Abstract
Appraisal of hatchery-related effects on Pacific salmonids (Oncorhynchus spp.) is a necessary component of species conservation. For example, hatchery supplementation can influence species viability by changing genetic, phenotypic and life-history diversity. We analyzed time series data for seven salmonid taxa from the Klamath River basin, California, to investigate trajectories of wild and hatchery adult populations. Linear regression coupled with randomized permutations (n = 99,999), two- tailed t tests, and Bayesian change point analysis were used to detect trends over time. Cross correlation was also used to evaluate relationships between wild and hatchery populations. The taxa of interest were spring, fall, and late-fall Chinook Salmon (O. tshawytscha); Coho Salmon (O. kisutch); Coastal Cutthroat Trout (O. clarki clarki); and summer and hybrid Steelhead Trout (O. mykiss). Significant decreases were detected for summer and hybrid Steelhead Trout. The proportion of wild fall Chinook has also significantly decreased concurrently with increases in hatchery returns. In comparison, returns of most Chinook and coho runs to the hatcheries, and fall Chinook strays to wild spawning areas from Iron Gate Hatchery have significantly increased since the 1970s. Increases were also detected for wild late-fall Chinook and spring Chinook adults. However, both of these were significantly correlated with Chinook Salmon returns to Trinity River Hatchery, suggesting augmentation by hatchery strays. Changes in abundances appeared related to changing ocean habitat conditions and hatchery practices. Our results suggest that anadromous salmonid populations in the Klamath River basin are becoming increasingly dependent on hatchery propagation, a pattern that can threaten population persistence.
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References
Anderson MJ (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639
Anderson JT, Legendre P (1999) An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. J Stat Comput Simul 62:271–303
Anderson MJ, Robinson J (2001) Permutation tests for linear models. Aust NZ J Stat 43:75–88
Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100–103
Araki H, Berejikian BA, Ford MJ, Blouin MS (2008) Fitness of hatchery-reared salmonids in the wild. Evol Appl 1:342–355
Araki H, Cooper B, Blouin MS (2009) Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild. Biol Lett 5:621–624
Barnett-Johnson R, Grimes CB, Royer CF, Donohoe CJ (2007) Identifying the contribution of wild and hatchery Chinook Salmon (Oncorhynchus tshawytscha) to the ocean fishery using otolith microstructure as natural tags. Can J Fish Aquat Sci 64:1683–1692
Battin J, Wiley MW, Ruckelshaus MH, Palmer RN, Korb E, Bartz KK, Imaki H (2007) Projected impacts of climate change on salmon habitat restoration. PNAS 104:6720–6725
Beamish RJ, Mahnken C (2001) A critical size and period hypothesis to explain natural regulation of salmon abundance and the linkage to climate and climate change. Prog Oceanogr 49:423–437
Berejikian BA, Tezak EP, Schroder SL (2001) Reproductive behavior and breeding success of captively reared Chinook salmon. N Am J Fish Manag 21:255–260
Bisson PA, Coutant CC, Goodman D, Gramling R, Lettenmaier D, Lichatowich J, Liss W, Loudenslager E, McDonald L, Philipp D, Riddell B (2002) Hatchery surpluses in the Pacific Northwest. Fisheries 27:16–27
Box GEP, Jenkins GM, Reinsel GC (2008) Time series analysis - forecasting and control. Wiley and Sons Inc., Hoboken
Brannon EL, Amend DF, Cronin MA, Lannan JE, LaPatra S, McNeil WJ, Noble RE, Smith CE, Talbot AJ, Wedemeyer GA, Westers H (2004) The controversy about salmon hatcheries. Fisheries 29:12–31
Brauner CJ, Iwama GK, Randall DJ (1994) The effect sf short-duration seawater exposure on the swimming performance of wild and hatchery-reared juvenile coho salmon (Oncorhynchus kisutch) during smoltification. Can J Fish Aquat Sci 51:2188–2194
Brown LR, Moyle PB, Yoshiyama RM (1994) Historical decline and current status of coho salmon in California. N Am J Fish Manag 14:237–261
Buhle ER, Holsman KK, Scheuerell MD, Albaugh A (2009) Using an unplanned experiment to evaluate the effects of hatcheries and environmental variation on threatened populations of wild salmon. Biol Conserv 142:2449–2455
Busby PJ, Wainwright TC, Waples RS (1994) Status review for Klamath Mountains Province steelhead. National Marine Fisheries Service, Seattle
Carmona-Catot G, Moyle PB, Simmons RE (2012) Long-term captive breeding does not necessarily prevent reestablishment: lessons learned from Eagle Lake rainbow trout. Rev Fish Biol Fish 22:325–342
CDFG (2002) Status review of California Coho salmon north of San Francisco. California Fish and Game Commission, Sacramento
CDFG (2010) Final hatchery and stocking program Environmental Impact Statement. Fisheries Management Branch, Sacramento
Chittenden CW, Sura S, Butterworth KG, Cubitt KF, Plantalech Manel-la N, Balfry S, Okland F, McKinley RS (2008) Riverine, estuarine and marine migratory behavior and physiology of wild and hatchery-reared coho salmon Oncorhynchus kisutch (Walbaum) smolts descending the Campbell River, BC, Canada. J Fish Biol 72:614–628
Chittenden CM, Biagi CA, Davidsen JG, Davidsen AG, Kondo H, McKnight A, Pedersen O-P, Raven PA, Rikardsen AH, Shrimpton JM, Zuehlke B, McKinley RS, Devlin RH (2010) Genetic versus rearing-environment effects on phenotype: hatchery and natural rearing effects on hatchery- and wild-born coho salmon. PLoS One 5:12261
Chu P, Zhao X (2004) Bayesian change-point analysis of tropical cyclone activity: the Central North Pacific case. J Climate 17:4893–4901
Denison DGT, Mallick BK, Smith AFM (1998) Automatic Bayesian curve fitting. J R Stat Soc Ser B 60:333–350
Dittman AH, May D, Larsen DA, Moser ML, Johnston M, Fast D (2010) Homing and spawning site selection by supplemented hatchery- and natural-origin Yakima River spring Chinook Salmon. Trans Am Fish Soc 139:1014–1028
Ebersole JL, Liss WJ, Frissell CA (2001) Relationship between stream temperature, thermal refugia and rainbow trout Oncorhynchus mykiss abundance in arid-land streams in the northwestern United States. Ecol Freshw Fish 10:1–10
Eldridge W, Killebrew K (2008) Genetic diversity over multiple generations of supplementation: an example from Chinook salmon using microsatellite and demographic data. Conserv Genet 9:13–28
Gresh T, Lichatowich J, Schoonmaker P (2000) An estimation of historic and current levels of salmon production in the northeast Pacific ecosystem: evidence of a nutrient deficit in the freshwater systems of the Pacific Northwest. Fisheries 25:15–21
Gutierrez CM (2006) Declaration concerning the Klamath River fall Chinook salmon fishery. Department of Commerce, Washington D.C
Hamilton J, Rondorf D, Hampton M, Quiñones RM, Simondet J, Smith T (2011) Synthesis of the effects to fish species of two management scenarios for the Secretarial Determination on removal of the lower four dams on the Klamath River. U.S. Fish and Wildlife Service, Yreka
Hard JJ, Gross MR, Heino M, Hilborn R, Kope RG, Law R, Reynolds JD (2008) Evolutionary consequences of fishing and their implications for salmon. Evol Appl 1:388–408
Heard WR (1998) Do hatchery salmon affect the North Pacific Ocean ecosystem? NPAFC Bull 1:405–411
Hilborn R (1992) Hatcheries and the future of salmon in the Northwest. Fisheries 17:5–8
Hill RA, Irvine JR (2001) Standardizing spawner escapement data: a case study of the Nechako River Chinook salmon. N Am J Fish Manag 21:651–655
Hjort RC, Schreck CB (1982) Phenotypic differences among stocks of hatchery and wild coho salmon, Oncorhynchus kisutch, in Oregon, Washington and California. Fish B-NOAA 80:105–119
Kaeriyama M (2004) Evaluation of carrying capacity of Pacific salmon in the North Pacific Ocean for ecosystem-based sustainable conservation management. NPAFC Bull 5:1–4
Katz J, Moyle PB, Quiñones RM, Israel J, Purdy S (2012) Impending extinction of salmon, steelhead, and trout (Salmonidae) in California. Environ Biol Fish. doi:10.1007/s10641-012-9974-8
Knudsen CM, Shroder SL, Busack CA, Johnston MV, Pearsons TN, Bosch WJ, Fast DE (2006) Comparison of life history traits between first-generation hatchery and wild upper Yakima River spring Chinook salmon. Trans Am Fish Soc 135:1130–1144
Kope R (2006) Cumulative effects of multiple sources of bias in estimating spawner-recruit parameters with application to harvested stocks of Chinook salmon (Oncorhynchus tshawytscha). Fish Res 82:101–110
Korman J, Higgins PS (1997) Utility of escapement time series data for monitoring the response of salmon populations to habitat alteration. Can J Fish Aquat Sci 54:2058–2067
Kostow KE (2004) Differences in juvenile phenotypes and survival between hatchery stocks and a natural population provide evidence for modified selection due to captive breeding. Can J Fish Aquat Sci 61:577–589
Kostow K (2009) Factors that contribute to the ecological risks of salmon and steelhead hatchery programs and some mitigating strategies. Rev Fish Biol Fish 19:9–31
Kostow KE, Marshall AR, Phelps SR (2003) Naturally spawning hatchery steelhead contribute to smolt production but experience low reproductive success. Trans Am Fish Soc 132:780–790
Lackey RT, Lach DH, Duncan SL (2006) Salmon 2100: The future of wild pacific salmon. American Fisheries Society, Bethesda
Legendre P (1999) Program for multiple linear regression with permutation test. Available at: http://adn.biol.umontreal.ca/numericalecology/old/regression.html. Accessed 22 Mar 2011
Levin PS, Williams JG (2002) Interspecific effects of artificially propagated fish: an additional conservation risk for salmon. Conserv Biol 16:1581–1587
Levin PS, Zabel RW, Williams JG (2001) The road to extinction is paved with good intentions: negative association of fish hatcheries with threatened salmon. Proc R Soc B Biol 268:1153–1158
Lichatowich JA (1999) Salmon without rivers: A history of the Pacific salmon crisis. Island Press, Washington D.C
Lindley ST, Grimes CB, Mohr MS, Peterson W, Stein J, Anderson JT, Botsford LW, Bottom DL, Busack CA, Collier TK, Ferguson J, Garza JC, Grover AM, Hankin DG, Kope RG, Lawson PW, Low A, MacFarlane RB, Moore K, Palmer-Zwahlen M, Schwing FB, Smith J, Tracy C, Webb R, Wells BK, Williams TH (2009) What caused the Sacramento River fall Chinook stock collapse? National Marine Fisheries Service, Santa Cruz
Lynch M, O’Hely M (2001) Captive breeding and the genetic fitness of natural populations. Conserv Genet 2:363–378
Mantua NJ, Hare SR (2002) The Pacific Decadal oscillation. J Oceanogr 58:35–44
Mantua NJ, Hare SR, Zhang Y, Wallace JM, Francis RC (1997) A Pacific interdecadal climate oscillation with impacts on salmon production. Bull Am Meteorol Soc 78:1069–1079
McClure MM, Utter FM, Baldwin C, Carmichael RW, Hassemer PF, Howell PJ, Spruell P, Cooney TD, Schaller HA, Petrosky CE (2008) Evolutionary effects of alternative artificial propagation programs: implications for viability of endangered anadromous salmonids. Evol Appl 1:356–375
McLean JE, Bentzen P, Quinn TP (2003) Differential reproductive success of sympatric, naturally spawning hatchery and wild steelhead trout (Oncorhynchus mykiss) through the adult stage. Can J Fish Aquat Sci 60(4):433–440
Melnychuk MC, Welch DW, Walters CJ (2010) Spatio-temporal migration patterns of Pacific salmon smolts in rivers and coastal marine waters. PLoS One 5:e12916
Moore JW, McClure M, Rogers LA, Schindler DE (2010) Synchronization and portfolio performance of threatened salmon. Conserv Lett 3:340–348
Moyle PB (2002) Inland fishes of California. University of California Press, Berkeley
Moyle PB, Israel JA, Purdy SE (2008) Salmon, steelhead, and trout in California: status of an emblematic fauna. CalTrout Inc., San Francisco
Murdoch AR, Pearsons TN, Maitland TW (2010) Estimating the spawning escapement of hatchery- and natural-origin spring Chinook salmon using redd and carcass data. N Am J Fish Manag 30:361–375
Myers JM, Kope RG, Bryant GJ, Teel D, Lierheimer LJ, Wainwright TC, Grant WS, Waknitz FW, Neely K, Lindley ST, Waples RS (1998) Status review of Chinook salmon from Washington, Idaho, Oregon, and California. National Marine Fisheries Service, Seattle, Long Beach, Newport and Tiburon
Myers RA, Levin SA, Lande R, James FC, Murdoch WW, Paine RT (2004) Hatcheries and endangered salmon. Science 303:1980
Nehlsen W, Williams JE, Lichatowich JA (1991) Pacific salmon at the crossroads: stocks at risk from California, Oregon, Idaho, and Washington. Fisheries 16:4–21
Nickelson T (2003) The influence of hatchery coho salmon (Oncorhynchus kisutch) on the productivity of wild coho salmon populations in Oregon coastal basins. Can J Fish Aquat Sci 60:1050–1056
NMFS (2010) Operation of the Klamath Project between 2010 and 2018, Biological Opinion 151422SWR2008AR00148. National Marine Fisheries Service, Long Beach
Noakes DJ, Beamish RJ, Sweeting RM, King J (2000) Changing the balance: interactions between hatchery and wild Pacific coho salmon in the presence of regime shifts. NPAFC Bull 2:155–164
NRC (2004) Endangered and threatened fishes in the Klamath River basin: causes of decline and strategies for recovery. The National Academies Press, Washington D.C
Pearse DE, Donohoe CJ, Garza JC (2007) Population genetics of steelhead (Oncorhynchus mykiss) in the Klamath River. Environ Biol Fish 80:377–387
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Reisenbichler RR, Rubin SP (1999) Genetic changes from artificial propagation of Pacific salmon affect the productivity and viability of supplemented populations. ICES J Mar Sci 56:459–466
Routledge RD, Irvine JR (1999) Chance fluctuations and the survival of small salmon stocks. Can J Fish Aquat Sci 56:1512–1519
Shrimpton JM, Bernier NJ, Randall DJ (1994) Changes in cortisol dynamics in wild and hatchery-reared juvenile coho salmon (Oncorhynchus kisutch) during smoltification. Can J Fish Aquat Sci 51:2179–2187
Sinnen W, Kier MC, Hill A, Hileman J, Borok S (2010) Annual report - Trinity River basin salmon and steelehad monitoring project, 2007–2008 season. California Department of Fish and Game, Redding
Spence BC, Wainwright TC, Bjorkstedt EP (2005) In: Good TP, Waples RS, Adams P (eds) Updated status of federally listed ESUs of West coast salmon and steelhead. National Marine Fisheries Service, Seattle, pp 339–362
Sweeting RM, Beamish RJ, Noakes DJ, Neville CM (2003) Replacement of wild coho salmon by hatchery-reared coho salmon in the Strait of Georgia over the past three decades. N Am J Fish Manag 23:492–502
Thomson JR, Kimmerer WJ, Brown LR, Newman KB, Nally RM, Bennett WA, Feyrer F, Fleishman E (2010) Bayesian change point analysis of abundance trends for pelagic fishes in the upper San Francisco Estuary. Ecol Appl 20:1431–1448
Tymchuk WE, Sundström LF, Devlin RH, Hughes K (2007) Growth and survival trade-offs and outbreeding depression in rainbow trout (Oncorhynchus mykiss). Evolution 61:1225–1237
Van Doornik DM, Berejikian BA, Campbell L, Volk EC (2010) The effect of a supplementation program on the genetic and life history characteristics of an Oncorhynchus mykiss population. Can J Fish Aquat Sci 67:1449–1458
Wainwright TC, Kope RG (1999) Methods of extinction risk assessment developed for US West Coast salmon. ICES J Mar Sci 56:444–448
Weitkamp LA, Wainwright TC, Bryant GJ, Milner GB, Teel DJ, Kope RG, Waples RS (1995) Status review of coho salmon from Washington, Oregon, and California. National Marine Fisheries Service, Seattle
Williams JG (2006) Central Valley salmon: a perspective on Chinook and steelhead in the Central Valley of California. San Francisco Estuary Watershed Sci 4:1–398
Zaporozhets OM, Zaporozhets GV (2004) Interaction between hatchery and wild Pacific salmon in the far east of Russia: a review. Rev Fish Biol Fish 14:305–319
Acknowledgments
We thank California Department of Fish and Game [Diana Chesney, Morgan Knechtle, Mark Hampton (now of National Marine Fisheries Service), Wade Sinnen], Yurok Tribe Fisheries (Dan Gale, Monica Hiner), Salmon River Restoration Council (Tom Hotaling) and Iron Gate Hatchery (Kim Rushton, Jeree Orr) for providing data; Trinity River Restoration Program (Nina Hemphill) for comments on Trinity River Hatchery practices; and Marcel Holyoak for his guidance on the use of permutation tests. Huge thanks to Joe Kiernan who was instrumental in facilitating the Bayesian change point analyses. Finally, thanks to Lisa Thompson for her thoughtful review of an earlier version of the manuscript.
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Quiñones, R.M., Johnson, M.L. & Moyle, P.B. Hatchery practices may result in replacement of wild salmonids: adult trends in the Klamath basin, California. Environ Biol Fish 97, 233–246 (2014). https://doi.org/10.1007/s10641-013-0146-2
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DOI: https://doi.org/10.1007/s10641-013-0146-2