JWARP  Vol.2 No.2 , February 2010
Temporal Study of Stress-Induced Effects Caused by Developmental Temperature Changes and Water Quality in an Isolated Northern Pike (Esox lucius L.) Population
ABSTRACT
Development perturbations may affect the regular phenotype and are commonly measured through fluctuat-ing asymmetry (FA) levels. Short-term climatic variations, that modify the temperature, can influence chemical and physical water characteristics. Fishes have been used as model organisms for studying stress-induced changes in body symmetry, since they are ectothermic, good bioindicators, easy to find and having economic relevance. Northern pike being a holoarctic, big, edible, top predator is one of the most economically important freshwater fish for recreational and commercial fisheries and freshwater ecosystems management. The isolated population of Lake Trasimeno (Central Italy)—in good health conditions and that can be considered one of the genetically best conserved of Italy—, was chosen as model. FA, seven mi-crosatellite loci and early developmental stages were investigated in order to correlate the developmental stability of this population to its genetic variability and to environmental perturbations. The results obtained underlined a positive correlation (>>0.40) between FA indexes and temperature; the non-parametric Kruskall- Wallis test showed significant differences in FA levels for some FA indexes and parameters. Over-all results underlined that FA increased in individuals grown at a temperature above 8°C as compared with those grown at 5°C or at lower temperatures. Both positive and negative correlations between FA parameters and chemical and physical water characteristics were shown. The comparison of genetic and FA data under-lined a low correlation between microsatellite and FA pairwise distances, nevertheless a positive and signifi-cant correlation emerged for some FA measurements and microsatellite data. In particular, only Elu87 locus showed a statistical significant correlation versus total FA. Finally, as expected, results indicated that the in-cubation time was temperature-dependent; the ODT was in the range 8–10°C and lower and higher tempera-tures caused drastic embryo mortality. These results showed robust correlations, both positive and negative, between some FA parameters and chemical and physical characters and were in agreement with the assump-tion that temperature variations as well as pH, conductibility and chloride variation, may increase molecular perturbations and, subsequently, the global developmental noise during development. These data suggest that FA could be considered a measure of animal welfare. The relative breeding easiness of this species may be a valid tool for the estimation of controlled environmental stress influences, not only of thermal origin, and a valid information basis for studies on wild populations. Furthermore, it has long been debated whether FA levels depend upon genetic variability, the particular molecular marker notwithstanding, and whether it is possible to use one or more molecular markers to better understand FA data. The Mantel tests performed in this study showed very interesting correlations between FA and the investigated microsatellites. For the lack of a linkage map for the investigated microsatellite loci, it is presently impossible to establish the relation-ships between the FA parameter and the microsatellite loci that the Mantel test defines as correlated.

Cite this paper
nullL. Lucentini, L. Gigliarelli, A. Palomba, M. Puletti and F. Panara, "Temporal Study of Stress-Induced Effects Caused by Developmental Temperature Changes and Water Quality in an Isolated Northern Pike (Esox lucius L.) Population," Journal of Water Resource and Protection, Vol. 2 No. 2, 2010, pp. 167-180. doi: 10.4236/jwarp.2010.22019.
References
[1]   G. A. Babbitt, “How accurate is the phenotype? - An analysis of developmental noise in a cotton aphid clone,” BMC Developmental Biology, Vol. 8, No. 19, pp. 1–9, February 2008.

[2]   P. Gienapp, C. Teplitsky and J. S. Alho, J. A. Mills, and J. Merila, “Climate change and evolution: disentangling en-vironmental and genetic responses,” Molecular Ecology, Vol. 17, No. 1, pp. 167–178, July 2008.

[3]   A. P. Moller and J. P. Swaddle, “Asymmetry, develop-mental stability, and evolution,” In: Oxford series in ecology and evolution, Oxford University Press, 1997.

[4]   S. Van Dongen, “What do we know about the heritability of developmental instability? Answers from a bayesian model,” Evolution, Vol. 61, No. 5, pp. 1033–1042, May 2007.

[5]   O. P. Moller and J. Manning, “Growth and developmen-tal instability,” Veterinary Journal, Vol. 166, No. 1, pp. 19–27, July 2003.

[6]   R. Palmer and C. Stobeck, “Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distribution and power of statistical test,” Acta Zoologica Fennica, Vol. 191, pp. 57–72, June 1992.

[7]   P. Siikamaki, A. Lammi and K. Mustajarvi, “No rela-tionship between fluctuating asymmetry and fitness in Lychnis viscaria,” Evolutionary Ecology, Vol. 16, No. 6, pp. 567–577, December 2002.

[8]   O. Johnson, K. Neely, and R. Waples, “Lopsided fish in the Snake River Basin – fluctuating asymmetry as a way of assessing impact of hatchery supplementation in chi-nook salmon, Oncorhynchus tshawytscha,” Environ-mental Biology of Fishes, Vol. 69, No. 4, pp. 379-393, March 2004.

[9]   X. Chang, B. Zhai, M. Wang, and B. Wang, “Relation-ship between exposure to an insecticide and fluctuating asymmetry in a damselfly (Odonata, Coenagriidae),” Hy-drobiologia, Vol. 586, No. 1, pp. 213-220, April 2007.

[10]   M. S. Eriksen, A. M. Espmark, T. Poppe, B. O. Braastad, R. Salte, and M. Bakken, “Fluctuating asymmetry in farmed Atlantic salmon (Salmo salar): also a maternal matter?,” Environmental Biology of Fishes, Vol. 81, No. 1, pp. 87-99, January 2008.

[11]   L. Lucentini, M. Lorenzoni, F. Panara, and M. Mearelli, “Effects of short- and long-term thermal stress in perch (Perca fluviatilis L.) determined through fluctuating asymmetry and HSP70 expression,” Italian Journal of Zoology, Vol. 69, No. 1, pp. 13-17, November 2002.

[12]   Sinclair and A. A. Hoffmann, “Developmental stability as a potential tool in the early detection of salinity stress in wheat,” International Journal of Plant Sciences, Vol. 164, No. 2, pp. 325-331, August 2003.

[13]   P. Fey and J.A. Hare, “Fluctuating asymmetry in the oto-liths of larval Atlantic menhaden Brevoortia tyrannus (Latrobe) - a condition indicator?” Journal of Fish Biol-ogy, Vol. 72, No. 1, pp. 121-130, January 2008.

[14]   K. Iguchi, K. Watanabe, and M. Nishid, “Validity of fluctuating asymmetry as a gauge of genetic stress in ayu stocks,” Fisheries Science, Vol. 71, No. 2, March 2005.

[15]   M. Lorenzoni, M. Corboli, A. J. M. D?rr, M. Mearelli, and G. Giovinazzo, “The growth of pike (Esox lucius Linnaeus, 1758) in Lake Trasimeno (Umbria, Italy),” Fisheries Research, Vol. 59, No. 1–2 , pp. 239–246, 2002.

[16]   P. A. Nilsson, C. Skov, and J.M. Farrell, “Current and future directions for pike ecology and management: a summary and synthesis,” Hydrobiologia, Vol. 601, No. 1, pp. 137–141, April 2008.

[17]   L. Lucentini, A. Palomba, L. Gigliarelli, G. Sgaravizzi, C. Ricciolini, M. E. Puletti, H. Lancioni, L. Lanfaloni, and F. Panara, “Northern Pike: A Species In Crisis?” In: Alex-andra M. Columbus and Luke Kuznetsov. Endangered Species: New Research. ISBN: 978-1-60692-241-5, 2009b.

[18]   B. Jacobsen, M. M. Hansen, and V. Loeschcke, “Mi-crosatellite DNA analysis of northern pike (Esox lucius L.): insights into the genetic structure and demographic history of a genetically depauperate species,” Biological Journal of the Linnean Society, Vol. 84, No. 1, pp. 91-101, February 2005.

[19]   S. Launey, F. Krieg, J. Morin, and J. Laroche, “Five new microsatellite markers for northern pike (Esox lucius),” Molecular Ecology Notes, Vol. 3, No. 3, pp. 366–368, September 2003.

[20]   J. C. Nicod, Y. Z. Wang, L. Excoffier, and C. R. Largia-der, “Low levels of mitochondrial DNA variation among central and southern European Esox lucius populations,” Journal of Fish Biology, Vol. 64, No. 5, pp. 1442–1449, April 2004.

[21]   R. Ahas, “Long-term phyto-, ornitho- and ichthyo-phenological time-series analyses in Estonia,” Interna-tional Journal of Biometeorology, Vol. 42, No. 3, pp. 119–123, February 1999.

[22]   J. M. Casselman, E. J. Crossman, P. E. Ihssen, J. D. Reist, and H. E. Booke, “Identification of muskellunge northern pike and their hybrids,” Special Publication of American Fisheries Society, Vol 15, No. 1, pp. 14–46, 1986.

[23]   J. Winfield, J. B. James, and J. M. Fletcher, “Northern pike (Esox lucius) in a warming lake: changes in popula-tion size and individual condition in relation to prey abundance,” Hydrobiologia, Vol. 601, No.1, pp. 29–40, April 2008.

[24]   L. Lucentini, A. Palomba, L. Gigliarelli, H. Lancioni, M. Natali, and F. Panara, “Microsatellite polymorphism in Italian populations of northern pike (Esox lucius L.),” Fisheries Research, Vol. 80, No. 2–3, pp. 251–262, Sep-tember 2006.

[25]   L. Lucentini, A. Palomba, L. Gigliarelli, G. Sgaravizzi, H. Lancioni, L. Lanfaloni, M. Natali, and F. Panara, “Tem-poral changes and effective population size of an Italian isolated and supportive-breeding managed northern pike (Esox lucius) population,” Fisheries Research. Vol. 96, No. 2–3, pp. 139–147, March 2009a.

[26]   L. Lucentini, A. Carosi, R. Erra, G. Giovinazzo, M. Lorenzoni, and M. Mearelli, “Fluctuating asymmetry in Perch (Perca fluviatilis L.) from three lakes of the region Umbria (Italy) as a tool to demonstrate the impact of man-made lakes on developmental stability,” Atti CEI IX, 1997.

[27]   M. J. Servia, F. Cobo, and M. A. González, “Effects of short-term climatic variations on fluctuating asymmetry levels in Chironomus riparius larvae at a polluted site,” Hydrobiologia, Vol. 523, No. 1–3, pp. 137-147, July 2004.

[28]   J. Pither and P. D. Taylor, “Directional and fluctuating asymmetry in the black-winged damselfly Calopteryx maculata (Beauvois) (Odonata: Calopterygidae),” Cana-dian Journal of Zoology, Vol. 78, No. 10, pp. 1740–1748, June 2000.

[29]   S. A. ?xnevad, K. ?stbye, and L. A. V?llestad, “Year class variation in fluctuating asymmetry in perch (Perca fluviatilis L.) from an acidic aluminium-rich lake,” Ecol-ogy of Freshwater Fisheries, Vol.3, pp.131–137, June 1995.

[30]   L. M. Miller and A. R. Kapuscinski, “Microsatellite DNA markers reveal new levels of genetic variation in pike,” Transactions of American Fishery Society, Vol.125, No.6, pp. 971–977, November 1996.

[31]   L. M. Miller and A. R. Kapuscinski, “Historical analysis of genetic variation reveals low effective population size in a northern pike (Esox lucius) population,” Genetics, Vol. 147, No. 3, pp. 1249–1258, November 1997.

[32]   B. S. Weir, and C. C. Cockerham, “Estimating F-statistics for the analysis of population structure,” Evolution, Vol.38, No. 6, pp. 1358–1370, May 1984.

[33]   P. E. Smouse, J. C. Long, and R. R. Sokal, “Multiple regression and correlation extensions of the Mantel test of matrix correspondence,” Systematic Zoology, Vol. 35, No. 4, pp. 627–632, 1986.

[34]   B. Kimmel, W. W. Ballard, S.R. Kimmel, B. Ullmann, and T. Schilling, “Stages of embryonic development of the zebrafish,” Developmental Dynamics, Vol. 203, No. 3, pp. 253–310, July 1995.

[35]   J. D. Shardo, “Comparative embryology of teleostean fishes. I. Development and staging of the American Shad, Alosa sapidissima (Willson, 1811),” Journal of Mor-phology, Vol. 225, No.2, pp. 125–167, February 1995.

[36]   R. F. Leary, F. W. Allendorf, and K. L. Knudsen, “Ge-netic, environmental, and developmental causes of meris-tic variation in rainbow trout,” Acta Zoologica Fennica, Vol. 191, pp. 79–95, 1992.

[37]   J. W. Chapman and D. Goulson, “Environmental versus genetic influences on fluctuating asymmetry in the house fly, Musca domestica,” Biological Journal of the Linnean Society, Vol. 70, No. 3, pp. 403–413, July 1998.

[38]   W. B. Campbell, J. M. Emlen, and W. K. Hershberger, “Thermally induced chronic developmental stress in coho salmon: integrating measures of mortality, early growth, and developmental instability,” Oikos, Vol. 81, No. 2, pp. 398–410, January 1998.

[39]   W. L. Seddon, “Mechanisms of temperature acclimation in the channel catfish Ictalarus punctatus: isozymes and quantitative changes,” Comparative Biochemistry and Physiology, Vol. 118, No.3, pp. 813–820, November 1997.

[40]   S. Watabe, J. Imai, M. Nakaya, Y. Hirayama, Y. Oka-moto, H. Masaki, T. Uozumi, I. Hirono, and T. Aoki, “Temperature acclimation induces light meromyosin iso-forms with different primary structures in carp fast skele-tal muscle,” Biochemical and Biophysical Research Communications, Vol. 208, No. 1, pp. 118–25, March 1995.

[41]   S. Prentice, A. P. Jobes, and G. Burness, “Fault bars and fluctuating asymmetry in birds: are the two measures correlated?,” Journal of Field Ornithology, Vol. 79, No. 1, pp. 58–63, March 2008.

[42]   V. L. Vershinin, E.A. Gileva, and N.V. Glotov, “Fluctu-ating asymmetry of measurable parameters in Rana ar-valis,” Russian Journal of Ecology, Vol. 38, No. 1, pp. 72–74, February 2007.

[43]   E. Zachos, G. B. Hartl, and F. Suchentrunk, “Fluctuating asymmetry and genetic variability in the roe deer (Capreolus capreolus): a test of the developmental stabil-ity hypothesis in mammals using neutral molecular markers,” Heredity, Vol. 98: pp. 392–400, March 2007.

[44]   A. Savage and P. J. Hogarth, “An analysis of tempera-ture-induced fluctuating asymmetry in Asellus aquati-cus,” Hydrobiologia, Vol. 411, No. 0, September 1999.

[45]   M. Mpho, A. Callaghan, and G. J. Holloway, “Tempera-ture and genotypic effects on life history and fluctuating asymmetry in a field strain of Culex pipiens,” Heredity, Vol. 88, No. 4, pp. 307-312, November 2002.

[46]   W. E. Bradshaw and C. M. Holzapfel, “Genetic response to rapid climate change: It’s seasonal timing that mat-ters,” Molecular Ecology, Vol. 17, No. 1, pp. 157–166, September 2008.

[47]   J. G. Wiener and P. J. Rago, “A test of fluctuating asym-metry in Bluegills (Lepomis macrochirus Rafinesque) as a measure of pH-related stress,” Environmental Pollution, Vol. 44, No. 1, pp. 27–36, June 1987.

[48]   L. Laikre, L. M. Miller, A. Palmé, S. Palm, A.R. Kapus-cinski, G. Thoresson, and N. Ryman, “Spatial genetic structure of northern pike (Esox lucius) in the Baltic Sea,” Molecular Ecology, Vol. 14, No.7, pp. 1955–1964, May 2005.

[49]   A. J. P. Raat, “Synopsis of biological data on the northern pike, Esox lucius Linnaeus, 1758,” FAO Fisheries Syn-opsis, No. 30, rev. 2, p. 178, 19.

 
 
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