Skip to main content

Complexity of bioindicator selection for ecological, human, and cultural health: Chinook salmon and red knot as case studies

Abstract

There is considerable interest in developing bioindicators of ecological health that are also useful indicators for human health. Yet, human health assessment usually encompasses physical/chemical exposures and not cultural well-being. In this paper, we propose that bioindicators can be selected for all three purposes. We use Chinook or king salmon (Oncorhynchus tshawytscha) and red knot (Calidris canutus rufa, a sandpiper) as examples of indicators that can be used to assess human, ecological, and cultural health. Even so, selecting endpoints or metrics for each indicator species is complex and is explored in this paper. We suggest that there are several endpoint types to examine for a given species, including physical environment, environmental stressors, habitat, life history, demography, population counts, and cultural/societal aspects. Usually cultural endpoints are economic indicators (e.g., number of days fished, number of hunting licenses), rather than the importance of a fishing culture. Development of cultural/societal endpoints must include the perceptions of local communities, cultural groups, and tribal nations, as well as governmental and regulatory communities (although not usually so defined, the latter have cultures as well). Endpoint selection in this category is difficult because the underlying issues need to be identified and used to develop endpoints that tribes and stakeholders themselves see as reasonable surrogates of the qualities they value. We describe several endpoints for salmon and knots that can be used for ecological, human, and cultural/societal health.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • Atlantic States Marine Fisheries Commission (ASMFC) (2001). Carl N. Shuster Jr. Horseshoe crab reserve designated. Fisheries Focus. 10(2):8–9.

  • Baker, A. J., Gonzalez, P. M., Piersma, T., Niles, L. J., deLima S.do Nascimento, I., Atkinson, P. W., Collins, P., Clark, N. A., Minton, C. D. T., Peck, M. K., & Aarts, G. (2004). Rapid population decline in Red Knots: fitness consequences of refuelling rates and late arrival in Delaware Bay. Proceedings of the Royal Society of London, 271, 875–882.

  • Bartell, S. M. (2006). Biomarkers, bioindicators, and ecological risk assessment—a brief review and evaluation. Environmental Bioindicators, 1, 39–50.

    Article  Google Scholar 

  • Baumann, P. C. (1992). The use of tumors in wild populations of fish to assess ecosystem health. Journal of Aquatic Ecosystem Health, 1, 135–146.

    Article  Google Scholar 

  • Beratan, K. K., Kabala, S. J., Loveless, S. M., Martin, P. J., & Spyke, N. P. (2004). Sustainability indicators as a communicative tool: building bridges in Pennsylvania. Environmental Monitoring and Assessment, 94, 179–191.

    Article  Google Scholar 

  • Bingham, G., Bishop, R., Brody, M., Bromley, D., Clark, E. E., Cooper, W., Costanza, R., Hale, T., Hayden, G., Kellert, S., Norgaard, R., Norton, B., Payne, J., Russell, C., & Suter, G. (1995). Issues in ecosystems valuation: improving information for decision making. Ecological Economy, 14, 73–90.

    Article  Google Scholar 

  • Bohnee, G., Mathews, J. P., Pinkham, J., Smith, A., & Stanfill, J. (2011). Nez Perce involvement with solving environmental problems: history, perspectives, treaty rights, and obligations. In J. Burger (Ed.), Stakeholders and scientists: achieving implementable solutions to energy and environmental issues (pp. 149–184). New York, NY: Springer.

    Chapter  Google Scholar 

  • Burger, J. (2006a). Bioindicators: types, development, and use in ecological assessment and research. Environmental Bioindicators, 1, 22–39.

    Article  Google Scholar 

  • Burger, J. (2006b). Bioindicators: a review of their use in the environmental literature 1970-2005. Bioindicators, 1, 136–144.

    Article  Google Scholar 

  • Burger, J. (2007). A model for selecting bioindicators to monitor radionuclide concentrations using Amchitka Island in the Aleutians as a case study. Environmental Research, 105, 316–323.

    CAS  Article  Google Scholar 

  • Burger, J. (2009). Stakeholder involvement in indicator selection: case studies and levels of participation. Environmental Bioindicators, 4, 170–190.

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    Google Scholar 

  • Burger, J., & Niles, L. (2012). Shorebirds and stakeholders: effects of beach closure and human activities on shorebirds at a New Jersey coastal beach. Urban Ecosystems, 16, 657–673.

    Article  Google Scholar 

  • Burger, J., Clark, K. L., & Niles, L. (1997). Importance of beach, mudflat and marsh for migrant shorebirds on Delaware Bay. Biological Conservation, 79, 283–292.

    Article  Google Scholar 

  • Burger, J., Carletta, M. A., Lowrie, K., Miller, K. T., & Greenberg, M. (2004a). Assessing ecological resources for remediation and future land uses on contaminated lands. Environmental Management, 34, 1–10.

    Article  Google Scholar 

  • Burger, J., Jeitner, C., Clark, K., & Niles, L. (2004b). The effect of human activities on migrant shorebirds: successful adaptive management. Environmental Conservation, 31(4), 283–288.

    Article  Google Scholar 

  • Burger, J., Carlucci, S. A., Jeitner, C. W., & Niles, L. (2007a). Habitat choice, disturbance, and management of foraging shorebirds and gulls at a migratory stopover. Journal of Coastal Research, 23, 1159–1166.

    Article  Google Scholar 

  • Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., Snigaroff, R., Snigaroff, D., Patrick, R., & Weston, J. (2007b). Mercury levels and potential risk from subsistence foods from the Aleutians. Science of the Total Environment, 384, 93–105.

    CAS  Article  Google Scholar 

  • Burger, J., Gochfeld, M., Pletnikoff, K., Snigaroff, R., Snigaroff, D., & Stamm, T. (2008). Ecocultural attributes: evaluating, ecological degradation in terms of ecological goods and services versus subsistence and tribal values. Risk Analysis, 28, 1261–1271.

    Article  Google Scholar 

  • Burger, J., Niles, L., Porter, R., Dey, A., Koch, S., & Gordon, C. (2012). Migration and overwintering of Red Knots (Calidris canutus rufa) along the Atlantic coast of the United States. Condor, 114, 302–313.

    Article  Google Scholar 

  • Burger, J., Gochfeld, M., Powers, C. W., Niles, L., Zappalorti, R., Feinberg, F., & Clarke, J. (2013a). Habitat protection for sensitive species: balancing species requirements and human constraints using bioindicators as examples. Natural Science, 5, 50–62.

    Article  Google Scholar 

  • Burger, J., Gochfeld, M., Powers, C. W., Clarke, J. H., Brown, K., Kosson, D., Niles, L., Dey, A., Jeitner, C., & Pittfield, T. (2013b). Determining environmental impacts for sensitive species: using iconic species as bioindicators for management and policy. Journal of Environmental Protection, 4, 87–95.

    Article  Google Scholar 

  • Butler, V. L., & O’Connor, J. E. (2004). 9000 years of salmon fishing on the Columbia River, North America. Quaternary Research, 62, 1–8.

    Article  Google Scholar 

  • Cairns J Jr. (Ed). (1980). The recovery process in damaged ecosystems. Ann arbor, Michigan:Ann Arbor Service.

  • 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 

  • Chelan County Public Utility (Chelan). (2012). Mid-Columbia Salmon Species. http://www.chelanpud.org/mid-columbia-salmon-species.html. Accessed 4 Oct 2013.

  • Cole, D. C., Eyles, J., & Gibson, B. L. (1998). Indicators of human health in ecosystems: what do we measure? Science of the Total Environment, 224, 201–213.

    CAS  Article  Google Scholar 

  • Collis, K., Roby, D. D., Craig, D. P., Ryan, B. A., & Ledgerwood, R. D. (2001). Colonial waterbird predation on juvenile salmonids tagged with passive integrated transponders in the Columbia River estuary: vulnerability of different salmonid species, stocks, and rearing types. Canadian Journal of Fisheries and Aquatic Sciences, 5, 1831–1841.

    Google Scholar 

  • Columbia River Inter-Tribal Fish Commission (CRITFC). (2013). We are all Salmon People, CRITFC. http://critfc.org/salmon-culture/columbia-river-salmon/columbia-river-salmon-species. Accessed 17 Nov 2013.

  • Connor, W. P., Sneva, J. G., Tiffan, K. E., Steinhorst, R. K., & Ross, D. (2005). Two alternative juvenile life history types for fall Chinook Salmon in the Snake River Basin. Transactions of the American Fisheries Society, 134, 291–305.

    Article  Google Scholar 

  • Costanza, R. (1993). Developing ecological research that is relevant to achieving sustainability. Ecological Applications, 3, 579–581.

    Google Scholar 

  • Dauble, D. D., & Geist, D. R. (2000). Comparison of mainstem spawning habitats for two populations of fall Chinook Salmon in the Columbia River Basin. Regulated Rivers: Research & Management, 16, 345–361.

    Article  Google Scholar 

  • Dauble, D. D., & Watson, D. G. (1997). Status of fall Chinook Salmon populations in the mid-Columbia River, 1948-1992. North American Journal of Fisheries Management, 17, 283–300.

    Article  Google Scholar 

  • Dauble, D.D., Poston, T.M., Patton, G.W., & Peterson, R.E. (2003a). Evaluation of the effects of chromium on fall Chinook Salmon in the Hanford Reach of the Columbia River: integration of recent toxicity test results. Pacific Northwest National Laboratory, U.S. Department of Energy .DE-AC06-76RL0183. 62 pp.

  • Dauble, D. D., Hanrahan, T. P., Geist, D. R., & Parsley, M. J. (2003b). Impacts of the Columbia River hydroelectric system on main-stem habitats of fall Chinook Salmon. North American Journal of Fisheries Management, 23, 641–659.

    Article  Google Scholar 

  • DiGuilio, R. T., & Monosson, E. (Eds.). (1996). Interconnections between human and ecological health. London: Chapman and Hall.

    Google Scholar 

  • Donley, E. E., Naiman, R. J., & Marineau, M. D. (2012). Strategic planning for instream flow restoration: a case study of potential climate change impacts in the central Columbia River basin. Global Change Biology, 18(10), 3071–3086.

  • Environmental Protection Agency (EPA). (2000). Evaluation Guidelines for ecological indicators: evaluation criteria. Environmental Protection Agency, Washington, D.C. http://www.epa.gov/emap/html/pubs/docs/resdocs/ecol_ind.pdf. Accessed 22 July 2009.

  • Environmental Protection Agency (EPA). (2008). Biological indicators of watershed health. EPA, Washington DC. http://www.epa.gov/bioiweb1/html/wqscore.html. Accessed 22 July 2009.

  • Environmental Protection Agency (EPA). 2009. Columbia River Basin: State of the River Report for Toxics. EPA 910-R-08-004.EPA, Region 4. http://www.nptwaterresources.org/Docs%20and%20Reports/Water%20Quality/Columbia_R_Basin_State_of_the_River_Report.pdf. Accessed 22 July 2009

  • Farag, A. M., Harper, D. D., Cleveland, L., Brumbaugh, W. G., & Little, E. E. (2006a). The potential for chromium to affect the fertilization process of Chinook Salmon (Oncorhynchus tshawytscha) in the Hanford Reach of the Columbia River, Washington, USA. Archives of Environmental Contamination and Toxicology, 50, 575–579.

    CAS  Article  Google Scholar 

  • Farag, A. M., May, T., Marty, G. D., Easton, M., Harper, D. D., Little, E. E., & Cleveland, L. (2006b). The effect of chronic chromium exposure on the health of Chinook Salmon (Oncorhynchus tshawytscha). Aquatic Toxicology, 76, 246–257.

    CAS  Article  Google Scholar 

  • Fox, G. (Ed.). (1994). Bioindicators as a measure of success for virtual elimination of persistence toxic substances. Hull, Quebec, Canada: International Joint Comm.

    Google Scholar 

  • Fox, G. A. (2001). Wildlife as sentinels of human health effects in the Great Lakes-St. Lawrence Basin. Environmental Health Perspectives, 109, 853–861.

    Google Scholar 

  • Fraser, J. D., Karpanty, S. M., & Cohen, J. B. (2010). Shorebirds forage disproportionately in horseshoe crab nest depressions. Waterbirds, 33, 96–100.

    Article  Google Scholar 

  • Fulton, L.A. (1968). Spawning areas and abundance of Chinook Salmon (Oncorhynchus tshawytscha) in the Columbia River Basin—past and present. US Fish and Wildlife Service, Special Scientific Report, Fisheries No. 571, Washington, D.C.

  • Galbraith, H., Jones, R., Park, R., Clough, J., Herod-Julius, S., Harrington, B., & Page, G. (2002). Global climate change and sea level rise: potential losses of intertidal habitat for shorebirds. Colonial Waterbirds, 25, 173–183.

    Article  Google Scholar 

  • Glbraith, H., DesRochers, D. W., Brown, S., & Reed, J. M. (2014). Predicting vulnerabilities of North American shorebirds to climate change. PloS One, 9(9), e108899.

    Article  Google Scholar 

  • Good, T., McClure, M. M., Sandford, B. P., Barnas, K. A., Marsh, D. M., Ryan, B. A., & Casillas, E. (2007). Quantifying the effect of the Caspian tern predation on threatened and endangered Pacific salmon in the Columbia River estuary. Endangered Species Research, 3, 11–21.

    Article  Google Scholar 

  • Goss-Custard, J. D., Stillman, R. A., West, A. D., McGrorty, S., Durell, S. E. A. E. V. D., & Caldow, R. W. G. (2000). The role of behavioural models in predicting the ecological impact of harvesting. In L. M. Gosling & W. J. Sutherland (Eds.), Behaviour and conservation (pp. 65–82). Cambridge: Cambridge University Press.

    Google Scholar 

  • Goss-Custard, J. D., Triplet, P., Sueur, R., & West, A. D. (2006). Critical thresholds of disturbance by people and raptors in foraging wading birds. Biological Conservation, 127, 88–97.

    Article  Google Scholar 

  • Groot, C., & Margolis, L. (Eds.). (1991). Pacific Salmon: life history. Vancouver BC: University British Columbia Press.

    Google Scholar 

  • Hamrick, K., & Smith, J. (2003). Subsistence food use in Unalaska and Nikolski. Anchorage, AK: Aleutian/Pribilof Island Association.

    Google Scholar 

  • Hanrahan, T. P., Dauble, D. D., & Geist, D. R. (2004). An estimate of Chinook Salmon (Oncorhynchus tshawytscha) spawning habitat and red capacity upstream of a migration barrier in the upper Columbia River. Canadian Journal of Fisheries and Aquatic Science, 61(1), 23–33.

  • Hardell, S., Tilander,H., Smith, G.W., Burger, J., & Carpenter D.O. (2010). Levels of polychlorinated biphenyls (PCBs) and three organochlorine pesticides in fish from the Aleutian Islands of Alaska. PloS One 5, 1–11.

  • Harwell, M. A., & Kelly, J. R. (1990). Indicators of ecosystem recovery. Environmental Management, 14, 527–545.

    Article  Google Scholar 

  • Hatten, J. R., Tiffan, K. F., Anglin, D. R., Haeseker, S. L., Skalicky, J. J., & Schaller, H. (2009). A spatial model to assess the effects of hydropower operations on Columbia River fall Chinook Salmon spawning habitat. North American Journal of Fisheries Management, 29, 1379–1405.

    Article  Google Scholar 

  • Hengstler, J. G., Vander Burg, B., Steinberg, P., & Oesch, F. (1999). Interspecific differences in cancer susceptibility and toxicity. Drug and Metabolic Reviews, 31, 917–970.

    CAS  Article  Google Scholar 

  • Hess, M. A., Rabe, G. D., Vogel, J. L., Stephenson, J. J., Nelson, D. D., & Narum, S. R. (2012). Supportive breeding boosts natural population abundance with minimal negative impacts on fitness of a wild population of Chinook Salmon. Molecular Ecology, 21, 5236–5250.

    Article  Google Scholar 

  • Holsman, K. K., Scheuereil, M. D., Buhle, E., & Emmett, R. (2012). Interacting effects of translocation, artificial propagation, and environmental condition on the marine survival of Chinook Salmon from the Columbia River, Washington, USA. Conservation Biology, 26, 912–922.

    Article  Google Scholar 

  • Honea, J. M., Jorgensen, J. C., McCLURE, M. M., Cooney, T. D., Engie, K., Holzer, D. M., & Hilborn, R. (2009). Evaluating habitat effects on population status: influence of habitat restoration on spring run Chinook salmon. Freshwater Biology, 54(7), 1576–1592.

  • Hyun, S.-Y., Keefer, M. W., Fryer, J. D., Jepson, M. A., Sharma, R., Caudill, C. C., Whiteaker, J. M., & Naughton, G. P. (2012a). Population-specific escapement of Columbia River fall Chinook Salmon: tradeoffs among estimation techniques. Fisheries Research, 129–130, 82–93.

    Article  Google Scholar 

  • Hyun, S.-Y., Sharma, R., Carlile, J. K., Norris, J. G., Brown, G., Briscoe, R. J., & Dobson, D. (2012b). Integrated forecasts of fall Chinook Salmon returns to the Pacific northwest. Fisheries Research, 125–126, 306–317.

    Article  Google Scholar 

  • Johnson, J., Johnson, T., & Copeland, T. (2012). Defining life histories of precocious male parr, minijack, and jack Chinook Salmon using scale patterns. Transactions of the American Fisheries Society, 141, 1545–1556.

    Article  Google Scholar 

  • Kopf, P. G., & Walker, M. K. (2009). Overview of developmental heart defects by dioxins, PCBs, and pesticides. Journal of Environmental Science and Health, 27, 276–285.

    CAS  Article  Google Scholar 

  • Kostow, K. (2012). Strategies for reducing the ecological risks of hatchery programs: case studies from the Pacific Northwest. Environmental Biology of Fishes, 94, 285–310.

    Article  Google Scholar 

  • Landeen, D., & Pinkham, A. (1999). Salmon and his people. Lewiston, Idaho: Confluence.

    Google Scholar 

  • Levin, P. S., & Tolimieri, N. (2001). Differences in the impacts of dams on the dynamics of salmon populations. Animal Conservation, 4, 291–299.

    Article  Google Scholar 

  • Linthurst, R. A., Bourdeau, P., & Tardiff, R. G. (1995). Methods to assess the effects of chemicals on ecosystems. Chichester, UK: Wiley.

    Google Scholar 

  • Maxted, A. M., Luttrell, M. P., Goekjian, V. H., Brown, J. D., Niles, L. J., Dey, A. D., Kalasz, K. S., Swayne, D. E., & Stallknecht, D. E. (2012). Avian influenza virus infection dynamics in shorebird hosts. Journal of Wildlife Diseases, 48, 322–335.

    Article  Google Scholar 

  • Mendelsohn, M. L., Mohr, L. C., & Peeters, J. P. (1998). Biomarkers: medical and workplace applications. Wash. DC: Joseph Henry Press.

    Google Scholar 

  • Morrison, R. I. G., McCaffery, B. J., Gil, R. E., Skagen, S. K., Jones, S. L., Page, G. W., Gratto-Trevor, C. L., & Andres, B. A. (2006). Population estimates of North American shorebirds. Wader Study Group Bulletin, 111, 67–85.

    Google Scholar 

  • Morrison, R. I. G., Davidson, N. C., & Wilson, J. R. (2007). Survival of the fattest: body stores on migration and survival in Red Knots, Calidris canutus islandica. Journal of Avian Biology, 38, 479–487.

    Article  Google Scholar 

  • Mueller, R. P. & Ward, D. L. (2010). Characterization of fall Chinook salmon spawning areas downstream. Final Report. PNWD-56286. Prepared for the Public Utility District No. 2 of Grant County, Ephrata, WA. 61 pp.

  • Mueller, R. M., Vernon, C. R., & Langshaw R. B. (2012). Evaluation of Fallback and Reascension of Fall ChinookSalmon as They Relate to Escapement to the Hanford Reach. PNWD-4264. Prepared for the Public Utility DistrictNo. 2 of Grant County, Ephrata, WA.31 pp.

  • Narum, S. R., Hess, J. E., & Metala, A. P. (2010). Examining genetic lineages of Chinook Salmon in the Colombia River Basin. Transactions of the American Fisheries Society, 139, 1465–1477.

    Article  Google Scholar 

  • National Research Council (NRC). (1991). Animals as sentinels of environmental health hazards. Washington, D.C.: National Academy Press.

    Google Scholar 

  • National Research Council (NRC). (1996). Upstream: salmon and society in the Pacific Northwest. Washington, DC: National Research Council.

    Google Scholar 

  • Niles, L. J., Sitters, H. P., Dey, A. D., Atkinson, P. W., Baker, A. J., Bennett, K. A., Carmona, R., Clark, K. E., Clark, N. A., Espoz, C., González, P. M., Harrington, B. A., Hernández, D. E., Kalasz, K. S., Lathrop, R. G., Matus, R. N., Minton, C. D. T., Morrison, R. I. G., Peck, M. K., Pitts, W., Robinson, R. A., & Serrano, I. L. (2008). Status of the Red Knot, Calidris canutus rufa, in the Western Hemisphere. Studies of Avian Biology, 36, 1–185.

    Google Scholar 

  • Niles, L. J., Bart, J., Sitters, H. P., Dey, A. D., Clark, D. E., & Atkinson, P. W. (2009). Effects of horseshoe crab harvest in Delaware Bay on Red Knots: are harvest restrictions working? BioScience, 59, 153–164.

    Article  Google Scholar 

  • Niles, L., Burger, J., Porter, R., Dey, A., Minton, C., Gonzalez, P., Baker, A., Fox, J., & Gordon, C. (2010). First results using light level geolocators to track Red Knots in the Western Hemisphere show rapid anf long intercontinental flights and new details of migration pathways. Wader Study Group Bulletin, 117, 1–8.

    Google Scholar 

  • Oregon Hanford Waste Board (OHWB). (2002). River without waste: recommendations for protecting the Columbia River from Hanford Site nuclear waste. USDOE, Hanford.

  • Piersma, T., Wiersma, P., & Van Gills, J. (1997). The many unknowns about plovers and sandpipers of the world: introduction to a wealth of research opportunities highly relevant for shorebird conservation. Wader Study Group Bulletin, 82, 23–33.

    Google Scholar 

  • Regetz, J. (2003). Landscale-level constraints on recruitment of Chinook Salmon (Oncorhynchus tshawytscha) in the Columbia River, USA. Aquatic Conservation: Marine and Freshwater Ecosystems, 13, 35–49.

    Article  Google Scholar 

  • Risebrough, R. W. (1991). Indicator species, birds, toxic contaminants, and global change. Acta 20th Congressional and International Ornithology, 20, 2480–2486.

    Google Scholar 

  • Schreck, C. B., Stahl, T. P., Davis, L. E., Roby, D. D., & Clemens, B. J. (2006). Mortality estimates of juvenile spring-summer Chinook Salmon in the lower Columbia River and estuary, 1992-1998: evidence of delayed mortality. Transactions of the American Fisheries Society, 135, 457–475.

    Article  Google Scholar 

  • Sharma, R., & Quinn, T. P. (2012). Linkages between the life history type and migration pathways in freshwater and marine environments for Chinook Salmon, Oncorhynchus tshawytscha. Acta Oecologica, 41, 1–13.

    Article  Google Scholar 

  • United States Fish & Wildlife Service (USFWS). 2012. Species Profile: Chinook Salmon. http://ecos.fws.gov/speciesProfile/profile/speciesProfile.action?spcode=E06D. Accessed 17 Jan 2013.

  • Williams, R. N. (Ed.). (2006). Return to the river: restoring salmon to the Columbia River. New York, NY: Elsevier.

    Google Scholar 

  • Williams, R. N., Bisson, P. A., Botton, D. L., Calvin, L. D., Coutant, C. C., Erho, M. W., Jr., Frissell, C. A., Lichatowich, J. A., Liss, W. J., McConnaha, W. E., Mundy, P. R., Stanford, J. A., & Whitney, R. R. (1999). Return to the River: scientific issues in the restoration of salmonid fishes in the Columbia River. Fisheries, 24, 10–19.

    Article  Google Scholar 

Download references

Acknowledgments

We thank the many people who we have discussed these topics with us or who have helped in the research, including L. Bliss, A. Bunn, E. DeVito, C. Duncan, C. Frank, M. Gilbertson, C. Jeitner, D. Jenkins, C. Minton, T. Pittfield, H. Sitters, and other field volunteers, as well as regulators and other governmental officials, tribal members associated with Hanford, and especially the Aleut people in Alaska who greatly influenced our views. We thank the many organizations and individuals who contributed throughout this research. This project was mainly funded by the Consortium for Risk Evaluation with Stakeholder Participation (Department of Energy, DE-FC01-86EW07053), with additional funding from NIEHS (P30ES005022), US Fish and Wildlife Foundation, NJ Department of Environmental Protection (Endangered and Nongame Program), Conserve Wildlife Foundation of New Jersey, Endangered and Nongame Species Program of the NJ Department of Environmental Protection, and Rutgers University. The views and opinions expressed in this paper are those of the authors and do not represent the funding agencies.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joanna Burger.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Burger, J., Gochfeld, M., Niles, L. et al. Complexity of bioindicator selection for ecological, human, and cultural health: Chinook salmon and red knot as case studies. Environ Monit Assess 187, 102 (2015). https://doi.org/10.1007/s10661-014-4233-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-014-4233-4

Keywords

  • Indicators
  • Human health
  • Ecological health
  • Endpoints
  • Cultural health
  • Subsistence