Skip to main content
SpringerLink
Log in

Lopsided Fish in the Snake River Basin — Fluctuating Asymmetry as a way of Assessing Impact of Hatchery Supplementation in Chinook Salmon, Oncorhynchus tshawytscha

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

The use of developmental instability (an individual's failure to produce a consistent phenotype in a given environment) was evaluated to detect the effects of outplanting hatchery fish on wild salmon. Juvenile chinook salmon were collected in 1989, 1990, and 1991 from five drainages in the Snake River Basin. In each drainage we attempted to collect fish from streams with no hatchery supplementation (wild), naturally spawning fish from streams with hatchery supplementation (natural), and fish collected at a hatchery. Forty fish were collected per site and the number of elements in bilateral characters were counted on each side of the fish. Indices of fluctuating asymmetry (FA), a measure of minor, random deviations in perfect symmetry of bilateral counts, were calculated as an estimator of developmental instability. Analysis of character counts from seven paired characters revealed normal distributions. Only one of the characters displayed counts that were statistically larger on one side than the other, indicating that directional asymmetry (DA) or antisymmetry was not a major bias of FA. However, the means of all individual characters revealed a non-statistically significant left side bias. We analyzed our data using two indices of FA (FA1 and FA5) with different levels of sensitivity to DA. Differences in both FA indices were found among years, with collection sites in 1989 having significantly larger FA values than in 1991 (FA p < 0.01). Levels of FA among wild, natural, and hatchery fish were comparatively small (FA1 p = 0.17). This suggests developmental conditions were different in the first year of the study than in the last. The cause of these differences may be linked to either genetic or environmental variation or to gene—environment interactions, but the general population declines of salmon that occurred during this time obscures more specific conclusions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alados, C.L., J. Escos & J.M. Emlen. 1993. Developmental instability as an indicator of environmental-stress in the Pacific hake (Merluccius productus). Fish. Bull. 91: 587–593.

    Google Scholar 

  • Alibert, P. & J. Auffray. 2003. Genomic coadaptation, outbreeding depression, and developmental instability. pp. 116–134. In: M. Polak (ed.) Developmental Instability Causes and Consequences, Oxford University Press, New York.

    Google Scholar 

  • Allenbach, D.M., K.B. Sullivan & M.J. Lydy. 1999. Higher fluctuating asymmetry as a measure of susceptibility to pesticides in fishes. Environ. Toxicol. Chem. 18: 899–905.

    Article  CAS  Google Scholar 

  • Allendorf, F.W. & N. Ryman. 1987. Genetic management of hatchery stocks. pp. 141–159. In: N. Ryman & F. Utters (ed.) Population Genetics and Fishery Management, University of Washington Press, Seattle, WA.

    Google Scholar 

  • Anderson, T.W. & J.D. Finn. 1996. The New Statistical Analysis of Data. Springer-Verlag, New York.

    Google Scholar 

  • Campton, D.E. 1995. Genetic effects of hatchery fish on wild populations of Pacific salmon and steelhead: What do we really know? pp. 337–353. In: H.L. Schramm Jr. & R.G. Piper (ed.) Uses and Effects of Cultured Fishes in Aquatic Ecosystems. Am. Fish. Soc. Symp. 15.

  • Clarke, G.M. 1993. The genetic basis of developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation. Genetica 89: 15–23.

    Google Scholar 

  • Clarke, G.M. 1995a. The genetic basis of developmental stability. II. Asymmetry of extreme phenotypes revisited. Am. Nat. 146: 708–725.

    Article  Google Scholar 

  • Clarke, G.M. 1995b. Relationships between developmental stability and fitness: Applications for conservation biology. Conserv. Biol. 9: 18–25.

    Article  Google Scholar 

  • Cuenco, M.L., T.H. Backman & P.R. Mundy. 1993. The use of supplementation to aid in natural stock restoration. pp. 269–293. In: J.G. Cloud & G.H. Thorgaard (ed.) Genetic Conservation of Salmonid Fishes. Proceedings of a NATO advanced Study Institute, Plenum Press, New York.

    Google Scholar 

  • Emlen, J.M. 1991. Heterosis and outbreeding depression: A multilocus model and an application to salmon production. Fish. Res. 12: 187–212.

    Article  Google Scholar 

  • Escos, J., C.L. Alados, J.M. Emlen & S. Alderstein. 1995. Developmental instability in the Pacific hake parasitized by myxosporeans Kudoa spp. Trans. Amer. Fish. Soc. 124: 943–945.

    Google Scholar 

  • Felley, J. 1980. Analysis of morphology and asymmetry in blue gill sunfish (Lepomis macrochirus) in the southeastern United states. Copeia 1: 1980, 18–29.

    Google Scholar 

  • Ferguson, M. 1986. Developmental stability of rainbow trout hybrids: Genomic coadaptation or heterozygosity. Evolution 40: 323–330.

    Google Scholar 

  • Ford, M.J. 2002. Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv. Biol. 16: 815–825.

    Article  Google Scholar 

  • Freeman, D.C., J.H. Graham, D.W. Byrd, E.D. McArthur & W.A. Turner. 1995. Narrow hybrid zone between two subspecies of big sagebrush, Artemisia tridentate (Asteraceae). III. Developmental instability. Amer. J. Bot. 82: 1144–1152.

    Google Scholar 

  • Gharrett, A.J. & W.W. Smoker. 1991. Two generations of hybrids between even-and odd-year pink salmon (Oncorhynchus gorbuscha): a test for outbreeding depression? Can. J. Fish. Aq. Sci. 48: 1744–1749.

    Google Scholar 

  • Gharrett, A.J., W.W. Smoker, R.R. Reisenbichler & S.G. Taylor. 1999. Outbreeding depression in hybrids between odd-and even-broodyear pink salmon. Aquaculture 173: 117–129.

    Article  Google Scholar 

  • Graham, J.H. 1992. Genomic coadaptation and developmental stability in hybrid zones. Acta Zool. Fennica 191: 121–131.

    Google Scholar 

  • Graham, J.H. & J.D. Felley. 1985. Genomic coadaptation and developmental stability within introgressed populations of Enneacanthus gloriosus and E. obesus (Pisces, Centrarchidae). Evolution 391: 104–114.

    Google Scholar 

  • Graham, J.H., D.C. Freeman & J.M. Emlen. 1993. Antisymmetry, directional asymmetry, and dynamic morphogenesis. Genetica 89: 121–137.

    Google Scholar 

  • Graham, J.H., J.M. Emlen, D.C. Freeman, L.J. Leamy & J.A. Kieser. 1998. Directional asymmetry and the measurement of developmental instability. Biol. J. Linn. Soc. 64: 1–16.

    Article  Google Scholar 

  • Graham, J.H., J.M. Emlen & D.C. Freeman. 2003. Nonlinear dynamics and developmental instability. pp. 35–50. In: M. Polak (ed.). Developmental Instability Causes and Consequences. Oxford University Press, New York.

    Google Scholar 

  • Ham, K.D. & T.N. Pearsons. 2000. Can reduced salmonid population abundance be detected in time to limit management impacts? Can. J. Fish. Aquat. Sci. 57: 17–24

    Article  Google Scholar 

  • Hindar, K., N. Ryman & F. Utter. 1991. Genetic effects of cultured fish on natural fish populations. Can. J. Fish. Aquat. Sci. 48: 945–957.

    Google Scholar 

  • Jagoe, C.H. & T.A. Haines. 1985. Fluctuating asymmetry in fishes inhabiting acidified and unacidified lakes. Can. J. Zool. 63: 130–138.

    CAS  Google Scholar 

  • Kieser, J.A. 1992. Fluctuating odontometric asymmetry and maternal alcohol consumption. Ann. Hum. Biol. 19: 513–520.

    CAS  Google Scholar 

  • Lagler, K.F., J.E. Bardach, R.R. Miller & D.R. Passion. 1977. Ichthyology, 2nd edition. John Wiley & Sons, New York, 506 pp.

    Google Scholar 

  • Landrum, B.J. 1966. Bilateral asymmetry in paired meristic characters of Pacific salmon. Pac. Sci. 20: 193–202.

    Google Scholar 

  • Leamy, L. 1984. Morphometric studies in inbred and hybrid house mice. V. Directional and fluctuating asymmetry. Am. Nat. 123: 579–593.

    Article  Google Scholar 

  • Leary, R. & F. Allendorf. 1989. Fluctuating asymmetry as an indicator of stress: implications for conservation biology. Trends in Ecology and Evolution. 4(7): 214–217.

    Article  Google Scholar 

  • Leary, R.F., F.W. Allendorf & K.L. Knudsen. 1983. Developmental stability and enzyme heterozygosity in rainbow trout. Nature 301: 71–72.

    Article  CAS  Google Scholar 

  • Leary, R.F., F.W. Allendorf & K.L. Knudsen. 1984. Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes. Am. Nat. 124: 540–551.

    Article  Google Scholar 

  • Leary, R.F., F.W. Allendorf & K.L. Knudsen. 1985a. Inheritance of meristic variation and the developmental stability in rainbow trout. Evolution 39: 308–314.

    Google Scholar 

  • Leary, R.F., F.W. Allendorf & K.L. Knudsen. 1985b. Developmental instability and high meristic counts in interspecific hybrids of salmonid fishes. Evolution 39: 1318–1326.

    Google Scholar 

  • Leary, R.F., F.W. Allendorf & K.L. Knudsen. 1985c. Developmental instability as an indicator of reduced genetic variation in hatchery trout. Trans. Amer. Fish. Soc. 114: 230–235.

    Article  Google Scholar 

  • Leary, R.F., F.W. Allendorf & K.L. Knudsen. 1987. Differences in inbreeding coefficients do not explain the association between heterozygosity at allozyme loci and developmental stability in rainbow trout. Evolution 41: 1413–1415.

    Google Scholar 

  • Leary, R.F., F.W. Allendorf & K.L. Knudsen. 1993. Null alleles at two lactate dehydrogenase loci in rainbow trout are associated with decreased developmental stability. Genetica 89: 3–14.

    CAS  Google Scholar 

  • Lens, L., S. Van Dongen & E. Matthysen. 2002. Fluctuating asymmetry as an early warning system in the critically endangered Taita thrush. Conserv. Biol. 16: 479–487.

    Article  Google Scholar 

  • Lerner, I.M. 1954. Genetic Homeostasis. Wiley, New York. 134 pp.

    Google Scholar 

  • Leung, B. & M.R. Forbes. 1997. Modeling fluctuating asymmetry in relation to stress and fitness. OKIOS 78: 397–405.

    Google Scholar 

  • Lindsey, C.C. 1988. Factors controlling meristic variation. pp. 197–274. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology. Vol. XIB, Academic Press, New York.

    Google Scholar 

  • Lynch, M. & M. O'Hely. 2001. Captive breeding and the genetic fitness of natural populations. Conserv. Genet. 2: 363–378.

    Article  Google Scholar 

  • Mara, R.L. 1995. Developmental Stability in Acer rubrum. M.S. Thesis, Wayne State University, Detroit, Michigan. 28 pp.

    Google Scholar 

  • Magnuson, J.J. 1996. Upstream: Salmon and Society in the Pacific Northwest. National Academy of Sciences, Washington D.C. 452 pp.

    Google Scholar 

  • Markow, T.A. & J.P. Ricker. 1992. Male size, developmental stability, and mating success in natural populations of three Drosophila species. Heredity 69: 122–127.

    Google Scholar 

  • Markow, T.A. & J. Martin. 1993. Inbreeding and developmental stability in a small human population. Ann. Hum. Biol. 20: 389–394.

    CAS  Google Scholar 

  • Martin, O.Y. & D.J. Hosken. 2002. Asymmetry and fitness in female yellow dung flies. Biol. J. Linn. Soc. Lond. 76: 557–563.

    Google Scholar 

  • Mather, K. 1953. Genetical control of stability in development. Heredity 7: 297–336.

    Google Scholar 

  • McClure, M.M., E.E Holmes, B.L. Sanderson & C.E. Jordan. 2003. A large-scale, multi-species assessment: Anadromous salmonids in the Columbia River Basin. Ecol. Appl. 13(4): 964–989.

    Google Scholar 

  • McKenzie, J.A. & G.M. Clarke. 1988. Diazinon resistance, fluctuating asymmetry, and fitness in the Australian sheep blowfly. Genetics 120: 213–220.

    CAS  Google Scholar 

  • McKenzie, J.A. & K. O'Farrell. 1993. Modification of developmental instability and fitness: Malathion-resistance in the Australian sheep blowfly, Lucilia cuprina. Genetica 89: 67–76.

    Google Scholar 

  • Møller, A.P. 1997. Developmental stability and fitness: a review. Am. Nat. 149: 916–932.

    Google Scholar 

  • Møller, A.P. & J.P. Swaddle. 1997. Asymmetry, Developmental Stability, and Evolution. Oxford University Press Inc., New York. 291 pp.

    Google Scholar 

  • Nehlsen, W., J.E. Williams & J.A. Lichatowich. 1991. Pacific salmon at the crossroads: Stocks at risk from California, Oregon, Idaho, and Washington. Fisheries 16: 4–21.

    Google Scholar 

  • Neville, A.C. 1976. Animal Asymmetry. Edward Arnold Publishers Ltd., London.

    Google Scholar 

  • Palmer, A.R. 1994. Fluctuating asymmetry:Aprimer. pp. 335–364. In: T.A. Markow (ed.) Developmental Instability: Its Origin and Evolutionary Implications, Kluwer Academic Publishers, Dordrecht, the Netherlands.

    Google Scholar 

  • Palmer, A.R. & C. Strobeck. 1992. Fluctuating Asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests. Acta Zool. Fennica 191: 57–72.

    Google Scholar 

  • Palmer, A.R. & C. Strobeck. 1986. Fluctuating asymmetry: Measurement, analysis and pattern. Annu. Rev. Ecol. Syst. 17: 391–421.

    Article  Google Scholar 

  • Perez-Tris, J., R. Carbonell & J.L. Telleria. 2002. Parasites and the blackcap's tail: Implications for the evolution of feather ornaments. Biol. J. Linn. Soc. 76: 481–492.

    Article  Google Scholar 

  • Piper, R.G., L.E. McElwain, J.P. McCaren, L.G. Fowler & J.R. Leonard. 1982. Fish Hatchery Management. U.S. Department of the Interior, Fish and Wildlife Service, Washington, D.C., 517 pp.

    Google Scholar 

  • Polak, M. 2003. Introduction. pp. xix–xxiii. In: M. Polak (ed.). Developmental Instability Causes and Consequences. Oxford University Press, New York.

    Google Scholar 

  • Polak, M. 1994. Parasites increase fluctuating asymmetry of male Drosophila nigrospiraculla: Implication for sexual selection. pp. 257–268. In: T. Markow (ed.) Developmental Instability: Its Origins and Evolutionary Implications, Kluwer Academic Publishers, Dordrecht, the Netherlands.

    Google Scholar 

  • Reisenbichler, R.R. & S.P. Rubin. 1999. Genetic changes from artificial propagation of Pacific salmon affect the productivity and viability of supplemented populations. ICES J. Mar. Sci. 56: 459–466.

    Article  Google Scholar 

  • Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.

    Google Scholar 

  • Ricker, W.E. 1972. Hereditary and environmental factors affecting certain salmonid populations. pp. 19–160. In: R.C. Simon & P.A. Larkin (ed.) The Stock Concept in Pacific Salmon, Macmillan Lectures in Fisheries, University of British Columbia, Vancouver, B.C.

    Google Scholar 

  • Sokal, R.R. & F.J. Rohlf. 1981. Biometry. W.H. Freeman & Co., New York, 859 pp.

    Google Scholar 

  • Soule, M.E. 1967. Phenetics of natural populations. II. Asymmetry and evolution in a lizard. Amer. Nat. 101: 142–159.

    Google Scholar 

  • Smith, C.E. & R.G. Piper. 1972. Pathological effects in formalin-treated rainbow trout (Salmo gairdneri). J. Fish. Res. Board. 29: 328–329.

    Google Scholar 

  • Taylor, E.B. 1991. A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98: 185–207.

    Article  Google Scholar 

  • Ueno, H. 1994. Fluctuating asymmetry in relation to two fitness components, adult longevity and male mating success in a ladybird beetle, Harmonia axyridis (Coleoptera: Coccinellidae). Ecol. Entomol. 19: 87–88.

    Google Scholar 

  • Valentine, D.W. & M.E. Soule. 1973. Effect of p,p-DDT on developmental stability of pectoral fin rays in the grunion, Leuresthes tenuis. Fish. Bull. 71: 921–926.

    Google Scholar 

  • Van Dongen, S. 1999. Accuracy and power in fluctuating asymmetry studies: Effects of sample size and number of within-subject repeats. J. Evol. Biol. 12: 547–550.

    Google Scholar 

  • Van Valen, L. 1962. A study of fluctuating asymmetry. Evolution 16: 125–142.

    Google Scholar 

  • Vrijenhoek, R.C. & S. Lerman. 1982. Heterozygosity and developmental stability under sexual and asexual breeding systems. Evolution 36: 768–776.

    Google Scholar 

  • Waddington, C.H. 1940. Organisers & Genes. Cambridge University Press, Cambridge, England, 160 pp.

    Google Scholar 

  • Waddington, C.H. 1957. The Strategy of the Genes. George Allen & Unwin, London.

    Google Scholar 

  • Waples, R.S. 1991. Genetic interactions between hatchery and wild salmonids: Lessons from the Pacific Northwest. Can. J. Fish. Aquat. Sci. 48(Suppl. 1): 124–133.

    Google Scholar 

  • Waples, R.S. & J. Drake. 2003. Risk/benefit considerations for marine stock enhancement: A Pacific salmon perspective. pp. 260–306. In: K.M. Leber, S. Kitada, T. Svåsand & H.L. Blankenship (ed.) Proceedings of Second International Symposium on Stock Enhancement. Kobe, Japan, January 2002, Blackwell Publishing Ltd, Oxford, U.K.

    Google Scholar 

  • Whitlock, M.C. & K. Fowler. 1997. The instability of studies of instability. J. Evol. Biol. 10: 63–67.

    Article  Google Scholar 

  • Wilkins, N.P., E. Gosling, A. Curatolo, A. Linnane, C. Jordan & H.P. Courtney. 1995. Fluctuating asymmetry in Atlantic salmon, European trout and their hybrids, including triploids. Aquaculture 137: 77–85.

    Article  Google Scholar 

  • Zakharov, V.M. 2003. Linking developmental stability and environmental stress; A whole organism approach. pp. 402–414. In: M. Polak (ed.) Developmental Instability Causes and Consequences. Oxford University Press, New York.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Marine Fisheries Service, Northwest Fisheries Science Center, 2725 Montlake Blvd. East, Seattle, WA, 98112, U.S.A.

    Orlay Johnson, Kathleen Neely & Robin Waples

Authors
  1. Orlay Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kathleen Neely
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robin Waples
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johnson, O., Neely, K. & Waples, R. Lopsided Fish in the Snake River Basin — Fluctuating Asymmetry as a way of Assessing Impact of Hatchery Supplementation in Chinook Salmon, Oncorhynchus tshawytscha . Environmental Biology of Fishes 69, 379–393 (2004). https://doi.org/10.1023/B:EBFI.0000022892.42826.1a

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:EBFI.0000022892.42826.1a

Search

Navigation