Desiccation Resistance in Embryos of the Killifish, Fundulus heteroclitus: Single Embryo Measurements

Journal of Experimental Zoology Part A: Ecological Genetics and Physiology

Volumn 319, Issue 4, 2013, Pages 179-201

  Chuaypanang, Sirilak ^a   Kidder, George W ^b   Preston, Robert L ^a,b  

^a ILLINOIS STATE UNIVERSITY   (United States)

^b MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

WATER;

ANIMAL; ANIMAL EMBRYO; ARTICLE; DESICCATION; EMBRYO DEVELOPMENT; FERTILIZATION; KILLIFISH; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; DESICCATION; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FERTILIZATION; KILLIFISHES; WATER;

CYPRINODONTIFORMES; CYPRINODONTOIDEI; FUNDULUS HETEROCLITUS;

EID: 84875916505     PISSN: 19325223     EISSN: 19325231     Source Type: Journal    
DOI: 10.1002/jez.1783     Document Type: Article

References (93)

1. Able KW. 2002. Killifishes: family Fundulidae. In: Collette BB, Klein-MacPhee G, editors. Bigelow and Schroeder's fishes of the Gulf of Maine. 3rd edition. Washington, DC: Smithsonian Institution Press. p 292-297.
2. Able KW, Felley JD. 1986. Geographical variation in Fundulus heteroclitus: tests for concordance between egg and adult morphologies. Am Zool 26:145-157.
3. Armstrong PB, Child JS. 1965. Stages in the normal development of Fundulus heteroclitus. Biol Bull 128:143-168.
4. Atz JW. 1986. History of Fundulus in the laboratory. Am Zool 26:111-120.
5. Baldwin JL, Goldsmith CE, Petersen CW, Preston RL, Kidder GW. 2004. Synchronous hatching in Fundulus heteroclitus embryos: production and properties. Bull Mt Desert I Biol Lab 43:110-111.
6. Baldwin JL, Petersen CW, Preston RL, Kidder GW. 2006. Aerobic and submerged development of embryos of Fundulus heteroclitus. Bull Mt Desert I Biol Lab 45:45-46.
7. Bigelow HB, Schroeder WC. 1953. Fishes of the Gulf of Maine. Fish Bull US 53:1-577.
8. Brummett AR, Dumont JN. 1981. A comparison of chorions from eggs of northern and southern populations of Fundulus heteroclitus. Copeia 3:607-614.
9. Bulger AJ. 1984. A daily rhythm in heat tolerance in salt marsh fish. J Exp Zool 230:11-15.
10. Bulger AJ, Tremaine SC. 1985. Magnitude of seasonal effects on heat tolerance in Fundulus heteroclitus. Physiol Zool 58:197-204.
11. Burnett KG, Bain LJ, Baldwin WS, et al. 2007. Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comp Biochem Physiol Part D Genomics Proteomics 2:257-286.
12. Choe KP, Strange K. 2009. Volume regulation and osmosensing in animal cells. In: Evans DH, editor. Osmotic and ionic regulation. Boca Raton, FL: CRC Press. p 37-67.
13. Cohen SP, Strathmann RR. 1996. Embryos at the edge of tolerance: effects of environment and structure of egg masses on supply of oxygen to embryos. Biol Bull 190:8-15.
14. Conway EJ, Byrne A. 1933. LXI. An absorption apparatus for the micro-determination of certain volatile substances. I. The micro-determination of ammonia. Biochem J 27:419-429.
15. Crawford DL, Powers DA. 1989a. Molecular adaptation to the thermal environment: the role of physiological and biochemical mechanisms. UCLA Symp Mol Cell Biol 122:213-222.
16. Crawford DL, Powers DA. 1989b. Molecular basis of evolutionary adaptation at the lactate dehydrogenase-B locus in the fish Fundulus heteroclitus. Proc Natl Acad Sci USA 86:9365-9369.
17. Crawford DL, Powers DA. 1992. Evolutionary adaptation to different thermal environments by transcriptional regulation. Mol Biol Evol 9:806-813.
18. Davenport J, Lønning S, Kjørsvik E. 1981. Osmotic and structural changes during early development of eggs and larvae of the cod, Gadus morhua L. J Fish Biol 19:317-331.
19. DiMichele L, Powers DA. 1984. Developmental and oxygen consumption rate differences between lactate dehydrogenase B genotypes of Fundulus heteroclitus and their effect on hatching time. Physiol Zool 57:52-56.
20. DiMichele L, Taylor MH. 1980. The environmental control of hatching in Fundulus heteroclitus. J Exp Zool 214:181-187.
21. DiMichele L, Westerman ME. 1997. Geographic variation in development rate between populations of the teleost Fundulus heteroclitus. Mar Biol 128:1-7.
22. DiMichele L, DiMichele JA, Powers DA. 1986. Developmental and physiological consequences of genetic variation at enzyme synthesizing loci in Fundulus heteroclitus. Am Zool 26:201-210.
23. Dumont JN, Brummett AR. 1980. The vitelline envelope, chorion, and micropyle of Fundulus heteroclitus eggs. Gamete Res 3:25-44.
24. Dunham PB, Cass A, Trinkaus JP, Bennett MVL. 1970. Water permeability of Fundulus eggs. Biol Bull Mar Biol Lab Woods Hole 139:420-421.
25. Eddy FB. 1974. Osmotic properties of the perivitelline fluid and some properties of the chorion of Atlantic salmon eggs (Salmo salar). J Zool 174:237-243.
26. Fangue NA, Hofmeister M, Schulte PM. 2006. Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J Exp Biol 209:2859-2872.
27. Fettiplace R, Haydon DA. 1980. Water permeability of lipid membranes. Physiol Rev 60:511-550.
28. Genz J, Grosell M. 2011. Fundulus heteroclitus acutely transferred from seawater to high salinity require few adjustments to intestinal transport associated with osmoregulation. Comp Biochem Physiol 160A:156-165.
29. Gray J. 1932. The osmotic properties of the eggs of the trout (Salmo fario). J Exp Biol 9:277-299.
30. Greenspan L. 1977. Humidity fixed points of binary saturated aqueous solutions. Res Nat Bureau Stand 81A:89-96.
31. Greytak SR, Champlin D, Callard GV. 2005. Isolation and characterization of two cytochrome P450 aromatase forms in killifish (Fundulus heteroclitus): differential expression in fish from polluted and unpolluted environments. Aquat Toxicol 71:371-389.
32. Griffith RW. 1974. Environmental and salinity tolerance in the genus Fundulus. Copeia 1974:319-331.
33. Guggino WB. 1980a. Water balance in embryos of Fundulus heteroclitus and F. bermudae in seawater. Am J Physiol 238:R36-R41.
34. Guggino WB. 1980b. Salt balance in embryos of Fundulus heteroclitus and F. bermudae adapted to seawater. Am J Physiol 238:R42-R49.
35. Hisaoka KK. 1958. The effects of 2-acetylaminofluorene on the embryonic development of the zebrafish. 1. Morphological studies. Cancer Res 18:527-535.
36. Hoffmann EK, Lambert IH, Pedersen SF. 2009. Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193-277.
37. Hølleland T, Fyhn HJ. 1986. Osmotic properties of the eggs of the herring Clupea harengus L. Mar Biol 91:377-383.
38. Hsiao SM, Greeley MS, Wallace RA. 1994. Reproductive cycling in female Fundulus heteroclitus. Biol Bull 186:271-284.
39. Kidder GW. 1998. Plasma osmolarity in the killifish, Fundulus heteroclitus. Bull Mt Desert I Biol Lab 37:79.
40. Kidder GW III, Petersen CW, Preston RL. 2006a. Energetics of osmoregulation: I. Oxygen consumption by Fundulus heteroclitus. J Exp Zool 305A:309-317.
41. Kidder GW III, Petersen CW, Preston RL. 2006b. Energetics of osmoregulation: II. Water flux and osmoregulatory work in the euryhaline fish, Fundulus heteroclitus. J Exp Zool 305A:318-327.
42. 2O. J Exp Biol 14:35-37.
43. Krylov AV, Pohl P, Zeidel ML, Hill WG. 2001. Water permeability of asymmetric planar lipid bilayers: leaflets of different composition offer independent and additive resistances to permeation. J Gen Physiol 118:333-340.
44. Kudo S. 1991. Fertilization, cortical reaction, polyspermy-preventing and antimicrobial mechanisms in fish eggs. Bull Inst Zool Acad Sci Monog 16:313-340.
45. Kudo S. 1992. Enzymatic basis for protection of fish embryos by the fertilization envelope. Experientia 4B:277-281.
46. Laale HW. 1980. The perivitelline space and egg envelopes of bony fishes: a review. Copeia 2:210-226.
47. Langeland J, Kimmel CB. 1997. The embryology of fish. In: Gilbert SF, Raunio AM, editors. Embryology: constructing the organism. Sunderland, MA: Sinauer Associates. p 383-407.
48. Loeffler CA, Løvtrup S. 1970. Water balance in the salmon egg. J Exp Biol 52:291-298.
49. Lønning S, Kjorsvik E, Davenport J. 1984. The hardening process of the egg chorion of the cod, Gadus morhua L., and lumpsucker, Cyclopterus lumpus L. J Fish Biol 24:505-522.
50. Mangor-Jensen A. 1987. Water balance in developing eggs of the cod Gadus morhua. Fish Phys and Bioc 3:17-24.
51. Mangor-Jensen A, Waiwood KG, Peterson RH. 1993. Water balance in eggs of striped bass (Morone saxatilis). J Fish Biol 43:345-353.
52. Marshall AV, Preston RL. 2011. Predation of killifish embryos by adult killifish (Fundulus heteroclitus). Bull Mt Desert I Biol Lab 50:48.
53. Marshall WS, Emberley TR, Singe TD, Bryson SE, McCormick SD. 1999. Time course of salinity adaptation in a strongly euryhaline estuarine teleost, Fundulus heteroclitus: a multivariable approach. J Exp Biol 202:1535-1544.
54. Meyer JN, Di Giulio RT. 2003. Heritable adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecol Appl 13:490-503.
55. Mitton JB, Koehn RK. 1975. Genetic organization and adaptive response of allozymes to ecological variables in Fundulus heteroclitus. Genetics 79:97-111.
56. Morgan TH, Stockard CR. 1907. The effects of salts and sugar solutions on the development of the Frog's egg. Biol Bull I 3:272-279.
57. Morin RP, Able KW. 1983. Patterns of geographic variation in the egg morphology of the fundulid fish, Fundulus heteroclitus. Copeia 1983:726-740.
58. Nacci DE, Coiro L, Champlin D, et al. 1999. Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar Biol 134:9-17.
59. Nacci DE, Champlin D, Coiro L, McKinney R, Jayaraman S. 2002. Predicting the occurrence of genetic adaptation to dioxinlike compounds in populations of the estuarine fish Fundulus heteroclitus. Environ Toxicol Chem 21:1525-1532.
60. Oleksiak MF, Churchill GA, Crawford DL. 2002. Variation in gene expression within and among natural populations. Nat Genet 32:261-266.
61. Ollivier H, Pichavant K, Puill-Stephan E, et al. 2006. Volume regulation following hyposmotic shock in isolated turbot (Scophthalmus maximus) hepatocytes. J Comp Physiol B 176:393-403.
62. Petersen CW, Salinas S, Preston RL, Kidder GW III. 2010. Spawning periodicity and reproductive behavior of Fundulus heteroclitus in a New England Salt Marsh. Copeia 2010:203-210.
63. Place AR, Powers DA. 1979. Genetic variation and relative catalytic efficiencies, LDH-B allozymes of Fundulus heteroclitus. Proc Natl Acad Sci USA 76:2354-2358.
64. Podrabsky JE, Carpenter JF, Hand SC. 2001. Survival of water stress in annual fish embryos: dehydration avoidance and egg amyloid fibers. Am J Physiol Regul Integr Comp Physiol 280:R123-R131.
65. Potts WTW, Eddy FB. 1973. The permeability to water of the eggs of certain marine teleosts. J Comp Physiol 82:305-315.
66. Potts WTW, Rudy PP Jr. 1969. Water balance in the eggs of the Atlantic salmon, Salmo salar. J Exp Biol 50:223-237.
67. Powers DA, Lauerman T, Crawford D, et al. 1991. The evolutionary significance of genetic variation at enzyme synthesizing loci in the teleost Fundulus heteroclitus. J Fish Biol 39:169-184.
68. Preston RL. 2009. Osmoregulation in annelids. In: DH Evans, editor. Osmotic and ionic regulation in animals. Boca Raton, FL: Taylor & Francis Group, LLC. p 135-164.
69. Preston RL, Clifford RJ, Guy AK, et al. 2003. Preliminary studies of salinity adaptation in Fundulus heteroclitus and apparent CFTR mRNA expression in gill tissue and oocytes. Bull Mt Desert I Biol Lab 42:68-70.
70. Preston RL, Clifford RJ, Thompson JA, et al. 2004. CFTR mRNA expression in developing Fundulus heteroclitus embryos. Bull Mt Desert I Biol Lab 43:25-27.
71. Preston RL, Flowers AE, Lahey BC, et al. 2006. Measurement of the desiccation of Fundulus heteroclitus embryos in controlled humidities. Bull Mt Desert I Biol Lab 45:101-103.
72. Preston RL, Edwards BR, Baumhardt PE, et al. 2008. Desiccation resistance by mid-stage Fundulus heteroclitus embryos. Bull Mt Desert I Biol Lab 47:94-96.
73. Riis-Vestergaard J. 1982a. Water and salt balance of halibut eggs and larvae (Hippoglossus hippoglossus). Mar Biol 70:135-139.
74. Riis-Vestergaard J. 1982b. Water permeation in plaice eggs (Pleuronectes platessa L.). Acta Physiol Scand 114:26A.
75. Scott GR, Richards JG, Forbush B, Isenring P, Schulte PM. 2004a. Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after salinity transfer. Am J Phyiol 287:C300-C309.
76. Scott GR, Rogers JT, Richards JG, Wood MC, Schulte PM. 2004b. Intraspecific divergence of ionoregulatory physiology in the euryhaline teleost Fundulus heteroclitus: possible mechanisms of freshwater adaptation. J Exp Biol 207:3399-3410.
77. Scott GR, Claiborne JB, Edwards SL, Schulte PM, Wood CM. 2005. Gene expression after freshwater transfer in gills and opercular epithelia of killifish: insight into divergent mechanisms of ion transport. J Exp Biol 208:2719-2729.
78. Scott GR, Baker DW, Schulte PM, Wood CM. 2008. Physiological and molecular mechanisms of osmoregulatory plasticity in killifish after seawater transfer. J Exp Biol 211:2450-2459.
79. Strathmann RR, Hess HC. 1999. Two designs of marine egg masses and their divergent consequences for oxygen supply and desiccation in air. Am Zool 39:253-260.
80. Taylor MH. 1999. A suite of adaptations for intertidal spawning. Am Zool 39:313-320.
81. Taylor MH, DiMichele L. 1983. Spawning site utilization in a Delaware population of Fundulus heteroclitus (Pisces: Cyprinodontidae). Copeia 1983:719-725.
82. Taylor MH, DiMichele L, Leach GJ. 1977. Egg stranding in the life cycle of the mummichog, Fundulus heteroclitus. Copeia 1977:397-399.
83. Taylor MH, Leach GJ, DiMichele L, Levitan WM, Jacob WF. 1979. Lunar spawning cycle in the mummichog, Fundulus heteroclitus (Pisces, Cyprinodontidae). Copeia 1979:291-297.
84. Tingaud-Sequeira A, Zapater C, Chauvigne F, Otero D, Cerdà J. 2009. Adaptive plasticity of killifish (Fundulus heteroclitus) embryos, dehydration-stimulated development and differential aquaporin-3 expression. Am J Physiol Regul Integr Comp Physiol 296:R1041-R1052.
85. Trinkaus JP. 1998. Gradient in convergent cell movement during Fundulus gastrulation. J Exp Zool 281:328-335.
86. Van Veld PA, Vogelbein WK, Smolowitz R, Woodin BR, Stegeman JJ. 1992. Cytochrome P450Ia1 in hepatic lesions of a teleost fish (Fundulus heteroclitus) collected from a polycyclic aromatic hydrocarbon-contaminated site. Carcinogenesis 13:505-507.
87. Van Veld PA, Vogelbein WK, Cochran MK, Goksoyr A, Stegeman JJ. 1997. Route-specific cellular expression of cytochrome P4501A (CYP1A) in fish (Fundulus heteroclitus) following exposure to aqueous and dietary benzo[a]pyrene. Toxicol Appl Pharmacol 142:348-359.
88. Vince S, Valiela I, Backus N, Teal JM. 1976. Predation by the salt marsh killifish Fundulus heteroclitus (L.) in relation to prey size and habitat structure: consequences for prey distribution and abundance. J Exp Mar Biol Ecol 23:255-266.
89. Wehner F, Olsen H, Tinel H, Kinne-Saffran E, Kinne RKH. 2003. Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. Rev Physiol Biochem Pharmacol 148:1-80.
90. Weis JS. 2002. Tolerance to environmental contaminants in the mummichog, Fundulus heteroclitus. Hum Ecol Risk Assess 8:933-953.
91. Whitehead A, Roach JL, Zhang S, Galvez F. 2012. Salinity- and population-dependent genome regulatory response during osmotic acclimation in the killifish (Fundulus heteroclitus) gill. J Exp Biol 215:1293-1305.
92. Wood CM, Marshall WS. 1994. Ion balance, acid-base regulation, and chloride cell function in the common killifish, Fundulus heteroclitus-a euryhaline estuarine teleost. Estuaries 17:34-52.
93. Yamahira K. 1997. Hatching success affects the timing of spawning by the intertidally spawning puffer Takifugu niphobles. Mar Ecol Prog Ser 155:239-248.