Embryonic staging series for the beach spawning, terrestrially incubating California grunion Leuresthes tenuiswith comparisons to other Atherinomorpha

Journal of Fish Biology

Volumn 75, Issue 1, 2009, Pages 17-38

  Martin, K L ^a   Moravek, C L ^a   Flannery, J A ^a,b  

^a PEPPERDINE UNIVERSITY   (United States)

^b CHILDREN S HOSPITAL COLORADO   (United States)

Author keywords

Delayed hatching; Development; Early life stages; Heterochrony; Teleost

Indexed keywords

ANIMAL; ANIMAL EMBRYO; ARTICLE; CYTOLOGY; EMBRYO DEVELOPMENT; OOCYTE; ORGANOGENESIS; PRENATAL DEVELOPMENT; SMEGMAMORPHA; SWIMMING; TIME; ZYGOTE;

ANIMALS; BATHING BEACHES; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; ORGANOGENESIS; OVUM; SMEGMAMORPHA; TIME FACTORS; ZYGOTE;

ATHERINOMORPHA; BELONIFORMES; CYPRINODONTIFORMES; LEURESTHES; LEURESTHES TENUIS; PISCES; TELEOSTEI;

EID: 68949147696     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2009.02260.x     Document Type: Article

References (55)

1. Arezo, M. J., Pereiro, L. & Berois, N. (2005). Early development in the annual fish Cynolebias viarius. Journal of Fish Biology 66, 1357 1370. doi: 10.1111/j.1095-8649.2005.00688.x (Pubitemid 40707849)
2. Armstrong, P. B. & Child, J. S. (1965). Stages in the normal development of Fundulus heteroclitus. Biological Bulletin 128, 143 168.
3. Bemis, W. E. & Grande, L. (1992). Early development of the actinopterygian head. I. External development and staging of the paddlefish Polyodon spathula. Journal of Morphology 213, 47 83.
4. Collazo, A., Bolker, J. A. & Keller, R. (1994). A phylogenetic perspective on teleost gastrulation. American Naturalist 144, 133 152.
5. Darken, R. S., Martin, K. L. M. & Fischer, M. C. (1998). Metabolism during delayed hatching in terrestrial eggs of a marine fish, the grunion Leuresthes tenuis. Physiological Zoology 71, 400 406.
6. David, L. R. (1939). Embryonic and early larval stages of the grunion, Leuresthes tenuis, and of the sculpin, Scorpaena guttata. Copeia 2, 75 81.
7. DiMichele, L. & Taylor, M. (1980). The environmental control of hatching in Fundulus heteroclitus. Journal of Experimental Zoology 217, 181 187.
8. DiMichele, L. & Westerman, M. E. (1997). Geographic variation in development rate between populations of the teleost Fundulus heteroclitus. Marine Biology 128, 1 7.
9. Ehrlich, K. F. & Farris, D. A. (1972). Some influences of temperature on the development of the grunion Leuresthes tenuis, an Atherine fish. Marine Biology 12, 267 271.
10. Fujimoto, T., Kataoka, T., Sakao, S., Saito, T., Yamaha, E. & Arai K. (2006). Developmental stages and germ cell lineage of the loach (Misgurnus anguillicaudatus). Zoological Science 23, 977 989.
11. Fujimura, K. & Okada, H. (2007). Development of the embryo, larva and early juvenile of Nile tilapia Oreochromis niloticus (Pisces: Cichlidae). Developmental staging system. Development, Growth and Differentiation 49, 310 324.
12. Greeley, M. S., Jr. 1984). Spawning by Fundulus pulverous and Adinia xenica (Cyprinodontidae) along the Alabama coast associated with semilunar tidal cycles. Copeia 1984, 797 800.
13. Greeley, M. S., Jr. & MacGregor, R. M. III. 1983). Annual and semilunar reproductive cycles of the gulf killifish, Fundulus grandis, on the Alabama gulf coast. Copeia 1983, 711 718.
14. Greeley, M. S., Jr., Marion, K. R. & MacGregor, R. III. 1986). Semilunar spawning cycles of Fundulus similis (Cyprinodontidae). Environmental Biology of Fishes 17, 125 131.
15. Gregory, P. A. (2001). Grunion. In California's Living Marine Resources: A Status Report, (Leet, W. S., Dewees, C. M., Klingbeill, R. & Larson, E. J., eds), pp. 246 247. Sacramento, CA : California Department of Fish and Game.
16. Griem, J. N. & Martin, K. L. M. (2000). Wave action: the environmental trigger for hatching in the California grunion Leuresthes tenuis. Marine Biology 137, 177 181.
17. Hall, T. E., Smith, P. & Johnston, I. A. (2004). Stages of embryonic development in the Atlantic cod Gadus morhua. Journal of Morphology 259, 255 270.
18. Harrington, R. W., Jr. 1959). Delayed hatching in stranded eggs of marsh killifish, Fundulus confluentes. Ecology 40, 430 437.
19. Haynes, J. L. (1995). Standardized classification of poeciliid development for life-history studies. Copeia 1995, 147 154.
20. Helvik, J. V. & Walther, B. T. (1993). Development of hatchability in halibut (Hippoglossus hippoglossus) embryos. International Journal of Developmental Biology 37, 487 490.
21. Hill, J. & Johnston, I. A. (1997). Photomicrographic atlas of Atlantic herring embryonic development. Journal of Fish Biology 51, 960 977. doi:10.1111/ j.1095-8649.1997.tb01535.x (Pubitemid 27503127)
22. Horn, M. H., Allen, L. G. & Lea, R. N. (2006). Biogeography. In The Ecology of Marine Fishes: California and Adjacent Waters (Allen, L., Horn, M. & Pondella, D. eds), pp. 3 25. Berkeley, CA : University of California Press.
23. Hubbs, C. (1965). Developmental temperature tolerance and rates of four southern California fishes, Fundulus parvipinnis, Atherinops affinis, Leuresthes tenius, and Hypsoblennius sp. California Fish and Game 51, 113 122.
24. Iwamatsu, T. (2004). Stages of normal development in the medaka Oryzias latipes. Mechanisms of Development 121, 605 618.
25. Johnson, P. B., Martin, K. L., Vandergon, T. L., Honeycutt, R. L., Burton, R. & Fry, A. (2009). Microsatellite and mitochondrial genetic comparisons between northern and southern populations of California grunion (Leuresthes tenuis). Copeia 2009, 467 476.
26. Jordaan, A., Hayhurst, S. E. & Kling, L. J. (2006). The influence of temperature on the stage at hatch of laboratory reared Gadus morhua and implications for comparisons of length and morphology. Journal of Fish Biology 68, 7 24. doi: 10.111/j.0022-1112.2006.00857x
27. 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.
28. Martin, K. L. M. (1999). Ready and waiting: delayed hatching and extended incubation of anamniotic vertebrate terrestrial eggs. American Zoologist 39, 279 288.
29. Martin, K. L. M. & Swiderski, D. L. (2001). Beach spawning in fishes: phylogenetic tests of hypotheses. American Zoologist 41, 526 537.
30. Martin, K. L. M., Van Winkle, C. R., Drais, J. E. & Lakisic, H. (2004). Beach spawning fishes, terrestrial eggs, and air breathing. Physiological and Biochemical Zoology 77, 750 759.
31. Martinez, G. M. & Bolker, J. A. (2003). Embryonic and larval staging of summer flounder (Paralichthys dentatus). Journal of Morphology 255, 162 176. doi: 10.1002/jmor.10053 (Pubitemid 36137505)
32. Metscher, B. D. & Ahlberg, P. E. (1999). Zebrafish in context: uses of a laboratory model in comparative studies. Developmental Biology 210, 1 14.
33. Middaugh, D. P. & Lempesis, P. W. (1976). Laboratory spawning and rearing of a marine fish, the silverside Menidia menidia menidia. Marine Biology 35, 295 300. doi: 10.1007/BF00386640
34. Miller, D. J. & Lea, R. N. (1972). Guide to the Coastal Marine Fishes of California. Sacramento, CA : California Department of Fish and Game.
35. Moffatt, N. M. & Thomson, D. A. (1978). Tidal influence on the evolution of egg size in the grunions Leuresthes, Atherinidae). Environmental Biology of Fishes 3, 267 273.
36. Nelson, J. S. (2006). Fishes of the World, 4th edn. Hoboken, NJ : John Wiley & Sons.
37. Palmer, C. J. & Cully, M. B. (1984). The egg and early life stages of the sandsmelt, Atherina presbyter Cuvier. Journal of Fish Biology 24, 537 544. doi:10.1111/ j.1095-8649.1984.tb04824.x
38. Parenti, L. R. (1981). A phylogenetic and biogeographic analysis of Cyprinodontiform fishes (Teleostei, Atherinomorpha). Bulletin of the American Museum of Natural History 168, 335 557.
39. Parenti, L. R. (2005). The phylogeny of atherinomorphs: evolution of a novel fish reproductive system. In Viviparous Fishes (Uribe, M. C. & Grier, H. J. eds), pp. 13 30. Homestead, FL : New Life Publications.
40. Richardson, M. K., Hanken, J. Gooneratne, M. L., Pieau, C., Raynaud, A., Selwood, L. & Wright, G. M. (1997). There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anatomy and Embryology 196, 91 106. doi: 10.1007/s004290050082 (Pubitemid 27393854)
41. Roberts, D., Lea, R. N. & Martin, K. L. M. (2007). First record of the occurrence of the California grunion, Leuresthes tenuis, in Tomales Bay, California; a northern extension of the species. California Fish and Game 93, 107 110.
42. Rosen, D. E. & Parenti, L. R. (1981). Relationships of Oryzias, and the groups of atherinomorph fishes. American Museum Novitates 2719, 1 25.
43. Setiamarga, D. H. E., Miya, M. Yamanoue, Y., Mabuchi, K., Satoh, T. P., Inoue, J. G. & Nishida, M. (2008). Interrelationships of Atherinomorpha (medakas, flyingfishes, killifishes, silversides, and their relatives): the first evidence based on whole mitogenome sequences. Molecular Phylogenetics and Evolution 49, 598 695. doi: 10.1016/j.ympev.2008.08.008
44. Shardo, J. D. (1995). Comparative embryology of teleostean fishes. I. Development and staging of the American shad, Alosa sapidissima (Wilson, 1811). Journal of Morphology 225, 125 167.
45. Smyder, E. A. & Martin, K. L. M. (2002). Temperature effects on egg survival and hatching during the extended incubation period of California grunion, Leuresthes tenuis. Copeia 2002, 313 320.
46. Speer Blank, T. M. & Martin, K. L. M. (2004). Hatching events in the California grunion, Leuresthes tenuis. Copeia 2004, 21 27.
47. Taylor, M. H. (1999). A suite of adaptations for intertidal spawning. American Zoologist 39, 313 320.
48. Walker, B. W. (1952). A guide to the grunion. California Fish and Game 38, 409 420.
49. White, B. N., Lavenberg, R. J. & McGowen, G. E. (1983). Atheriniformes: development and relationships. In Ontogeny and Systematics of Fishes (Moser, H. G., Richards, W. J Cohen, D. M. Fahay, M. P Kendall, Jr. A. W. & Richardson, S. L. eds), pp. 355 362. Lawrence, KS : University of Kansas Press.
50. Wourms, J. P. (1964). Comparative observations on the early embryology of Nothobranchus taeniopygus (Hilgendorf) and Aplocheilichthys pumilis (Boulenger) with special reference to the problem of naturally occurring embryonic diapauses in teleost fishes. Annual Report East African Freshwater Fisheries Institute 1964, 68 73.
51. Yamagami, K. (1988). Mechanisms of hatching in fish. In Fish Physiology Vol. 11 A. (Hoar, W. S. & Randall, D. J. eds), pp. 447 499. San Diego, CA : Academic Press.
52. Yamahira, K. (1996). The role of intertidal egg deposition on survival of the puffer, Takifugu niphobles (Jordan et Snyder), embryos. Journal of Experimental Marine Biology and Ecology 198, 291 306.
53. Yamahira, K. & Conover, D. (2002). Intra- vs. interspecific latitudinal variation in growth: adaptation to temperature or seasonality? Ecology 83, 1252 1262.
54. Yamahira, K. & Conover, D. O. (2003). Interpopulation variability in temperature-dependent sex determination of the Tidewater Silverside Menidia peninsulae (Pisces: Atherinidae). Copeia 1, 155 159.
55. Yamahira, K., Kawajiri, M., Takeshi, K., & Irie, T. (2007). Inter- and intrapopulation variation in thermal reaction norms for growth rate: evolution of latitudinal compensation in ectotherms with a genetic constraint. Evolution 61, 1577 1589.