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Developmental progression of gill rakers as a post-hatch developmental marker in pink salmon, Oncorhynchus gorbuscha

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Abstract

We evaluate the usefulness of gill rakers as a post-hatch developmental marker in salmon by tracking development in undisturbed and stressed yolk-bearing salmon embryos. Native pink salmon (Oncorhynchus gorbuscha) from Auke Creek, Juneau, Alaska and genetically stressed outbred hybrids between Auke Creek and Pillar Creek (Kodiak Island) salmon were incubated in ambient-temperature Auke Creek water. Environmentally stressed native embryos were reared in water that was 2 to 4 °C warmer than ambient. The sum of rakers on the first left and right branchial arches of natives reared at ambient temperatures averaged 23.20 (SD ± 1.64) per embryo when post-hatch sampling began. The subsequent increase in raker counts was linear and positively correlated with the accumulation of thermal units until counts reached maxima 223 days after fertilization, which coincided with the complete consumption of yolk reserves. The average maximum raker count was 39.55 (SD ± 1.76) per embryo, which is substantially fewer than the 60 rakers typically observed in adults. Neither raker development nor yolk consumption patterns were affected by hybridization. Elevated incubation temperatures accelerated raker formation and yolk consumption in native embryos, but the number of rakers associated with a given amount of yolk was the same regardless of temperature suggesting that changes in yolk consumption rate and raker development rate did not influence raker counts. These results indicate that rakers are easily observed and counted, grow in a predictable sequence, and are developmentally stable in the face of both genetic and environmental stress, thereby making them potentially reliable post-hatch developmental markers.

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References

  • Adkison MD (1995) Population differentiation in Pacific salmon: local adaptation, genetic drift, or the environment? Can J Fish Aquat Sci 52:2762–2777

    Article  Google Scholar 

  • Ballard WW (1973) Normal embryonic stages for salmonid fishes based on Salmo gairdneri Richardson and Salvelinus fontinalis Mitchell. J Exp Zool 184:7–26

    Article  Google Scholar 

  • Ban M (2000) Effects of photoperiod and water temperature on smoltification of yearling sockeye salmon (Oncorhynchus nerka). Bull Nat Salmon Res Center 3:25–28

    Google Scholar 

  • Battle HI (1944) The embryology of the Atlantic salmon (Salmo salar Linnaeus). Can J Res 22D(5):105–125

    Article  Google Scholar 

  • Bestgen KR (2008) The effects of water temperature on growth of razorback sucker larvae. West N Am Nat 68:15–20

    Article  Google Scholar 

  • Bornbusch A, Lee M (1992) Gill raker structure and development in Indo-Pacific Anchovies (Teleostei: Engrauloidea), with a discussion of the structural evolution of Engrauloid gill rakers. J Morphol 214:10–119

    Article  Google Scholar 

  • Britz R (1997) Egg surface structure and larval cement glands in nandid and badid fishes with remarks on phylogeny and biogeography. Am Mus Novit 3195:1–17

    Google Scholar 

  • Campbell WB (2003) Assessing developmental errors in branchiostegal rays as indicators of chronic stress in two species of Pacific salmon. Can J Zool 81:1876–1884

    Article  Google Scholar 

  • Campbell WB, Emlen JM, Hershberger WK (1998) Thermally induced chronic developmental stress in coho salmon: Integrating measures of mortality, early growth, and developmental instability. Oikos 81:398–410

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Debat V, David P (2001) Mapping phenotypes: canalization, plasticity, and developmental stability. Trends Ecol Evol 16:555–561

    Article  Google Scholar 

  • Foote CJ, Moore K, Stenberg K, Craig KJ, Wenburg JK, Wood CC (1999) Genetic differentiation in gill raker number and length in sympatric anadromous and nonanadromous morphs of sockeye salmon, Oncorhynchus nerka. Environ Biol Fish 54:263–274

    Article  Google Scholar 

  • Gaillard JM, Yoccoz NG (2003) Temporal variation in survival of mammals: a case of environmental canalization? Ecology 84:3294–3306

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gharrett AJ, Smoker WW, Geiger HJ, Wang IA, Hebert, KP, Goddard PL, McGregor AJ, Lane S, Joyce J, Taylor SG (1999) Genetic structure in Auke Creek pink salmon and its role in productivity. Bull Natl Res Inst Aquacult Suppl. I:19–26

  • Gilbert SG (2000) Developmental biology, 6th edn. Sinauer Associates, Maryland

    Google Scholar 

  • Gilk SE, Wang IA, Hoover CL, Smoker WW, Taylor SG (2004) Outbreeding depression in hybrids between spatially separated pink salmon, Oncorhynchus gorbuscha, populations: marine survival, homing ability, and variability in family size. Environ Biol Fishes 69:287–297

    Article  Google Scholar 

  • Gisbert E, Merino G, Muguet JB, Bush D, Piedrahita RH, Conklin DE (2002) Morphological development and allometric growth patterns in hatchery-reared California halibut larvae. J Fish Biol 61:1217–1229

    Article  Google Scholar 

  • Groot C, Margolis L (1991) Pacific salmon life histories. UBC Press, Vancouver

    Google Scholar 

  • Haddon M, Willis TJ (1995) Morphometric and meristic comparison of orange roughy (Hoplostethus atlanticus: Trachichthyidae) from Puysegur Band and Lord Howe Rise, New Zealand, and its implications for stock structure. Mar Biol 123:19–27

    Article  Google Scholar 

  • Heard WR (1991) Life history of pink salmon (Oncorhynchus gorbuscha). In: Groot CG, Margolis L (eds) Pacific salmon life histories. UBC Press, Vancouver, pp 121–230

    Google Scholar 

  • Humphries P (1993) A comparison of the mouth morphology of three co-occurring species of atherinid. J Fish Biol 42:585–593

    Article  Google Scholar 

  • Jobling M (1994) Fish bioenergetics. Fish & Fisheries Series, vol. 13. Springer, New York

    Google Scholar 

  • Johnson O, Neely K, Waples R (2004) Lopsided fish in the Snake River Basin—fluctuating asymmetry as a way of assessing impact of hatchery supplementation in Chinook salmon, Oncorhynchus tshawytscha. Environ Biol Fish 69:379–394

    Article  CAS  Google Scholar 

  • Koumoundouros G, Kiriakos Z, Divanach P, Kentouri M (1994) Morphometric relationships as criteria for the evaluation of culture conditions of gilthead sea bream (Sparus aurata) at the larval stage. In: Kestemont P, Muir J, Sevilia F, Williot P (eds) Measures for success. Cemagref-DICOVA, Bordeaux, pp 199–205

    Google Scholar 

  • Leary RF, Allendorf FW (1989) Fluctuating asymmetry as an indicator of stress: implications for conservation biology. Trends Ecol Evol 4:214–217

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Assoc. Inc., Maryland

    Google Scholar 

  • Malecha PW (2002) Survival and development of pink salmon (Oncorhynchus gorbuscha) embryos and fry as related to egg size and quantitative genetic variation. Masters Dissertation, University of Alaska, Fairbanks

  • Marshall TC, Spalton JA (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian Oryx. Anim Conserv 3:241–248

    Article  Google Scholar 

  • McClelland EK, Myers JM, Hard JJ, Park LK, Naish KA (2005) Two generations of outbreeding in Coho salmon (Oncorhynchus kisutch): effects on size and growth. Can J Fish Aquat Sci 62:2538–2547

    Article  Google Scholar 

  • Miller DJ, Lea RN (1972) Guide to the coastal marine fishes of California. Calif. Dept. Fish and Game. Fish. Bull. 157

  • Moller AP (1997) Developmental stability and fitness: a review. Am Nat 149:916–932

    Article  PubMed  CAS  Google Scholar 

  • Neira FJ, Miskiewicz AG, Trnski T (1998) Larvae of temperate Australian fishes—laboratory guide for larval fish identification. University of Western Australia Press, Nedlands

    Google Scholar 

  • Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental instability: its origins and evolutionary implications. Kluwer, Dordrecht, pp 335–364

    Chapter  Google Scholar 

  • Palmer AR, Strobeck C (2003) Fluctuating asymmetry analyses revisited. In: Polak M (ed) Developmental instability—causes and consequences. Oxford University Press, New York, pp 279–319

    Google Scholar 

  • Parsons PA (1990) Fluctuating asymmetry: an epigenetic measure of stress. Biol Rev 65:131–145

    Article  PubMed  CAS  Google Scholar 

  • Pelluet D (1944) Criteria for the recognition of developmental stages in the salmon (Salmo salar). J Morph 74:395–407

    Article  Google Scholar 

  • SAS Institute Inc (2002) SAS 9.1.3 help and documentation. The SAS Institute, Cary

    Google Scholar 

  • Searle SR, Casella G, McCulloch CE (1992) Variance components. Wiley, New York

    Book  Google Scholar 

  • Shaw RG (1987) Maximum-likelihood approaches to quantitative genetics of natural populations. Evolution 41:812–826

    Article  Google Scholar 

  • Shields WM (1982) Philopatry, inbreeding and the evolution of sex. State University of New York Press, Albany

    Google Scholar 

  • Taylor SG, Lum JL (2003) Auke Creek Weir 2002 Annual report, operations, fish counts, and historical summaries. National marine fisheries service, Auke Bay Laboratory, 11305 Glacier Highway, Juneau, Alaska, pp 99801–8626

  • Valentine DW, Soule ME, Samollow PM (1973) Asymmetry analysis in fishes: a possible statistical indicator of environmental stress. Fish Bull 71:357–368

    Google Scholar 

  • Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    Article  Google Scholar 

  • Waddington CH (1957) The strategy of genes. George Allen & Unwin, London

    Google Scholar 

  • Wang IA, Gilk SE, Smoker WW, Gharrett AJ (2007) Outbreeding effect of embryo development in hybrids of allopatric pink salmon (Oncorhynchus gorbuscha) populations, a potential consequence of stock translocation. Aquaculture 272S1:S52–S160

    Google Scholar 

  • Whitehead PJP (1985) FAO Species Catalogue, Vol. 7. Clupeoid fishes of the world. An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, anchovies, and wolfherrings. Part I—Chirocentridae, Clupeidae, and Pristigasteridae. FAO Fisheries Synopsis 7

  • Witte F, Welten M, Heemskerk M, van der Stap I, Ham L, Rutjes H, Wanink J (2008) Major morphological changes in a Lake Victoria cichlid fish within two decades. Biol J Linn Soc 94:41–52

    Article  Google Scholar 

  • Yokogawa K, Seki S (1995) Morphological and genetic differences between Japanese and Chinese bass of the genus Lateolabrax. Jpn J Ichthyol 41:437–455

    Google Scholar 

Download references

Acknowledgments

This publication is the result of research sponsored by Alaska Sea Grant with funds from the National Oceanic and Atmospheric Administration Office (NOAA) of Sea Grant, Department of Commerce, under grant no. NA 86RG0050 (project no. R/31–06). We thank NOAA Fisheries AFSC for the use and operation of the Auke Creek Research Station, as well as the Alaska Department of Fish and Game’s Mark, Tag, and Age Laboratory (Ron Josephson, Director) for providing additional funding, laboratory facilities, and logistical support. Special thanks go to Peter Hagen at NOAA who helped develop the image analysis system. We would also like to acknowledge P. Hagen, G. Cailliet, and M. Adkison for providing critical reviews of this manuscript. The protocol for this research was approved by the University of Alaska, Fairbanks Institutional Animal Care and Use Committee as governed by regulations of the US Department of Agriculture and US Institute of Health.

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Correspondence to Dion S. Oxman.

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Oxman, D.S., Smoker, W.W. & Gharrett, A.J. Developmental progression of gill rakers as a post-hatch developmental marker in pink salmon, Oncorhynchus gorbuscha . Environ Biol Fish 96, 677–689 (2013). https://doi.org/10.1007/s10641-012-0058-6

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  • DOI: https://doi.org/10.1007/s10641-012-0058-6

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