Abstract
Temperature stress on developing steelhead (Oncorhynchus mykiss) was evaluated using asymmetry of skeletal characters, fish condition factor, and metabolic fingerprints. Eggs from three female hatchery steelhead were fertilized by a single male. The eggs from each female were divided into two groups and incubated at either 8°C or 18°C. Mortality, growth, and condition factor were measured at stage 6 (32 cells), stage 20 (eyed), and stage 21 (caudal flexing). In addition, 1H-nuclear magnetic resonance (NMR) spectroscopy was used to establish metabolic fingerprints of developing eggs at the three stages. After hatching, all alevins were moved to tanks at 18°C and allowed to develop to 60 days post-emergence (DPE), at which point they were examined for structural asymmetry. Eggs incubated at 18°C experienced higher mortality, with all eggs from one hen dying at the higher temperature. Eggs incubated at the higher temperature that did survive hatched as larger larval fish than eggs incubated at the lower temperature. Fish incubated at the higher temperature exhibited greater structural asymmetry than fish incubated at the lower temperature. A principle components (PC) analysis of the metabolic fingerprints indicated that PC1 and PC2 accounted for 60% of the variance in the metabolites. Separation along PC1 corresponded to differences in developmental stage, and separation along PC2 corresponded to differences in hen. Eggs incubated at 18°C lagged behind eggs incubated at 8°C along PC1, indicating a potential problem with embryo staging. PC1 scores were highly correlated with the accumulated thermal units during development, indicating that scores along PC1 were a robust measure of developmental stage.
Similar content being viewed by others
References
Baxter JHS (1988) Pattern and variety in development. In: Hoar WS, Randall DJ (eds) Fish physiology vol XI pt A: Eggs, larvae. Academic, New York, pp 1–58
Bjorn TC, Reiser DW (1991) Habitat requirements of anadromous salmonids. In: Meehan WR (ed) Influence of forest and range management on salmonid fishes their habitats. Special publication 19. American Fisheries Society, Bethesda, MD, pp 83–138
Bollard ME, Garrod S, Holmes E, Lindon JC, Humpfer E, Spraul M, Nicholson JK (2000) High-resolution 1H and 1H−13C magic angle spinning NMR spectroscopy of rat liver. Magn Reson Med 44:201–207
Bryden C, Heath D (2000) Heritability of fluctuating asymmetry for multiple traits in chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 57:2186–2192
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
Fan WMT (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog Nucl Magn Res 28:161–129
Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2002) Effects of size and temperature on metabolic rate. Science 293:2248–2251
Huuskonen H, Penttinen O-P, Piironen J (2003) Effects of temperature and parental background on embryonic survival and metabolic rate of newly hatched Arctic charr. In: Browman HI, Skiftesvik AB (eds) The big fish bang. Proceedings of the 26th annual larval fish conference. Institute of Marine Research, Bergen Norway, pp 35–44
Jagoe CH, Haines TA (1985) Fluctuating asymmetry in fishes inhabiting acidified and unacidified lakes. Can J Fish Aquat Sci 63:130–138
Leamy L (1999) Heritability of directional and fluctuating asymmetry for mandibular characters in random-bred mice. J Evol Biol 12:146–155
Leary RF, Allendorf FW, Knudsen KL (1984) Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes. Am Nat 124:540–551
Leary RF, Allendorf FW, Knudson RL (1992) Genetic, environmental, and developmental causes of meristic variation in rainbow trout. Acta Zool Fenn 191:79–95
Lee GC, Woodruff DL (2004) Beam search for peak alignment of NMR signals. Anal Chim Acta 513:413–416
Møller AP, Shykoff JA (1999) Morphological developmental stability in plants: patterns and causes. Int J Plant Sci 160:S135–S146
Nathanailides C (1996) Metabolic specialization of muscle during development in cold-water and warmwater fish species exposed to different thermal conditions. Can J Fish Aquat Sci 53:2147–2155
Ojanguren AF, Reyes-Gavilán FG, Munoz RR (1999) Effects of temperature on growth and efficiency of yolk utilization in eggs and pre-feeding larval stages of Atlantic salmon. Aquac Int 7:81–87
Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow EA (ed) Developmental instability: its origins and evolutionary implications. Kluwer, Dordrecht, pp 335–364
Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zool Fenn 191:57–72
Purohit PV, Rocke DM, Viant MR, Woodruff DL (2004) Discrimination models using variance stabilizing transformation of metabolomic NMR data. Omics 8:118–130
Reimchen TE, Nosil P (2001) Lateral plate asymmetry, diet and parasitism in threespine stickleback. J Evol Biol 14:632–645
Rombough PJ (1994) Energy partitioning during fish development—additive or compensatory allocation of energy to support growth. Funct Ecol 8:178–186
Snyder DE, Muth RT (1990) Description and identification of razorback, flannelmouth, white, Utah, bluehead, and mountain sucker larvae and early juveniles. Colorado Division of Wildlife Technical Publication no. 38
Somarakis IK, Peristeraki N, Tsimenides N (1997) Fluctuating asymmetry in the otoliths of larval anchovy Engraulis encrasicolus and the use of developmental instability as an indicator of condition in larval fish. Mar Ecol Prog Ser 151:191–203
Srivastava RK, Brown JA, Shahidi F (1995) Changes in the amino acid pool during embryonic development of cultured and wild Atlantic salmon (Salmo salar). Aquaculture 131:115–124
Sullivan K, Martin DJ, Cardwell RD, Toll JE, Duke S (2000) An analysis of the effects of temperature on salmonids of the Pacific northwest with implications for selecting temperature criteria. Sustainable Ecosystems Institute, Portland, OR
Sze DY, Jardetzky O (1990) Determination of metabolite and nucleotide concentrations in proliferating lymphocytes by 1H-NMR of acid extracts. Biochim Biophys Acta 1054:181–197
Van Valen L (1962) A study of fluctuating asymmetry. Evolution 16:125–142
Viant MR (2003) Improved methods for the acquisition and interpretation of NMR metabolomic data. Biochem Biophys Res Commun 310:943–948
Wagner EJ (1996) History and fluctuating asymmetry of Utah salmonid broodstocks. Prog Fish Cult 58:92–103
Weckwerth W (2003) Metabolomics in systems biology. Annu Rev Plant Biol 54:669–689
Windig JJ, Nylin S (2000) How to compare fluctuating asymmetry of different traits. J Evol Biol 13:29–37
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Turner, M.A., Viant, M.R., Teh, S.J. et al. Developmental rates, structural asymmetry, and metabolic fingerprints of steelhead trout (Oncorhynchus mykiss) eggs incubated at two temperatures. Fish Physiol Biochem 33, 59–72 (2007). https://doi.org/10.1007/s10695-006-9117-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-006-9117-2