Metabolic Dormancy and Responses to Environmental Desiccation in Fish Embryos

  • Jason E. PodrabskyEmail author
  • Angèle Tingaud-Sequeira
  • Joan CerdàEmail author
Part of the Topics in Current Genetics book series (TCG, volume 21)


Metabolic depression is relatively uncommon among the fishes with the greatest number of species exhibiting dormancy as embryos. Dormancy in fish embryos is largely associated with deposition of embryos into terrestrial habitats to avoid embryo predation or to survive intermittent drying of aquatic habitats. Killifish embryos in general, and especially the embryos of annual killifish, are highly adapted for life at the interface between land and water and thus have evolved a suite of characters that allows them to survive in an aerial environment. Here we review the available literature on embryonic dormancy and dehydration tolerance in killifish embryos.


Dehydration Tolerance Evaporative Water Loss Anoxia Tolerance Embryonic Diapause Annual Killifish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The research conducted by the authors was financed by the U.S. National Science Foundation (IOS 0344578, JEP) and the American Heart Association (0335286 N, JEP), European Commission New and Emerging Science and Technologies (NEST) program (Contract No. 012674-2 Sleeping Beauty, JC), and by the Spanish Ministry of Science and Innovation (AGL2007-60262/ACU, JC).


  1. Armstrong PB, Child JW (1965) Stages in the normal development of Fundulus heteroclitus. Biol Bull 128:143–168CrossRefGoogle Scholar
  2. Barcroft LC, Offenberg H, Thomsen P, Watson AJ (2003) Aquaporin proteins in murine trophectoderm mediate transepithelial water movements during cavitation. Dev Biol 256:342–354PubMedCrossRefGoogle Scholar
  3. Berra TM, Allen DR (1989) Burrowing, emergence, behavior, and functional morphology of the Australian salamanderfish, Lepidogalaxias salamandroides. Fisheries 14:2–10CrossRefGoogle Scholar
  4. Beuron F, Le Cahérec F, Guillam MT, Cavalier A, Garret A, Tassan JP, Delamarche C, Schultz P, Mallouh V, Rolland JP et al (1995) Structural analysis of a MIP family protein from the digestive tract of Cicadella viridis. J Biol Chem 270:17414–17422PubMedCrossRefGoogle Scholar
  5. Bigelow HB, Schroeder WC (1953) Fishes of the Gulf of Maine. US Fish & Wildlife Service. Fish Bull 53(74):1–577Google Scholar
  6. Brosset A (2003) Convergent and divergent evolution in rain-forest populations and communities of cyprinodontiform fishes (Aphyosemion and Rivulus) in Africa and South America. Can J Zool 81:1484–1493CrossRefGoogle Scholar
  7. Burnett KG, Bain LJ, Baldwin WS, Callard GV, Cohen S, Di Giulio RT, Evans DH, Gómez-Chiarri M, Hahn ME, Hoover CA, Karchner SI, Katoh F, Maclatchy DL, Marshall WS, Meyer JN, Nacci DE, Oleksiak MF, Rees BB, Singer TD, Stegeman JJ, Towle DW, Van Veld PA, Vogelbein WK, Whitehead A, Winn RN, Crawford DL (2007) Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comp Biochem Physiol D 2:257–286Google Scholar
  8. Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an antarctic fish: on ice for winter. PLoS ONE 3:e1743. doi:10.1371/ journal.pone.0001743PubMedCrossRefGoogle Scholar
  9. Charteris SC, Allibone RM, Death RG (2003) Spawning site selection, egg development, and larval drift of Galaxias postvectis and G. fasciatus in a New Zealand stream. N Z J Mar Freshwater Res 37:493–505CrossRefGoogle Scholar
  10. Chew SF, Gan J, Ip YK (2005) Nitrogen metabolism and excretion in the swamp eel, Monopterus albus, during 6 or 40 days of estivation in mud. Physiol Biochem Zool 78:620–629PubMedCrossRefGoogle Scholar
  11. Darken RS, Martin KLM, Fisher MC (1998) Metabolism during delayed hatching in terrestrial eggs of a Marine fish, the Grunion Leuresthes tenuis. Physiol Zool 71:400–406PubMedCrossRefGoogle Scholar
  12. Denucé JM (1989) Developmental changes in annual fish embryos kept in the proximity of adult fishes. Acta Embryol Morphol Exper 10:87–94Google Scholar
  13. Denver RJ (1997) Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Horm Behav 31:169–179PubMedCrossRefGoogle Scholar
  14. DiMichele L, Powers DA (1982) LDH-B genotype-specific hatching times of Fundulus heteroclitus embryos. Nature 296:563–564PubMedCrossRefGoogle Scholar
  15. DiMichele L, Powers DA (1984a) The relationship between oxygen consumption rate and hatching in Fundulus heteroclitus. Physiol Zool 57:46–51Google Scholar
  16. DiMichele L, Powers DA (1984b) Developmental and oxygen consumption rate differences between lactate dehydrogenase B genotypes of Fundulus heteroclitus and their effect on hatching time. Physiol Zool 57:52–56Google Scholar
  17. DiMichele L, Taylor MH (1980) The environmental control of hatching in Fundulus heteroclitus. J Exp Zool 214:181–187CrossRefGoogle Scholar
  18. DiMichele L, Taylor MH (1981) The mechanism of hatching in Fundulus heteroclitus: development and physiology. J Exp Zool 217:73–79CrossRefGoogle Scholar
  19. dos Santos Ferreira da Silva G, Giustia H, Sancheza AP, do Carmoa JM, Glass ML (2008) Aestivation in the South American lungfish, Lepidosiren paradoxa: effects on cardiovascular function, blood gases, osmolality and leptin levels. Respir Physiol Neurobiol 164:380–385PubMedCrossRefGoogle Scholar
  20. Edashige K, Tanaka M, Ichimaru N, Ota S, Yazawa K, Higashino Y, Sakamoto M, Yamaji Y, Kuwano T, Valdez DM Jr, Kleinhans FW, Kasai M (2006) Channel-dependent permeation of water and glycerol in mouse morulae. Biol Reprod 74:625–632PubMedCrossRefGoogle Scholar
  21. Eduardo J, Bicudo PW, Johansen K (1979) Respiratory gas exchange in the airbreathing fish, Synbranchus marmoratus. Environ Biol Fishes 4:55–64CrossRefGoogle Scholar
  22. Eldon GA (1979) Breeding, growth, and aestivation of the Canterbury mudfish, Neochanna burrowsius (Salmoniformes: Galaxiidae). N Z J Mar Freshwater Res 13:331–346CrossRefGoogle Scholar
  23. Enajjar S, Bradai MN, Bouain A (2008) New data on the reproductive biology of the common guitarfish of the Gulf of Gabès (southern Tunisia, central Mediterranean). J Mar Biol Assoc UK 88:1063–1068CrossRefGoogle Scholar
  24. Fergusson-Kolmes L, Podrabsky JE (2007) Differential effects of anoxia on heart rate in developmental stages of the annual killifish Austrofundulus limnaeus that differ in their tolerance of anoxia. J Exp Zool 307A:419–423CrossRefGoogle Scholar
  25. Fishman AP, Galante RJ, Winokur A, Pack AI (1992) Aestivation in the African lungfish. Proc Am Phil Soc 136:61–72Google Scholar
  26. Gallardo PA, Cortes A, Bozinovic F (2005) Phenotypic flexibility at the molecular and organismal level allows desert-dwelling rodents to cope with seasonal water availability. Physiol Biochem Zool 78:145–152PubMedCrossRefGoogle Scholar
  27. Greenwood PH (1986) The natural history of African lungfish. J Morphol Suppl 1:163–179CrossRefGoogle Scholar
  28. Gutierrez-Estrada JC, Prenda J, Oliva F, Fernández-Delgado C (1998) Distribution and habitat preferences of the introduced mummichog Fundulus heteroclitus (Linneaus) in South-western Spain. Estuar Coast Shelf Sci 46:827–835CrossRefGoogle Scholar
  29. Hand SC (1998) Quiescence in Artemia franciscana embryos: reversible arrest of metabolism and gene expression at low oxygen levels. J Exp Biol 201:1233–1242PubMedGoogle Scholar
  30. Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annu Rev Physiol 58:539–563PubMedCrossRefGoogle Scholar
  31. Hansen CA, Sidell BD (1983) Atlantic hagfish cardiac muscle: metabolic basis of tolerance to anoxia. Am J Physiol Regul Integr Comp Physiol 244:R356–R362Google Scholar
  32. Harrington RW Jr (1959) Delayed hatching in stranded eggs of marsh killifish, Fundulus confluentus. Ecology 40:430–437CrossRefGoogle Scholar
  33. Helvik JV, Walther BT (1993) Development of hatchability in halibut (Hippoglossus hippoglossus) embryos. Int J Dev Biol 37:487–490PubMedGoogle Scholar
  34. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New YorkGoogle Scholar
  35. Hrbek T, Larson A (1999) The evolution of diapause in the killifish family Rivulidae (Atherinomorpha, Cyprinodontiformes): a molecular phylogenetic and biogeographic perspective. Evolution 53:1200–1216CrossRefGoogle Scholar
  36. Hsiao SM, Meier AH (1989) Comparison of semilunar cycles of spawning activity in Fundulus grandis and F. heteroclitus held under constant laboratory conditions. J Exp Zool 252:213–218CrossRefGoogle Scholar
  37. Hsiao SM, Greeley MS, Wallace RA (1994) Reproductive cycling in female Fundulus heteroclitus. Biol Bull 186:217–281CrossRefGoogle Scholar
  38. Hsiao SM, Limesand SW, Wallace RA (1996) Semilunar follicular cycle of an intertidal fish: the Fundulus model. Biol Reprod 54:809–818PubMedCrossRefGoogle Scholar
  39. Hyvarinen H, Holopainen IJ, Piironen J (1985) Anaerobic wintering of crucian carp (Carassius carassius L.). I: Annual dynamics of glycogen reserves in nature. Comp Biochem Physiol 82:797–803CrossRefGoogle Scholar
  40. Inglima K, Perlmutter A, Markofsky J (1981) Reversible stage-specific embryonic inhibition mediated by the presence of adults in the annual fish Nothobranchius guentheri. J Exp Zool 215:23–33PubMedCrossRefGoogle Scholar
  41. Jonsson KI (2003) Causes and consequences of excess resistance in cryptobiotic metazoans. Physiol Biochem Zool 76:429–435PubMedCrossRefGoogle Scholar
  42. Kawaguchi M, Yasumasu S, Shimizu A, Hiroi J, Yoshizaki N, Nagata K, Tanokura M, Iuchi I (2005) Purification and gene cloning of Fundulus heteroclitus hatching enzyme. A hatching enzyme system composed of high choriolytic enzyme and low choriolytic enzyme is conserved between two different teleosts, Fundulus heteroclitus and medaka Oryzias latipes. FEBS J 272:4315–4326PubMedCrossRefGoogle Scholar
  43. Kawamura K, Uehara K (2005) Effects of temperature on free-embryonic diapause in the autumn-spawning bitterling Acheilognathus rhombeus (Teleostei: Cyprinidae). J Fish Biol 67:684–695CrossRefGoogle Scholar
  44. Kikawada T, Saito A, Kanamori Y, Fujita M, Snigórska K, Watanabe M, Okuda T (2008) Dehydration-inducible changes in expression of two aquaporins in the sleeping chironomid, Polypedilum vanderplanki. Biochim Biophys Acta 1778:514–520PubMedCrossRefGoogle Scholar
  45. King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5:687–698PubMedCrossRefGoogle Scholar
  46. Koenig CC, Livingston RJ (1976) The embryological development of the diamond killifish (Adinia xenica). Copeia 1976:435–445CrossRefGoogle Scholar
  47. Krumschnabel G (2000) Cellular and molecular basis of anoxia-tolerance and -intolerance in vertebrates: comparative studies using hepatocytes from goldfish and trout. Recent Res Dev Comp Biochem Physiol 1:1–11Google Scholar
  48. Lee DS, Gilbert CR, Hocutt VH, Jenkins RE, McAllister DC, Stauffer JR (1980) Atlas of North American freshwater fishes. North Carolina State Museum of Natural History, Publication of the North Carolina Biological Survey No. 1980-12Google Scholar
  49. Lesser MP, Martini FH, Heiser JB (1996) Ecology of the hagfish. Myxine glutinosa L. in the Gulf of Maine I. Metabolic rates and energetics. J Exp Mar Biol Ecol 208:215–225CrossRefGoogle Scholar
  50. Levels PJ, Denucé JM (1988) Intrinsic variability in the frequency of embryonic diapauses of the annual fish Nothobranchius korthausae, regulated by light: dark cycle and temperature. Environ Biol Fishes 22:211–223CrossRefGoogle Scholar
  51. Levels PJ, Gubbels REMB, Denucé JM (1986) Oxygen consumption during embryonic development of the annual fish Nothobranchius korthausae with special reference to diapause. Comp Biochem Physiol 84A:767–770CrossRefGoogle Scholar
  52. Machado BE, Podrabsky JE (2007) Salinity tolerance in diapausing embryos of the annual killifish Austrofundulus limnaeus is supported by exceptionally low water and ion permeability. J Comp Physiol B 177:809–820PubMedCrossRefGoogle Scholar
  53. Markofsky J, Matias JR (1977) The effects of temperature and season of collection on the onset and duration of diapause in embryos of the annual fish Nothobranchius guentheri. J Exp Zool 202:49–56PubMedCrossRefGoogle Scholar
  54. Markofsky J, Matias JR, Inglima K, Vogelman JH, Orentreich N (1979) The variable effects of ambient and artificial light: dark cycles on embryonic diapause in a laboratory population of the annual fish Nothobranchius guentheri. J Exp Biol 83:203–215Google Scholar
  55. Martin KLM (1999) Ready and waiting: delayed hatching and extended incubation of anamniotic vertebrate terrestrial eggs. Am Zool 39:279–288Google Scholar
  56. Martinez AS, Cutler CP, Wilson GD, Phillips C, Hazon N, Cramb G (2005) Regulation of expression of two aquaporin homologs in the intestine of the European eel: effects of seawater acclimation and cortisol treatment. Am J Physiol Regul Integr Comp Physiol 288:R1733–R1743PubMedCrossRefGoogle Scholar
  57. Matias JR, Markofsky J (1978) The survival of embryos of the annual killifish Nothobranchius guentheri exposed to temperature extremes and the subsequent effects on embryonic diapause. J Exp Zool 204:219–228CrossRefGoogle Scholar
  58. McDowall RM, Charteris SC (2006) The possible adaptive advantages of terrestrial egg deposition in some fluvial diadromous galaxiid fishes (Teleostei: Galaxiidae). Fish Fish 7:153–164CrossRefGoogle Scholar
  59. Müller C, Sendler M, Hildebrandt JP (2006) Downregulation of aquaporins 1 and 5 in nasal gland by osmotic stress in ducklings, Anas platyrhynchos: implications for the production of hypertonic fluid. J Exp Biol 209:4067–4076PubMedCrossRefGoogle Scholar
  60. Murphy WJ, Collier GE (1997) A molecular phylogeny for Aplocheiloid fishes (Atherinomorpha, Cyprinodontiformes): the role of vicariance and the origins of annualism. Mol Biol Evol 14:790–799PubMedCrossRefGoogle Scholar
  61. Murphy WJ, Nguyen TN, Taylor EB, Collier GE (1999) Mitochondrial DNA phylogeny of West African Aplocheiloid killifishes (Cyprinodontiformes, Aplocheilidae). Mol Phylogenet Evol 11:343–350PubMedCrossRefGoogle Scholar
  62. Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA (1995) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92:1013–1017PubMedCrossRefGoogle Scholar
  63. Nilsson GE, Renshaw GMC (2004) Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207:3131–3139PubMedCrossRefGoogle Scholar
  64. O’Boyle S, Bree RT, McLoughlin S, Grealy M, Byrnes L (2007) Identification of zygotic genes expressed at the midblastula transition in zebrafish. Biochem Biophys Res Commun 358:462–468PubMedCrossRefGoogle Scholar
  65. Papadopoulos MC, Saadoun S, Verkman AS (2008) Aquaporins and cell migration. Pflugers Arch 456:693–700PubMedCrossRefGoogle Scholar
  66. Peters N (1963) Embryonale anpassungen oviparer Zahnkarpfen aus periodisch austrocknenden Gewässern. Int Rev Ges Hydrobiol 48:257–313CrossRefGoogle Scholar
  67. Peters N (1965) Diapause und embryonale missbildung bei eierlegenden Zahnkarpfen. Wilhelm Roux Arch Entwickl Mech Org 156:75–87CrossRefGoogle Scholar
  68. Philip BN, Yi SX, Elnitsky MA, Lee RE Jr (2008) Aquaporins play a role in desiccation and freeze tolerance in larvae of the goldenrod gall fly, Eurosta solidaginis. J Exp Biol 211:1114–1119PubMedCrossRefGoogle Scholar
  69. Pletcher FT (1963) The life history and distribution of lampreys in the Salmon and certain other rivers in British Columbia, Canada. M.Sc. Thesis, The University of British Columbia, Vancouver, BC, p 195Google Scholar
  70. Podrabsky JE, Hand SC (1999) The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus. J Exp Biol 202:2567–2580PubMedGoogle Scholar
  71. Podrabsky JE, Hand SC (2000) Depression of protein synthesis during diapause in embryos of the annual killifish Austrofundulus limnaeus. Physiol Biochem Zool 73:799–808PubMedCrossRefGoogle Scholar
  72. Podrabsky JE, Somero GN (2007) An inducible 70 kDa-class heat shock protein is constitutively expressed during early development and diapause in the annual killifish Austrofundulus limnaeus. Cell Stress Chaperones 12:199–204PubMedCrossRefGoogle Scholar
  73. Podrabsky JE, Hrbek T, Hand SC (1998) Physical and chemical characteristics of ephemeral pond habitats in the Maracaibo and Llanos region of Venezuela. Hydrobiologia 362:67–78CrossRefGoogle Scholar
  74. Podrabsky JE, Carpenter JF, Hand SC (2001) Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers. Am J Physiol Integr Regul Comp Physiol 280:R123–R131Google Scholar
  75. Podrabsky JE, Lopez JP, Fan TWM, Higashi R, Somero GN (2007) Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: insights from a metabolomics analysis. J Exp Biol 210:2253–2266PubMedCrossRefGoogle Scholar
  76. Podrabsky JE, Clelen D, Crawshaw LI (2008) Temperature preference and reproductive fitness of the annual killifish Austrofundulus limnaeus exposed to constant and fluctuating temperatures. J Comp Physiol A 194:385–393CrossRefGoogle Scholar
  77. Powers DA, Lauerman T, Crawford D, DiMichele L (1991) Genetic mechanisms for adapting to a changing environment. Annu Rev Genet 25:629–659PubMedCrossRefGoogle Scholar
  78. Pusey BJ (1989) Aestivation in the teleost fish Lepidogalaxias salamandroides (Mees). Comp Biochem Physiol 92A:137–138CrossRefGoogle Scholar
  79. Raldúa D, Otero D, Fabra M, Cerdà J (2008) Differential localization and regulation of two aquaporin-1 homologs in the intestinal epithelia of the marine teleost Sparus aurata. Am J Physiol Regul Integr Comp Physiol 294:R993–R1003PubMedCrossRefGoogle Scholar
  80. Randall JE (1987) Introductions of marine fishes to the Hawaiian Islands. Bull Mar Sci 41:490–502Google Scholar
  81. Reichard M, Polacik M, Sedlacek O (2009) Distribution, colour polymorphism and habitat use of the African killifish Nothobranchius furzeri, the vertebrate with the shortest life span. J Fish Biol 74:198–212PubMedCrossRefGoogle Scholar
  82. Schoots AFM, Stikkelbroeck JJM, Bekhuis JF, Denucé JM (1982) Hatching in Teleostean fishes: fine structural changes in the egg envelope during enzymatic breakdown in vivo and in vitro. J Ultrastruct Res 80:185–196PubMedCrossRefGoogle Scholar
  83. Scott WB, Crossman EJ (1998) Freshwater Fishes of Canada. Galt House Publications Ltd., Oakville, CanadaGoogle Scholar
  84. Seale A (1910) The successful transference of black bass into the Philippine Islands with notes on the transportation of live fish long distances. Philippine J Sci 5:153–159Google Scholar
  85. Simpfendorfer CA (1992) Reproductive strategy of the Australian sharpnose shark, Rhizoprionodon taylori (Elasmobranchii: Carcharhinidae), from Cleveland Bay, northern Queensland. Aust J Mar Freshwater Res 43:67–75CrossRefGoogle Scholar
  86. Smith HW (1930) Metabolism of the lung-fish, Protopterus aethiopicus. J Biol Chem 88:97–130Google Scholar
  87. Smith-Espinoza CJ, Richer A, Salami F, Bartels D (2003) Dissecting the response to dehydration and salt (NaCl) in the resurrection plant Craterostigma plantagineum. Plant Cell Environ 26:1307–1315CrossRefGoogle Scholar
  88. Taylor MH (1986) Environmental and endocrine influences on reproduction of Fundulus heteroclitus. Am Zool 26:159–171Google Scholar
  89. Taylor MH (1991) Entrainment of the semilunar reproductive cycle of Fundulus heteroclitus. Proc 4th Int Symp Reprod Physiol Fish, Sheffield: Fish Symp 91:157–159Google Scholar
  90. Taylor MH (1999) A suite of adaptations for intertidal spawning. Am Zool 39:313–320Google Scholar
  91. Taylor MH, DiMichele L, Leach GJ (1977) Egg stranding in the life cycle of the Mummichog, Fundulus heteroclitus. Copeia 1977:397–399CrossRefGoogle Scholar
  92. Taylor MH, Leach GJ, DiMichele L, Levitan WM, Jacob WF (1979) Lunar spawning cycle in the mummichog, Fundulus heteroclitus (Pisces: Cyprinodontidae). Copeia 1979:291–297CrossRefGoogle Scholar
  93. Tewksbury HT, Conover DO (1987) Adaptive significance of intertidal egg deposition in the Atlantic Silverside Menidia menidia. Copeia 1987:76–83CrossRefGoogle Scholar
  94. Tingaud-Sequeira A, Zapater C, Chauvigné 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–R1052Google Scholar
  95. Tomiyama M, Yanagibashi S (2004) Effect of temperature, age class, and growth on induction of aestivation in Japanese sandeel (Ammodytes personatus) in Ise Bay, central Japan. Fish Oceanogr 13:81–90CrossRefGoogle Scholar
  96. Watters BR (2009) The ecology and distribution of Nothobranchius fishes. J Am Killifish Assoc 42:37–76Google Scholar
  97. White WT, Hall NG, Potter LC (2002) Reproductive biology and growth during pre- and postnatal life of Trygonoptera personata and T. mucosa (Batoidea: Urolophidae). Mar Biol 140:699–712CrossRefGoogle Scholar
  98. Wourms JP (1964) Comparative observations on the early embryology of Nothobranchius taeniopygus (Hilgendorf) and Aplochcheilichthys pumilis (Boulenger) with special reference to the problem of naturally occurring embryonic diapause in teleost fishes. In: East African Freshwater Research Organization, Annual Report, Jinja, pp 68–73Google Scholar
  99. Wourms JP (1967) Annual Fishes. In: Wilt FH and Wessels NK (eds). Methods in Developmental Biology. Thomas Y. Crowell Co., New York, pp 123–137Google Scholar
  100. Wourms JP (1972a) Developmental biology of annual fishes I. Stages in the normal development of Austrofundulus myersi Dahl. J Exp Zool 182:143–168PubMedCrossRefGoogle Scholar
  101. Wourms JP (1972b) The developmental biology of annual fishes II. Naturally occurring dispersion and reaggregation of blasotmeres during the development of annual fish eggs. J Exp Zool 182:169–200PubMedCrossRefGoogle Scholar
  102. Wourms JP (1972c) The developmental biology of annual fishes III. Pre-embryonic and embryonic diapause of variable duration in the eggs of annual fishes. J Exp Zool 182:389–414PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Department of BiologyPortland State UniversityPortlandUSA
  2. 2.Laboratory of Institut de Recerca i Tecnologia Agroalimentàries (IRTA)-Institut de Ciències del MarConsejo Superior de Investigaciones Científicas (CSIC)BarcelonaSpain
  3. 3.Génomique et Physiologie des PoissonsUniversité Bordeaux 1, UMR NuAGeTalenceFrance

Personalised recommendations