Embryonic development of lake whitefish Coregonus clupeaformis: A staging series, analysis of growth and effects of fixation

Journal of Fish Biology

Volumn 87, Issue 3, 2015, Pages 539-558

  Sreetharan, S ^a   Thome, C ^a   Mitz, C ^a   Eme, J ^a   Mueller, C A ^a   Hulley, E N ^a   Manzon, R G ^b   Somers, C M ^b   Boreham, D R ^a,c   Wilson, J Y ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF REGINA   (Canada)

^c NORTHERN ONTARIO SCHOOL OF MEDICINE   (Canada)

Author keywords

Coregonid; Embryo; Fixative; Morphology; Teleost

Indexed keywords

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL EMBRYO; BLASTODERM; EMBRYO DEVELOPMENT; EMBRYOLOGY; FERTILIZATION; GROWTH, DEVELOPMENT AND AGING; OOCYTE; SALMONID;

ANIMALS; BLASTODERM; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FERTILIZATION; OVUM; SALMONIDAE;

EID: 84940602450     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/jfb.12725     Document Type: Article

References (42)

1. Battle, H. I. (1944). The embryology of the Atlantic salmon (Salmo salar Linnaeus). Canadian Journal of Research 22, 105-125. doi: 10.1139/cjr44d-008
2. Blaxter, J. H. S. (1969). Development: eggs and larvae. In Fish Physiology, Vol. III (Hoar, W. S. & Randall, D. J., eds), pp. 177-252. New York, NY: Academic Press.
3. Broadie, K. S., Bate, M. & Tublitz, N. J. (1991). Quantitative staging of embryonic development of the tobacco hawkmoth, Manduca sexta. Roux's Archives of Developmental Biology 199, 327-334. doi: 10.1007/BF01705925
4. Brooke, L. T. (1975). Effect of Different Constant incubation temperatures on egg survival and embryonic development in lake whitefish (Coregonus clupeaformis). Transactions of the American Fisheries Society 104, 555-559. doi: 10.1577/1548-8659
5. Colby, P. J. & Brooke, L. T. (1973). Effects of temperature on embryonic development of lake herring (Coregonus artedii). Journal of the Fisheries Board of Canada 30, 799-810. doi: 10.1139/f73-135
6. Cooke, S. J. & Schreer, J. F. (2001). Additive effects of chlorinated biocides and water temperature on fish in thermal effluents with emphasis on the Great Lakes. Reviews in Fisheries Science 9, 69-113. doi: 10.1080/20016491101717
7. Coulombre, A. J. (1961). Cytology of the developing eye. International Review of Cytology 11, 161-194.
8. Coulombre, A. J. (1965). The eye. In Organogenesis (DeHaan, R. L. & Ursprung, H., eds), pp. 219-251. New York, NY: Holt, Rinehart, Winston.
9. Ficke, A. D., Myrick, C. A. & Hansen, L. J. (2007). Potential impacts of global climate change on freshwater fisheries. Reviews in Fish Biology and Fisheries 17, 581-613. doi: 10.1007/s11160-007-9059-5
10. Garside, E. T. (1966). Developmental rate and vertebral number in salmonids. Journal of the Fisheries Board of Canada 23, 1537-1551. doi: 10.1139/f66-143
11. Gaston, G. R., Bartlett, J. H. & McAllister, A. P. (1996). Biomass variations of estuarine macrobenthos preserved in ethanol and formalin. Estuaries 19, 674-679. doi: 10.2307/1352527
12. Gorodilov, Y. N. (1996). Description of the early ontogeny of the Atlantic salmon, Salmo salar, with a novel system of interval (state) identification. Environmental Biology of Fishes 47, 109-127. doi: 10.1007/BF00005034
13. Hart, J. L. (1931). The spawning and early life history of the whitefish, Coregonus clupeaformis (Mitchill), in the Bay of Quinte, Ontario. Contributions to Canadian Biology and Fisheries 6, 165-214. doi: 10.1139/f31-007
14. Heyland, A. & Hodin, J. (2014). A detailed staging scheme for late larval development in Strongylocentrotus purpuratus focused on readily-visible juvenile structures within the rudiment. BMC Developmental Biology 14, 22. doi: 10.1186/1471-213X-14-22
15. Jennings, S. (1991). The effects of capture, net retention and preservation upon lengths of larval and juvenile bass, Discentrarchus labrax (L.). Journal of Fish Biology 38, 349-357. doi: 10.1111/j.1095-8649.1991.tb03125.x
16. Johansen, A. C. & Krogh, A. (1914). The influence of temperature and certain other factors upon the rate of development of the eggs of fishes. Journal du Conseil international pour l'Exploration de la Mer 1, 1-43.
17. Johnson, P. O. & Fay, L. C. (1950). The Johnson-Neyman technique, its theory and application. Psychometrika 15, 349-367. doi: 10.1007/BF02288864
18. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. & Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Developmental Dynamics 203, 253-310. doi: 10.1002/aja.1002030302
19. Kinne, O. & Kinne, E. M. (1962). Rates of development in embryos of a cyprinodont fish exposed to different temperature-salinity-oxygen combinations. Canadian Journal of Zoology 40, 231-253. doi: 10.1139/z62-025
20. Kohno, H., Hara, S. & Taki, Y. (1986). Early larval development of the seabass Lates calcarifer with emphasis on the transition of energy sources. Nippon Suisan Gakkaishi 52, 1719-1725.
21. Krogh, A. (1914). The quantitative relation between temperature and standard metabolism in animals. Zeitschrift für Physikalische Chemie Biologie 1, 491-508.
22. Kunz, Y. W. (2004). Development of the eye. In Developmental Biology of Teleost Fishes (Noakes, D. L. G., ed.), pp. 303-359. Dordrecht: Springer.
23. Lönning, S., Kjörsvik, E. & Davenport, J. (1984). The hardening process of the egg chorion of the cod, Gadus morhua L., and lumpsucker, Cyclopterus lumpus L. Journal of Fish Biology 24, 505-522. doi: 10.1111/j.1095-8649.1984.tb04821.x
24. Lukšiene, D., Sandström, O., Lounasheimo, L. & Andersson, J. (2000). The effects of thermal effluent exposure on the gametogenesis of female fish. Journal of Fish Biology 56, 37-50. doi: 10.1111/j.1095-8649.2000.tb02085.x
25. Mabee, P. M., Aldridge, E., Warren, E. & Helenurm, K. (1998). Effect of clearing and staining on fish length. Copeia 1998, 346-353. doi: 10.2307/1447428
26. Melo, M. T., Saturnino, C., Santos, J. N. S., Vasconcellos, R. M., Cruz-Filho, A. G. & Araujo, F. G. (2010). Correction of the weight and length for juveniles Atherinella brasilliensis (Actinopterygii: Atherinopsidae) after fixation in formalin and preservation in ethanol. Zoologia 27, 892-896. doi: 10.1590/S1984-46702010000600009
27. Mitz, C., Thome, C., Cybulski, M. E., Laframboise, L., Somers, C. M., Manzon, R. G., Wilson, J. Y. & Boreham, D. R. (2014). A self-contained hatchery system for rearing lake Whitefish embryos for experimental aquaculture. North American Journal of Aquaculture 76, 179-184. doi: 10.1080/15222055.2014.893472
28. Parichy, D. M., Elizondo, M. R., Mills, M. G., Gordon, T. N. & Engeszer, R. E. (2009). Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Developmental Dynamics 238, 2975-3015. doi: 10.1002/dvdy.22113
29. Parker, R. R. (1963). Effects of formalin on length and mass of fishes. Journal of the Fisheries Research Board of Canada 20, 1441-1455. doi: 10.1139/f63-098
30. Price, J. W. (1934a). The embryology of the whitefish, Coregonus clupeaformis (Mitchill). Part I. The Ohio Journal of Science 34, 287-305.
31. Price, J. W. (1934b). The Embryology of the Whitefish Coregonus clupeaformis (Mitchill). Part II. Organogenesis. The Ohio Journal of Science 34, 399-414.
32. Price, J. W. (1935). The embryology of the whitefish Coregonus clupeaformis (Mitchill). Part III. The second half of the incubation period. The Ohio Journal of Science 35, 40-53.
33. Price, J. W. (1940). Time-temperature relations in the incubation of the whitefish, Coregonus clupeaformis (Mitchill). The Journal of General Physiology 23, 449-468. doi: 10.1085/jgp.23.4.449
34. Rajagopal, P. K. (1979). The embryonic development and the thermal effects on the development of the mountain whitefish, Prosopium williamsoni (Girard). Journal of Fish Biology 15, 153-158. doi: 10.1111/j.1095-8649.1979.tb03578.x
35. Rønnestad, I., Koven, W. M., Tandler, A., Harel, M. & Fyhn, H. J. (1994). Energy metabolism during development of eggs and larvae of gilthead sea bream (Sparus aurata). Marine Biology 120, 187-196. doi: 10.1007/BF00349678
36. Santos, J. N., Araújo, F. G. & Wilva, D. S. (2009). Length correction for early-juvenile Brazilian herring Sardinella janeiro (Eigenmann, 1984) after preservation in formalin, ethanol and freezing. Neotropical Ichthyology 7, 87-92. doi: 10.1590/S1679-62252009000100011
37. Shields, P. A. & Carlson, S. R. (1996). Effects of formalin and alcohol preservation on lengths and weights of juvenile sockeye salmon. Alaska Fishery Research Bulletin 3, 81-93.
38. Smith, B. B. & Walker, K. F. (2003). Shrinkage of 0+ carp (Cyprinus carpio L.) after preservation in ethanol. Marine and Freshwater Research 54, 113-116. doi: 10.1071/MF02089
39. Vergara-Solana, F. J., Garcia-Rodriguez, F. J. & Cruz-Aguero, J. (2014). Effect of preservation procedures on the body shape of the golden mojarra, Diapterus aureolus (Actinoptyerygii: Perciformes: Gerreidae) and its repercussions in a taxonomic study. Acta Ichthyologica et Piscatoria 44, 65-70.
40. Vernier, J. M. (1969). Chronological table of the embryonic development of rainbow trout, Salmo gairdneri Rich. 1836. Annals of Embryology and Morphology 2, 495-520 (Fisheries and Marine Service Translation Series No. 3913).
41. Wallich, C. (1901). A method of recording egg development for use of fish-culturists. Report of the U.S. Fish Commissioners for 1900, pp. 185-194. Washington, DC: Government Printing Office.
42. Yamamoto, T. O. (1961). Physiology of fertilization in fish eggs. International Review of Cytology 12, 361-405. doi: 10.1016/S0074-7696(08)60545-8