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Tissue toxicants and prespawn mortality in Willamette River Chinook salmon

Abstract

In some Pacific salmon Oncorhynchus spp. populations, many adults die after reaching freshwater spawning sites but prior to spawning, a phenomenon known as prespawn mortality (PSM). Causal factors for PSM are often uncertain, but pathogens, warm water temperature, and environmental toxicants have been implicated in several studies. In this two-year project, we examined the relationship between toxicants and PSM in a threatened population of spring-run Chinook salmon O. tshawytscha (Walbaum) in the Willamette River, Oregon. Muscle and skin samples from 63 female carcasses were screened for ~125 potential toxicants, including trace elements, pesticides, and organohalogens. Mean concentrations for five toxicants selected for their known adverse effects on salmonids were: 4.3 (SD = 2.0) ng/g cadmium, 72.9 (122.7) ng/g nickel, 10.0 (9.0) ng/g lead, 12.7 (8.6) ng/g polychlorinated biphenyls (PCBs), and 17.6 (10.3) ng/g DDT (an organochlorine pesticide). Using generalized linear models, we found no statistical differences in toxicants concentrations between successful (n = 37, 58.7%) and unsuccessful (n = 26, 41.3%) female spawners. We conclude that selected contaminants did not provoke acute toxicity in Willamette River Chinook salmon. It remains unknown whether sub-lethal or chronic toxicant effects on adult salmon physiology or behavior have affected the fitness of this threatened population.

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References

  1. Alvarez D, Perkins S, Nilsen E, Morace J (2014) Spatial and temporal trends in occurrence of emerging and legacy contaminants in the lower Columbia River 2008–2010. Sci Total Environ 484:322–330

  2. Ankley GT et al (2009) Endocrine disrupting chemicals in fish: developing exposure indicators and predictive models of effects based on mechanism of action. Aquat Toxicol 92:168–178

  3. Arkoosh MR et al (1998) Effects of pollution on fish diseases: potential impacts on salmonid populations. J Aquat Anim Health 10:182–190

  4. Baker JP et al (2004) Alternative futures for the Willamette River basin, Oregon. Ecol Appl 14(2):313–324

  5. Baldwin DH, Spromberg JA, Collier TK, Scholz NL (2009) A fish of many scales: extrapolating sublethal pesticide exposures to the productivity of wild salmon populations. Ecol Appl 19(8):2004–2015

  6. Baldwin DH, Tatara CP, Scholz NL (2011) Copper-induced olfactory toxicity in salmon and steelhead: extrapolation across species and rearing environments. Aquat Toxicol 101:295–297

  7. Benda SE, Naughton GP, Caudill CC, Kent ML, Schreck CB (2015) Cool, pathogen-free refuge lowers pathogen-associated prespawn mortality of Willamette River Chinook salmon. Trans Am Fish Soc 144:1159–1172

  8. Bosch AC, O'Neill B, Sigge GO, Kerwath SE, Hoffman LC (2016) Heavy metals in marine fish meat and consumer health: a review. Sci Food Agric 96:32–48

  9. Bowerman T, Keefer ML, Caudill CC (2016) Pacific salmon prespawn mortality: patterns, methods, and study design considerations. Fisheries 41(12):738–749

  10. Bowerman T, Roumasset A, Keefer ML, Sharpe CS, Caudill CC (2018) Prespawn mortality of female Chinook Salmon increases with water temperature and percent hatchery origin. Trans Am Fish Soc 147:31–42

  11. Chapman GA (1978) Toxicities of cadmium, copper, and zinc to four juvenile stages of Chinook salmon and steelhead. Trans Am Fish Soc 107:841–847

  12. Chow MI et al (2019) An urban stormwater runoff mortality syndrome in juvenile coho salmon. Aquat Toxicol 214:105231

  13. Cullon DL et al (2009) Persistent organic pollutants in Chinook salmon (Oncorhynchus tshawytscha): implications for resident killer whales of British Columbia and adjacent waters. Environ Toxicol Chem 28(1):148–161

  14. deBruyn AMH, Ikonomou MG, Gobas FAPC (2004) Magnification and toxicity of PCBs, PCDDs, and PCDFs in upriver-migrating Pacific salmon. Environ Sci Technol 38:6217–6224

  15. DeWeber JT, Peterson JT, Sharpe C, Kent ML, Colvin ME, Schreck CB (2017) A hidden-process model for estimating prespawn mortality using carcass survey data. N Am J Fish Manag 37:162–175

  16. Evans DH (1987) The fish gill: site of action and model for toxic effects of environmental pollutants. Environ Health Perspect 71:47–58

  17. Feist BE et al (2017) Roads to ruin: conservation threats to a sentinel species across an urban gradient. Ecol Appl 27(8):2382–2396

  18. Greenfield BK et al (2008) Contaminant concentrations and histopathological effects in Sacramento splittail (Pogonichthys macrolepidotus). Arch Environ Contam Toxicol 55(2):270–281

  19. Hamilton PB, Rolshausen G, Webster TMU, Tyler CR (2017) Adaptive capabilities and fitness consequences associated with pollution exposure in fish. Philos Trans R Soc Lond B Biol Sci 372(1712):20160042

  20. Hinch SG, Cooke SJ, Farrell AP, Miller KM, Lapointe M, Patterson DA (2012) Dead fish swimming: a review of research on the early migration and high premature mortality in adult Fraser River sockeye salmon Oncorhynchus nerka. J Fish Biol 81:576–599

  21. Huff ES, Klingeman PC (1976) Restoring the Willamette River: costs and impacts of water quality control. Water Pollut Control Fed 48(10):2410–2415

  22. Hwang H-M, Green PG, Young TM (2006) Tidal salt marsh sediment in California, USA. Part 1: occurrence and sources of organic contaminants. Chemosphere 64:1383–1392

  23. Hwang HM, Green PG, Holmes RW (2009a) Anthropogenic impacts on the quality of streambed sediments in the lower Sacramento River watershed, California. J Environ Sci Health A 44(1):1–11

  24. Hwang HM, Green PG, Young TM (2009b) Historical trends of trace metals in a sediment core from a contaminated tidal salt marsh in San Francisco Bay. Environ Geochem Health 31(4):421–430

  25. Islam MS, Tanaka M (2004) Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Mar Pollut Bull 48:624–649

  26. Johnson L et al (2013) Persistent organic pollutants in juvenile Chinook Salmon in the Columbia River basin: implications for stock recovery. Trans Am Fish Soc 142:21–40

  27. Jonsson B, Jonsson N (2009) A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow. J Fish Biol 75:2381–2447

  28. Keefer ML, Caudill CC (2014) Homing and straying by anadromous salmonids: a review of mechanisms and rates. Rev Fish Biol Fisheries 24:333–368. https://doi.org/10.1007/s11160-013-9334-6

  29. Keefer ML, Taylor GA, Garletts DF, Gauthier GA, Pierce TM, Caudill CC (2010) Prespawn mortality in adult spring Chinook salmon outplanted above barrier dams. Ecol Freshw Fish 19:361–372

  30. Kelly BC, Ikonomou MG, MacPherson N, Sampson T, Patterson DA, Dubetz C (2011) Tissue residue concentrations of organohalogens and trace elements in adult Pacific salmon returning to the Fraser River, British Columbia, Canada. Environ Toxicol Chem 30(2):367–376

  31. Kent ML, Benda S, St-Hilaire S, Schreck CB (2013) Sensitivity and specificity of histology for diagnoses of four common pathogens and detection of nontarget pathogens in adult Chinook salmon (Oncorhynchus tshawytscha) in fresh water. J Vet Diagn Invest 25:341–351

  32. King-Heiden TC et al (2012) Reproductive and developmental toxicity of dioxin in fish. Mol Cell Endocrinol 354(1–2):121–138

  33. Krümmel EM et al (2003) Delivery of pollutants by spawning salmon. Nature 425:255

  34. Lundin JI et al (2018) Legacy habitat contamination as a limiting factor for Chinook salmon recovery in the Willamette Basin, Oregon, USA. PLoS One 14(3):e0214399

  35. Mallatt J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42(4):630–648

  36. McGourty CR et al (2009) Likely population-level effects of contaminants on a resident estuarine fish species: comparing Gillichthys mirabilis population static measurements and vital rates in San Francisco and Tomales bays. Estuar Coast 32(6):1148–1154

  37. McIntyre JK, Baldwin DH, Beauchamp DA, Scholz NL (2012) Low-level copper exposures increase visibility and vulnerability of juvenile coho salmon to cutthroat trout predators. Ecol Appl 22:1460–1471

  38. McIntyre JK et al (2018) Interspecies variation in the susceptibility of adult Pacific salmon to toxic urban stormwater runoff. Environ Pollut 238:196–203

  39. McKim JM (1977) Evaluation of tests with early life stages of fish for predicting long-term toxicity. J Fish Res Board Can 34(8):1148–1154

  40. Meador JP, Collier TK, Stein JE (2002) Use of tissue and sediment-based threshold concentrations of polychlorinated biphenyls (PCBs) to protect juvenile salmonids listed under the US Endangered Species Act. Aquat Conserv Mar Freshwat Ecosyst 12:493–516

  41. Montory M, Habit E, Fernandez P, Grimalt JO, Barra R (2010) PCBs and PBDEs in wild Chinook salmon (Oncorhynchus tshawytscha) in the northern Patagonia, Chile. Chemosphere 78:1193–1199

  42. Musick JA et al (2000) Marine, estuarine, and diadromous fish stocks at risk of extinction in North America (exclusive of Pacific salmonids). Fisheries 25(11):6–30

  43. Naughton GP, Keefer ML, Clabough TS, Knoff MJ, Blubaugh TJ, Caudill CC (2018a) Tag effects on prespawn mortality of Chinook Salmon: a field experiment using PIT tags, radio transmitters, and untagged controls. N Am J Fish Manag 38:96–103

  44. Naughton GP et al (2018b) Reservoir provides cool-water refuge for adult Chinook salmon in a trap-and-haul reintroduction program. Mar Freshw Res 69(12):1995–2007

  45. Nehlsen W, Williams JE, Lichatowich JA (1991) Pacific salmon at the crossroads: stocks at risk from California, Oregon, Idaho and Washington. Fisheries 16(2):4–21

  46. Nilsen E et al (2014) Contaminants of legacy and emerging concern in largescale suckers (Catostomus macrocheilus) and the foodweb in the lower Columbia River, Oregon and Washington, USA. Sci Total Environ 484:344–352

  47. NMFS (National Marine Fisheries Service) (1999) Endangered and threatened species: threatened status for three Chinook salmon evolutionarily significant units (ESUs) in Washington and Oregon, and endangered status for one Chinook salmon ESU in Washington. Fed Regist 64(56):14308–14328

  48. NMFS (National Marine Fisheries Service) (2008). Endangered Species Act section 9(a)(2) consultation biological opinion and Magnuson–Stevens Fishery Conservation and Management Act essential fish habitat consultation: consultation on the “Willamette RIVER BASIN FLOOD CONTROL Probject”. National Oceanic and Atmospheric Administration, NMFS, northwest region, F/NWR/2000/02177, Seattle

  49. Norli HR, Christiansen A, Deribe E (2011) Application of QuEChERS method for extraction of selected persistent organic pollutants in fish tissue and analysis by gas chromatography mass spectrometry. J Chromatogr A 1128(41):7234–7241

  50. O'Neill SM, West JE (2009) Marine distribution, life history traits, and the accumulation of polychlorinated biphenyls in Chinook Salmon from Puget Sound, Washington. Trans Am Fish Soc 138:616–632

  51. O'Toole S, Metcalfe C, Craine I, Gross M (2006) Release of persistent organic contaminants from carcasses of Lake Ontario Chinook salmon (Oncorhynchus tshawytscha). Environ Pollut 140:102–113

  52. Pane EF, Haque A, Goss GG, Wood CM (2004) The physiological consequences of exposure to chronic, sublethal waterborne nickel in rainbow trout (Oncorhynchus mykiss): exercise vs resting physiology. J Exp Biol 207:1249–1261

  53. Ross PS et al (2013) The trouble with salmon: relating pollutant exposure to toxic effect in species with transformational life histories and lengthy migrations. Can J Fish Aquat Sci 70:1252–1264

  54. Scholz NL et al (2000) Diazinon disrupts antipredator and homing behaviors in chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 57:1911–1918

  55. Scholz NL et al (2011) Recurrent die-offs of adult coho salmon returning to spawn in Puget Sound lowland urban streams. PLoS One 6(12):e28013

  56. Schroeder RK, Whitman LD, Cannon B, Olmsted P (2016) Juvenile life-history diversity and population stabiltiy of spring Chinook salmon in the Willamette River basin, Oregon. Can J Fish Aquat Sci 73:921–934

  57. Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369–392

  58. Shaw SS, Brenner D, Berger ML, Carpenter DO, Hong C-S, Kannan K (2006) PCBs, PCDD/Fs, and organochlorine pesticides in farmed Atlantic salmon from Maine, eastern Canada, and Norway, and wild salmon from Alaska. Environ Sci Technol 40(17):5347–5354

  59. Spromberg JA, Meador JP (2005) Relating results of chronic toxicity responses to population-level effects: modeling effects on wild Chinook salmon populations. Integr Environ Assess 1(1):9–21

  60. Spromberg JA, Scholz NL (2011) Estimating the future decline of wild coho salmon populations resulting from early spawner die-offs in urbanizing watersheds of the Pacific northwest, USA. Integr Environ Assess Manag 7(4):648–656

  61. Spromberg JA et al (2016) Coho salmon spawner mortality in wester US urban watersheds: bioinfiltration prevents lethal storm water impacts. J Appl Ecol 53:398–407

  62. USEPA (U. S. Environmental Protection Agency) (2000). National priorities list for uncontrolled hazardous waste sites, proposed rule No. 33. Federal Register 65:145(27 July 2000):46131–43167

  63. Veldhoen N et al (2010) Gene expression profiling and environmental contaminant assessment of migrating Pacific salmon in the Fraser River watershed of British Columbia. Aquat Toxicol 97(3):212–225

  64. Waite IR, Carpenter KD (2000) Associations among fish assemblage structure and environmental variables in Willamette basin streams, Oregon. Trans Am Fish Soc 129:754–770

  65. Weitkamp LE (2010) Marine distributions of Chinook Salmon from the West coast of North America determined by coded wire tag recoveries. Trans Am Fish Soc 139:147–170

  66. Wold S, Esbensen K, Geladi P (1987) Principal component analysis. Chemometr Intell Lab Syst 2:37–52

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Acknowledgements

Many people assisted with this studyand its successful completion was made possible through their efforts. We would like to thank: Ryan Mann, Charles Erdman, Jeff Garnett, Eric Johnson, Grant Brink, Eric Powell, Dan Joosten, Mike Turner, and Chris Noyes (University of Idaho) for assisting with field work and data collection; Greg Taylor, Doug Garletts, and Chad Helms, from the USACE Lookout Point office for field help and project coordination; Cameron Sharpe, Dan Peck, and Tim Wright, (Oregon Department of Fish and Wildlife). This study was conducted under Cooperative Ecosystems Study Unit (CESU) agreement CESU W912HZ-12-2-0004 funded by the U.S. Army, Corps of Engineers (USACE), Portland District, with the assistance of Robert Wertheimer, Rich Piaskowski, David Griffith, Glen Rhett, and Deberay Carmichael.

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Correspondence to Matthew L. Keefer.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures were in accordance with the ethical standards of the University of Idaho and were approved by The University of Idaho Institutional Animal Care and Use Committee (e.g., Protocol 2012–36).

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Keefer, M.L., Naughton, G.P., Clabough, T.S. et al. Tissue toxicants and prespawn mortality in Willamette River Chinook salmon. Environ Biol Fish 103, 175–183 (2020). https://doi.org/10.1007/s10641-019-00944-w

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Keywords

  • Organohalogens
  • Pesticides
  • Pollutants
  • Prespawn mortality
  • Trace elements
  • Toxic chemicals