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

  • Joanna BurgerEmail author
  • Michael Gochfeld
  • Lawrence Niles
  • Charles Powers
  • Kevin Brown
  • James Clarke
  • Amanda Dey
  • David Kosson
Article

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.

Keywords

Indicators Human health Ecological health Endpoints Cultural health Subsistence 

Notes

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.

References

  1. Atlantic States Marine Fisheries Commission (ASMFC) (2001). Carl N. Shuster Jr. Horseshoe crab reserve designated. Fisheries Focus. 10(2):8–9.Google Scholar
  2. 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.Google Scholar
  3. Bartell, S. M. (2006). Biomarkers, bioindicators, and ecological risk assessment—a brief review and evaluation. Environmental Bioindicators, 1, 39–50.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. Burger, J. (2006a). Bioindicators: types, development, and use in ecological assessment and research. Environmental Bioindicators, 1, 22–39.CrossRefGoogle Scholar
  9. Burger, J. (2006b). Bioindicators: a review of their use in the environmental literature 1970-2005. Bioindicators, 1, 136–144.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. Burger, J. (2009). Stakeholder involvement in indicator selection: case studies and levels of participation. Environmental Bioindicators, 4, 170–190.CrossRefGoogle Scholar
  12. Burger, J., & Gochfeld, M. (2001). On developing bioindicators for human and ecological health. Environmental Monitoring and Assessment, 66, 23–46.CrossRefGoogle Scholar
  13. 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
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. Butler, V. L., & O’Connor, J. E. (2004). 9000 years of salmon fishing on the Columbia River, North America. Quaternary Research, 62, 1–8.CrossRefGoogle Scholar
  25. Cairns J Jr. (Ed). (1980). The recovery process in damaged ecosystems. Ann arbor, Michigan:Ann Arbor Service.Google Scholar
  26. Carignan, V., & Villard, M. A. (2001). Selecting indicator species to monitor ecological integrity: a review. Environmental Monitoring and Assessment, 78, 45–61.CrossRefGoogle Scholar
  27. Chelan County Public Utility (Chelan). (2012). Mid-Columbia Salmon Species. http://www.chelanpud.org/mid-columbia-salmon-species.html. Accessed 4 Oct 2013.
  28. 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.CrossRefGoogle Scholar
  29. 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
  30. 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.
  31. 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.CrossRefGoogle Scholar
  32. Costanza, R. (1993). Developing ecological research that is relevant to achieving sustainability. Ecological Applications, 3, 579–581.Google Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.Google Scholar
  36. 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.CrossRefGoogle Scholar
  37. DiGuilio, R. T., & Monosson, E. (Eds.). (1996). Interconnections between human and ecological health. London: Chapman and Hall.Google Scholar
  38. 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.Google Scholar
  39. 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.
  40. 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.
  41. 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
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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
  45. 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
  46. Fraser, J. D., Karpanty, S. M., & Cohen, J. B. (2010). Shorebirds forage disproportionately in horseshoe crab nest depressions. Waterbirds, 33, 96–100.CrossRefGoogle Scholar
  47. 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.Google Scholar
  48. 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.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. 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
  52. 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.CrossRefGoogle Scholar
  53. Groot, C., & Margolis, L. (Eds.). (1991). Pacific Salmon: life history. Vancouver BC: University British Columbia Press.Google Scholar
  54. Hamrick, K., & Smith, J. (2003). Subsistence food use in Unalaska and Nikolski. Anchorage, AK: Aleutian/Pribilof Island Association.Google Scholar
  55. 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.Google Scholar
  56. 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.Google Scholar
  57. Harwell, M. A., & Kelly, J. R. (1990). Indicators of ecosystem recovery. Environmental Management, 14, 527–545.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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.CrossRefGoogle Scholar
  60. 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.CrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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.Google Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. 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.CrossRefGoogle Scholar
  66. 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.CrossRefGoogle Scholar
  67. 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.CrossRefGoogle Scholar
  68. Landeen, D., & Pinkham, A. (1999). Salmon and his people. Lewiston, Idaho: Confluence.Google Scholar
  69. Levin, P. S., & Tolimieri, N. (2001). Differences in the impacts of dams on the dynamics of salmon populations. Animal Conservation, 4, 291–299.CrossRefGoogle Scholar
  70. Linthurst, R. A., Bourdeau, P., & Tardiff, R. G. (1995). Methods to assess the effects of chemicals on ecosystems. Chichester, UK: Wiley.Google Scholar
  71. 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.CrossRefGoogle Scholar
  72. Mendelsohn, M. L., Mohr, L. C., & Peeters, J. P. (1998). Biomarkers: medical and workplace applications. Wash. DC: Joseph Henry Press.Google Scholar
  73. 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
  74. 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.CrossRefGoogle Scholar
  75. 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.Google Scholar
  76. 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.Google Scholar
  77. 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.CrossRefGoogle Scholar
  78. National Research Council (NRC). (1991). Animals as sentinels of environmental health hazards. Washington, D.C.: National Academy Press.Google Scholar
  79. National Research Council (NRC). (1996). Upstream: salmon and society in the Pacific Northwest. Washington, DC: National Research Council.Google Scholar
  80. 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
  81. 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.CrossRefGoogle Scholar
  82. 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
  83. Oregon Hanford Waste Board (OHWB). (2002). River without waste: recommendations for protecting the Columbia River from Hanford Site nuclear waste. USDOE, Hanford.Google Scholar
  84. 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
  85. 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.CrossRefGoogle Scholar
  86. Risebrough, R. W. (1991). Indicator species, birds, toxic contaminants, and global change. Acta 20th Congressional and International Ornithology, 20, 2480–2486.Google Scholar
  87. 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.CrossRefGoogle Scholar
  88. 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.CrossRefGoogle Scholar
  89. 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.
  90. Williams, R. N. (Ed.). (2006). Return to the river: restoring salmon to the Columbia River. New York, NY: Elsevier.Google Scholar
  91. 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.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Joanna Burger
    • 1
    • 2
    • 3
    Email author
  • Michael Gochfeld
    • 2
    • 3
    • 4
  • Lawrence Niles
    • 5
  • Charles Powers
    • 3
    • 6
  • Kevin Brown
    • 3
    • 6
  • James Clarke
    • 3
    • 6
  • Amanda Dey
    • 7
  • David Kosson
    • 3
    • 6
  1. 1.Division of Life SciencesRutgers UniversityPiscatawayUSA
  2. 2.Environmental and Occupational Health Sciences, Robert Wood Johnson Medical SchoolRutgers UniversityPiscatawayUSA
  3. 3.Consortium for Risk Evaluation with Stakeholder ParticipationVanderbilt UniversityNashvilleUSA
  4. 4.Environmental and Occupational MedicineRutgers UniversityPiscatawayUSA
  5. 5.Conserve WildlifeGreenwichUSA
  6. 6.Department of Civil and Environmental Engineering and CRESPVanderbilt UniversityNashvilleUSA
  7. 7.NJ Department of Environmental ProtectionEndangered and Nongame Species Program TrentonNew JerseyUSA

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