snape, I. (2009). Impacts of local human activities on the Antarctic environment. Antarctic Science, 21, 3–33.CrossRefGoogle Scholar
  55. Tong, S. T. (1990). Roadside dusts and soils contamination in Cincinnati, Ohio, U.S.A. Environmental Management, 14, 107–113.CrossRefGoogle Scholar
  56. UChile. (2013). Informe país, estado del medio ambiente en Chile 2012. Universidad de Chile. [In Spanish]. http://www.uchile.cl/publicaciones/97817/informe-pais-estado-del-medio-ambiente-en-chile-2012. Accessed 21 Sept 2016.
  57. Xie, Z., & Sun, L. (2008). A 1,800-year record of arsenic concentration in the penguin dropping sediment, Antarctic. Environmental Geology, 55, 1055–1059.CrossRefGoogle Scholar
  58. Yang, J., Huang, J., Lazzaro, A., Tang, Y., & Zeyer, J. (2014). Response of soil enzyme activity and microbial community in vanadium-loaded soil. Water, Air, and Soil Pollution, 225, 2012. doi: 10.1007/s11270-014-2012-z.CrossRefGoogle Scholar
  59. Yin, X., Xia, L., Sun, L., Luo, H., & Wang, Y. (2008). Animal excrement: a potential biomonitor of heavy metal contamination in the marine environment. Science of the Total Environment, 399, 179–185.CrossRefGoogle Scholar
  60. Zeng, Q. P., Brown, P. H., & Zeng, Q. P. (2000). Soil potassium mobility and uptake by corn under differential soil moisture regimes. Plant and Soil, 221, 121–134.CrossRefGoogle Scholar
  61. Zhu, R., Sun, L., Kong, D., Geng, J., Wang, N., Wang, Q., & Wang, X. (2006). Matrix-bound phosphine in Antarctic biosphere. Chemosphere, 64, 1429–1435.CrossRefGoogle Scholar
  62. Zhu, R., Wang, Q., Ding, W., Wang, C., Hou, L., & Ma, D. (2014). Penguins significantly increased phosphine formation and phosphorus contribution in maritime Antarctic soils. Scientific Reports, 4, 7055. doi: 10.1038/srep07055.CrossRefGoogle Scholar
  63. Ziólek, M., & Melke, J. (2014). The impact of seabirds on the content of various forms of phosphorus in organic soils of the Bellsund coast, western Spitsbergen. Polar Research, 33. doi:  10.3402/polar.v33.19986

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Winfred Espejo
    • 1
  • José E. Celis
    • 2
  • Marco Sandoval
    • 3
  • Daniel González-Acuña
    • 2
  • Ricardo Barra
    • 1
  • Juan Capulín
    • 4
  1. 1.Department of Aquatic Systems, Faculty of Environmental Sciences and EULA Chile CentreUniversidad de ConcepciónConcepciónChile
  2. 2.Department of Animal Science, Facultad de Ciencias VeterinariasUniversidad de ConcepciónChillánChile
  3. 3.Department of Soil and Natural Resources, Facultad de AgronomíaUniversidad de ConcepciónChillánChile
  4. 4.Instituto de Ciencias AgropecuariasUniversidad Autónoma del Estado de HidalgoTulancingoMexico

Personalised recommendations