Skip to main content

Kelp as a Bioindicator: Does it Matter Which Part of 5 M Long Plant is Used for Metal Analysis?

Abstract

Kelp may be useful as a bioindicator because they are primary producers that are eaten by higher trophic level organisms, including people and livestock. Often when kelp or other algae species are used as bioindicators, the whole organism is homogenized. However, some kelp can be over 25 m long from their holdfast to the tip of the blade, making it important to understand how contaminant levels vary throughout the plant. We compared the levels of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in five different parts of the kelp Alaria nana to examine the variability of metal distribution. To be useful as a bioindicator, it is critical to know whether levels are constant throughout the kelp, or which part is the highest accumulator. Kelp were collected on Adak Island in the Aleutian Chain of Alaska from the Adak Harbor and Clam Cove, which opens onto the Bering Sea. In addition to determining if the levels differ in different parts of the kelp, we wanted to determine whether there were locational or size-related differences. Regression models indicated that between 14% and 43% of the variation in the levels of arsenic, cadmium, chromium, manganese, mercury, and selenium was explained by total length, part of the plant, and location (but not for lead). The main contributors to variability were length (for arsenic and selenium), location (mercury), and part of the plant (for arsenic, cadmium, chromium and manganese). The higher levels of selenium occurred at Clam Cove, while mercury was higher at the harbor. Where there was a significant difference among parts, the holdfast had the highest levels, although the differences were not great. These data indicate that consistency should be applied in selecting the part of kelp (and the length) to be used as a bioindicator. While any part of Alaria could be collected for some metals, for arsenic, cadmium, chromium, and manganese a conversion should be made among parts. In the Aleutians the holdfast can be perennial while the blade, whipped to pieces by winter wave action, is regrown each year. Thus the holdfast may be used for longer-term exposure for arsenic, cadmium, chromium and manganese, while the blade can be used for short-term exposure for all metals. Cadmium, lead and selenium were at levels that suggest that predators, including people, may be at risk from consuming Alaria. More attention should be devoted to heavy metal levels in kelp and other algae from Adak, particularly where they may play a role in a subsistence diets.

This is a preview of subscription content, access via your institution.

References

  • Al-Masri, M. S., Mamish, S., & Budier, Y. (2003). Radionuclides and trace metals in eastern Mediterranean sea algae. Journal of Environmental Radioactivity, 67, 157–168.

    Article  CAS  Google Scholar 

  • ATSDR (2002). Public health assessment: Naval Air Facility, Adak. http://www.atsdr.cdc.gov/HAC/PHA/adak/ada_toc.htmlv (accessed 6/13/06).

  • Black, W. A. P., & Mitchell, R. L. (1952). Trace elements in the common brown algae and in sea water. Journal of the Marine Biological Association of the United Kingdom, 30, 575–584.

    CAS  Google Scholar 

  • Blackmore, G. (1998). An overview of trace metal pollution in the coastal waters of Hong Kong. Science of the Total Environment, 214, 21–48.

    Article  CAS  Google Scholar 

  • Bryan, G. W. (1969). The absorption of zinc and other metals by the brown seaweed Laminaria digitata. Journal of the Marine Biological Association of the United Kingdom, 49, 225–243.

    CAS  Google Scholar 

  • Bryan, G. W. (1971). The effects of heavy metals (other than mercury) on marine and estuarine organisms. Proceedings of the Royal Society of London, Ser. B, 177, 389–410.

    CAS  Google Scholar 

  • Bryan, G. W., & Hummerstone, L. G. (1973). Brown seaweed as an indicator of heavy metals in estuaries in South-west England. Journal of the Marine Biological Association of the United Kingdom, 53, 705–720.

    CAS  Google Scholar 

  • Bull, K. R., Murton, R. K., Osborn, D., & Ward, P. (1977). High levels of cadmium in Atlantic seabirds and sea-skaters. Nature, 269, 507–509.

    Article  CAS  Google Scholar 

  • Burger, J. (2006). Bioindicators: Types, development, and use in ecological assessment and research. Environmental Bioindicators, 1, 1–18.

    Google Scholar 

  • Burger, J., Gaines, K. F., Peles, J. D., Stephens Jr., W. L., Boring, C. S., Brisbin, Jr., I. L. et al. (2001). Radiocesium in fish from the Savannah River and Steel Creek: Potential food chain exposure to the public. Risk Analysis, 21, 545–559.

    Article  CAS  Google Scholar 

  • Burger, J., & Gochfeld, M. (2000). Effects of lead on birds (Laridae): A review of laboratory and field studies. Journal of Toxicology and Environmental Health, 3, 59–78.

    Article  CAS  Google Scholar 

  • Burger, J., & Gochfeld, M. (2001). On developing bioindicators for human and ecological health. Environmental Monitoring and Assessment, 66, 23–46.

    Article  CAS  Google Scholar 

  • Burger, J., & Gochfeld, M. (2004a). Bioindicators for assessing human and ecological health. In G. B. Wiersma (Ed.), Environmental monitoring (pp. 541–566). Boca Raton, Florida: CRC.

    Google Scholar 

  • Burger, J., & Gochfeld, M. (2004b). Mercury in canned tuna: White versus light and temporal variation. Environmental Research, 94, 239–249.

    Article  CAS  Google Scholar 

  • Burger, J., & Gochfeld, M. (2005). Heavy metals in commercial fish in New Jersey. Environmental Research, 99, 403–412.

    Article  CAS  Google Scholar 

  • Burger, J., & Gochfeld, M. (in press). Locational differences in heavy metals in Pacific blue mussels Mytilus [edulis] trossulus from Adak in the Aleutian Chain. Science of the Total Environment. sub.

  • CAFF (Conservation of Arctic Flora and Fauna) (2001). Arctic flora and fauna: Status and conservation. Helsinki, Edita, 272 pp.

  • Caliceti, M., Argese, E., Sfriso, A., & Pavoini, B. (2002). Heavy metal contamination in the seaweeds of the Venice lagoon. Chemosphere, 47, 443–454.

    Article  CAS  Google Scholar 

  • Carignan, V., & Villard, M. A. (2001). Selecting indicator species to monitor ecological integrity: A review. Environmental Monitoring and Assessment, 78, 45–61.

    Article  Google Scholar 

  • Chan, H. M., Kim, C., Khoday, K., Receveur, O., & Kuhnlein, H. V. (1995). Assessment of dietary exposure to trace metals in Baffin Inuit food. Environmental Health Perspectives, 103, 740–746.

    Article  CAS  Google Scholar 

  • Codex Alimentarius Commission (2002). Codex committee on food additives and contaminants: Maximum level for lead in fish. Joint FAO/WHO Food Standards Programme’, Document CL-2002 10-FAC. United Nations, Rome.

  • Codex Alimentarius Commission (2003). Codex committee on food additives and contaminants: Schedule 1 of the proposed draft general standard for contaminants and toxins in food. Document CX/FAC 3/18, Rome.

  • Coyle, J. J., Ingersoll, D. R., Fairchild, C. G., & May, T. W. (1993). Effects of dietary selenium on the reproductive success of bluegills (Lepomis macrochirus). Environmental Toxicology and Chemistry, 12, 551–565.

    CAS  Google Scholar 

  • Dean, T. A., Thies, K., & Lagos, S. L. (1989). Survival of juvenile giant kelp: The effects of demographic factors, competition, and grazers. Ecology, 70, 483–495.

    Article  Google Scholar 

  • Eisler, R. (1985). Cadmium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Rep, 85(1.4), Washington, District of Columbia.

  • Eisler, R. (1986). Chromium hazards to fish, wildlife, and invertebrates: A synoptic review. US Fish and Wildlife Service Rep, 85(1.6), Washington, District of Columbia.

  • Eisler, R. (1987). Mercury hazards to fish, wildlife, and invertebrates: A synoptic review. US Fish and Wildlife Service Rep, 85(1.10), Washington, District of Columbia.

  • Eisler, R. (1988). Lead hazards to fish, wildlife, and invertebrates: A synoptic review. U. S. Fish and Wildlife Service, Washington, District of Columbia.

  • Eisler, R. (1994). A review of arsenic hazards to plants and animals with emphasis on fishery and wildlife resources. In J. O. Nriagu (Ed.), Arsenic in the environment part, II. New York, New York: Wiley.

    Google Scholar 

  • Fowler, S. W. (1990). Critical review of selected heavy metal and chlorinated hydrocarbon concentrations in the marine environment. Marine Environmental Research, 29, 1–64.

    Article  CAS  Google Scholar 

  • Fuge, R., & James, K. H. (1973). Trace metal concentrations in brown seaweeds, Cardigan Bay, Wales. Marine Chemistry, 1, 281–293.

    Article  CAS  Google Scholar 

  • Fuge, R., & James, K. H. (1974). Trace metal concentrations in Fucus from the Bristol Channel. Marine Pollution Bulletin, 5, 9–12.

    Article  CAS  Google Scholar 

  • Furness, R. W. (1996). Cadmium in birds. In W. N. Beyer, G. H. Heinz, & A. W. Redmom-Norwood (Eds.), Environmental contaminants in wildlife: Interpreting tissue concentrations (pp. 389–404). Boca Raton, Florida: Lewis.

    Google Scholar 

  • Gao, Y. (2001). Atmospheric deposition of trace elements, mercury and nitrogen to the New York-New Jersey harbor estuary. Unpublished manuscript, Rutgers University, Piscataway, New Jersey.

  • Garza, D. (2005). Common edible seaweeds in the Gulf of Alaska. Fairbanks, Alaska: Alaska Sea Grant Program.

    Google Scholar 

  • Haritonidis, S., & Malea, P. (1995). Seasonal and local variation of Cr, Ni and Co concentrations in Ulva rigida C. Agardh and Enteromorpha linza (Linneaeus) from Thermaikos Gulf, Greece. Environmental Pollution, 89, 319–327.

    Article  CAS  Google Scholar 

  • Hou, X., & Yan, X. (1998). Study on the concentration and seasonal variation of inorganic elements in 35 species of marine algae. Science of the Total Environment, 222, 141–156.

    Article  CAS  Google Scholar 

  • Jackson, L. J. (1998). Paradigms of metal accumulation in rooted aquatic vascular plants. Science of the Total Environment, 219, 223–231.

    Article  CAS  Google Scholar 

  • Kohlhoff, D. W. (2002). Amchitka and the bomb: Nuclear testing in Alaska. Seattle, Washington: University of Washington.

    Google Scholar 

  • Lebednik, P. A., & Palmisano, J. F. (1977). Ecology of marine algae. In M. L. Merritt & R. G. Fuller (Eds.), The environment of Amchitka Island, Alaska (pp. 353–394). Springfield, Virginia: Technical Information Center.

    Google Scholar 

  • Lemly, D. A. (1993a). Guidelines for evaluating selenium data from aquatic monitoring and assessment studies. Environmental Monitoring and Assessment, 28, 83–100.

    Article  CAS  Google Scholar 

  • Lemly, D. A. (1993b). Metabolic stress during winter increases the toxicity of selenium to fish. Aquatic Toxicology, 27, 133–158.

    Article  CAS  Google Scholar 

  • Mehta, S. D., & Gaur, J. P. (2005). Use of algae for removing heavy metal ions from wastewater: Progress and prospects. Critical Reviews in Biotechnology, 25, 113–152.

    Article  CAS  Google Scholar 

  • Miramand, P., & Bentley, D. (1992). Heavy metal concentrations in two biological indicators (Patella vulgata and Fucus serratus) collected near the French nuclear reprocessing plant at La Hague. Science of the Total Environment, 111, 135–149.

    Article  CAS  Google Scholar 

  • OSPAR (Oslo Paris Commission) (1992). Monitoring manual – principles and methodology of the joint monitoring programme. Oslo Paris Commission, Update 1992. Paris, France.

  • Peakall, D. (1992). Animal biomarkers as pollution indicators. London: Chapman and Hall.

    Google Scholar 

  • Phaneuf, D., Cote, I., Duman, P., Ferron, L. A., & LeBlanc, A. (1999). Evaluation of the contamination of marine algae (seaweed) from the St. Lawrence River and likely to be consumed by humans. Environmental Research, 80, 5175–5182.

    Article  Google Scholar 

  • Phillips, D. J. H. (1990). Use of macroalgae and invertebrates as monitors of metal levels in estuarine and coastal waters. In R. W. Furness & P. S. Rainbow (Eds.), Heavy metals in the marine environment (pp. 81–100). Boca Raton, Florida: CRC.

    Google Scholar 

  • Piotrowski, J. K. (1985). Individual exposure and biological monitoring. In V. B. Vouk, G. C. Butler, D. G. Hoel, & D. B. Peakall (Eds.), Methods for estimating risk of chemical injury: Human and non-human biota and ecosystems (pp. 123–135). Chichester, UK: Wiley.

    Google Scholar 

  • Pourian, S., & Smith, M. (1974). Evaluation of digestion techniques for the AAS determination of metal concentrations in kelp. American Chemical Society, 14, 237–244.

    CAS  Google Scholar 

  • Powers, H. A., Coats, R. R., & Nelson, W. H. (1960). Geology and submarine physiography of Amchitka Island, Alaska. U.S. Geological Survey, Bulletin, 1028, 521–554.

    Google Scholar 

  • Ragan, M. A., Smidsrod, O., & Larsen, B. (1979). Chelation of divalent metal ions by brown algal polyphenols. Marine Chemistry, 7, 265–271.

    Article  CAS  Google Scholar 

  • Ray, S., McLeese, D. W., Metcalfe, C. F., Burridge, L. E., & Waiwood, B. A. (1980). Distribution of cadmium marine biota in the vicinity of Belledune. Canadian Technical Report of Fisheries and Aquatic Sciences, 963, 12–27.

    Google Scholar 

  • Ringdal, O., & Julshamn, K. (1985). Effect of selenite on the uptake of methylmercury in cod (Gadus morhua). Bulletin of Environmental Contamination and Toxicology, 35, 335–344.

    Article  CAS  Google Scholar 

  • Sanchez-Rodriguez, I., Huerta-Diaz, M. A., Choumiline, E., Holguin-Quinones, O., & Zertuche-Gonzalez, J. A. (2001). Elemental concentrations in different species of seaweeds from Loreto Bay, Baja California Sur, Mexico: Implications for the geochemical control of metals in algal tissue. Environmental Pollution, 114, 145–160.

    Article  CAS  Google Scholar 

  • Sanchiz, G., Garcia-Carrascosa, A. M., & Pastor, A. (1999). Bioaccumulation of Hg, Cd. Pb, and Zn in four marine phanerogams and the alga Caulerpa prolilfera (Foersskal) Lamouroux from the east coast of Spain. Botanica Marina, 42, 157–164.

    Article  CAS  Google Scholar 

  • Sharp, G. J., Samant, H. S., & Vaidya, O. C. (1988). Selected metal levels of commercially valuable seaweeds adjacent to and distant from point sources of contamination in Nova Scotia and New Brunswick. Bulletin of Environmental Contamination and Toxicology, 40, 724–730.

    Article  CAS  Google Scholar 

  • Spry D. J., & Wiener, G. (1991). Metal bioavailability and toxicity to fish in low alkalinity lakes: A critical review. Environmental Pollution, 71, 243–304.

    Article  CAS  Google Scholar 

  • Statistical Analysis System (SAS). 1995. SAS Users’ Guide, Cary S NC: Statistical Institute, Inc.

  • U.S. Navy (2005). Institutional controls primary site inspection report: Adak Island, Alaska. Poulsbo, Washington: Naval facilities engineering command, U.S. Navy.

  • VanNetten, C., Cann, S. A. H., Morley, D. R., & VanNetten, J. P. (2000). Elemental and radioactive analysis of commercially available seaweed. Science of the Total Environment, 255, 169–175.

    Article  CAS  Google Scholar 

  • Weber, D. N., & Dingel, W. M. (1997). Alterations in neurobehavioral responses in fishes exposed to lead and lead-chelating agents. American Zoologist, 37, 354–362.

    CAS  Google Scholar 

  • White, C., & Gadd, G. M. (1995). Determination of metals and metal fluxes in algae and fungi. Science of the Total Environment, 176, 107–115.

    Article  CAS  Google Scholar 

  • Wiener, J. G., & Spry, D. J. (1996). Toxicological significance of mercury in freshwater fish. In W. N. Beyer, G. H. Heinz, & A. W. Redmon-Norwood (Eds.), Environmental contaminants in wildlife: Interpreting tissue concentrations. Boca Raton, Florida: SETAC, Lewis.

    Google Scholar 

  • World Health Organization (WHO) (1990). IPCS-Methylmercury. Environmental Health Criteria, 101.

  • World Health Organization (WHO) (1991). IPCS-Inorganicmercury. Environmental Health Criteria, 118.

  • Young, M. L. (1975). The transfer of Zn65 and Fe59 along a Fucus serratus (L.) to Littorina obtusata (L.) food chain. Journal of the Marine Biological Association of the United Kingdom, 55, 583–610.

    CAS  Article  Google Scholar 

  • Younker, L. (2002). How we got here: why the Amchitka site was chosen and what tests were conducted. In Proceedings of the Amchitka Island long-term stewardship workshop. CRESP-University of Alaska, Fairbanks, Alaska.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joanna Burger.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Burger, J., Gochfeld, M., Jeitner, C. et al. Kelp as a Bioindicator: Does it Matter Which Part of 5 M Long Plant is Used for Metal Analysis?. Environ Monit Assess 128, 311–321 (2007). https://doi.org/10.1007/s10661-006-9314-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-006-9314-6

Keywords

  • Alaria
  • Algae
  • Aleutian Islands
  • Bioindicator
  • Cadmium
  • Kelp
  • Lead
  • Mercury