Effects of environmental oxygen on development and respiration of Australian lungfish (Neoceratodus forsteri) embryos
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Abstract
The effects of oxygen partial pressure (\( P_{{{\text{O}}_{2} }} \)) on development and respiration were investigated in the eggs of the Australian lungfish, Neoceratodus forsteri. At 20°C, embryonic survival and development was optimal at 15 and 20.9 kPa. Development was slowed at 5 and 10 kPa and embryos did not survive 2 kPa. At lower \( P_{{{\text{O}}_{2} }} \), the rate of oxygen consumption also decreased. Embryos responded to hypoxia by hatching at an earlier age and stage of development, and hatching wet and dry gut-free masses were reduced. The role of oxygen conductance (\( G_{{{\text{O}}_{2} }} \)) in gas exchange was also examined under selected environmental \( P_{{{\text{O}}_{2} }} \) and temperatures. The breakdown of the vitelline membrane changed capsule geometry, allowed water to be absorbed into the perivitelline space and increased capsule \( G_{{{\text{O}}_{2} }} \). This occurred at embryonic stage 32 under all treatments and was largely independent of both \( P_{{{\text{O}}_{2} }} \) and temperature (15, 20 and 25°C), demonstrating that capsule \( G_{{{\text{O}}_{2} }} \) cannot adaptively respond to altered environmental conditions. The membrane breakdown increased capsule diffusive \( G_{{{\text{O}}_{2} }} \) and stabilised perivitelline \( P_{{{\text{O}}_{2} }} \), but reduced the convective \( G_{{{\text{O}}_{2} }} \) of the perivitelline fluid, as the large perivitelline volume and inadequate convective current resulted in a \( P_{{{\text{O}}_{2} }} \) gradient within the egg prior to hatch.
Keywords
Neoceratodus forsteri Embryos Development Respiration Hypoxia Capsule conductanceNotes
Acknowledgments
We thank Rolf Ericsson from the Australian lungfish laboratory, Macquarie University for his expertise and help in the collection of eggs and the two anonymous reviewers for helpful comments on the manuscript. We acknowledge funding from the University of Adelaide and Australian Geographic Society.
References
- Adolph EF (1979) Development of dependence on oxygen in embryo salamanders. Am J Physiol 236:R282–R291PubMedGoogle Scholar
- Alderdice DF, Wickett WP, Brett JR (1958) Some effects of temporary exposure to low dissolved oxygen levels on Pacific salmon eggs. J Fish Res Board Can 15:229–249CrossRefGoogle Scholar
- Alderdice DF, Jensen JOT, Velsen FPJ (1984) Measurement of hydrostatic pressure in salmonid eggs. Can J Zool 62:1977–1987CrossRefGoogle Scholar
- Bradford DF, Seymour RS (1985) Energy conservation during the delayed-hatching period in the frog Pseudophryne bibronii. Physiol Zool 58:491–496Google Scholar
- Bradford DF, Seymour RS (1988) Influence of environmental PO2 on embryonic oxygen consumption, rate of development, and hatching in the frog Pseudophryne bibronii. Physiol Zool 61:475–482Google Scholar
- Burggren W (1985) Gas exchange, metabolism, and “ventilation” in gelatinous frog egg masses. Physiol Zool 58:503–514Google Scholar
- Czerkies P, Brzuzan P, Kordalski K, Luczynski M (2001) Critical partial pressures of oxygen causing precocious hatching in Coregonus lavaretus and C. albula embryos. Aquaculture 196:151–158CrossRefGoogle Scholar
- Davenport J (1983) Oxygen and the developing eggs and larvae of the lumpfish, Cyclopterus lumpus. J Mar Biol Assoc UK 63:633–640CrossRefGoogle Scholar
- Daykin PN (1965) Application of mass transfer theory to the problem of respiration of fish eggs. J Fish Res Board Can 22:159–171CrossRefGoogle Scholar
- Dejours P (1981) Principles of comparative respiratory physiology. Elsevier/North-Holland Biomedical Press, AmsterdamGoogle Scholar
- DiMichele L, Powers DA (1984) The relationship between oxygen consumption rate and hatching in Fundulus heteroclitus. Physiol Zool 57:46–51Google Scholar
- Eldridge MB, Echeverria T, Whipple JA (1977) Energetics of Pacific herring (Clupea harengus pallasi) embryos and larvae exposed to low concentrations of benzene, a monoaromatic component of crude oil. Tran Am Fish Soc 106:452–461CrossRefGoogle Scholar
- Garside ET (1959) Some effects of oxygen in relation to temperature on the development of lake trout embryos. Can J Zool 37:689–698CrossRefGoogle Scholar
- Green BS (2004) Embryogenesis and oxygen consumption in benthic egg clutches of a tropical clownfish, Amphiprion melanopus (Pomacentridae). Comp Biochem Physiol A 138:33–38CrossRefGoogle Scholar
- Groot EP, Alderdice DF (1985) Fine structure of the external egg membrane of five species of Pacific salmon and steelhead trout. Can J Zool 63:552–566CrossRefGoogle Scholar
- Gruber K, Wieser W (1983) Energetics of development of the alpine charr, Salvelinus alpinus, in relation to temperature and oxygen. J Comp Physiol 149:485–493Google Scholar
- Hamor T, Garside ET (1976) Developmental rates of embryos of Atlantic salmon, Salmon salar L., in responses to various levels of temperature, dissolved oxygen, and water exchange. Can J Zool 54:1912–1917PubMedCrossRefGoogle Scholar
- Hamor T, Garside ET (1977) Size relations and yolk utilization in embryonated ova and alevins of Atlantic salmon Salmo salar L. in various combinations of temperature and dissolved oxygen. Can J Zool 55:1892–1898PubMedCrossRefGoogle Scholar
- Hamor T, Garside ET (1979) Hourly and total oxygen consumption by ova of Atlantic salmon, Salmo salar L., during embryogenesis, at two temperatures and three levels of dissolved oxygen. Can J Zool 57:1196–1200CrossRefGoogle Scholar
- Hayes FR, Wilmot IR, Livingstone DA (1951) The oxygen consumption of the salmon egg in relation to development and activity. J Exp Zool 116:377–395PubMedCrossRefGoogle Scholar
- Kemp A (1982) The embryological development of the Queensland lungfish, Neoceratodus forsteri (Krefft). Mem Queenl Mus 20:553–597Google Scholar
- Kemp A (1984) Spawning of the Australian lungfish, Neoceratodus forsteri (Krefft) in the Brisbane River and in Enoggera Reservoir, Queensland. Mem Queenl Mus 21:391–399Google Scholar
- Kemp A (1986) The biology of the Australian lungfish, Neoceratodus forsteri (Krefft 1870). J Morphol Suppl 1:181–198CrossRefGoogle Scholar
- Latham KE, Just JJ (1989) Oxygen availability provides a signal for hatching in the rainbow trout (Salmo gairdneri) embryo. Can J Fish Aquat Sci 46:55–58CrossRefGoogle Scholar
- Mills NE, Barnhart MC (1999) Effects of hypoxia on embryonic development in two Ambystoma and two Rana species. Physiol Biochem Zool 72:179–188PubMedCrossRefGoogle Scholar
- Mills NE, Barnhart MC, Semlitsch RD (2001) Effects of hypoxia on egg capsule conductance in Ambystoma (Class Amphibia, Order Caudata). J Exp Biol 204:3747–3753PubMedGoogle Scholar
- Mueller CA, Seymour RS (2011) The importance of perivitelline fluid convection on oxygen uptake of Pseudophryne bibronii eggs. Physiol Biochem Zool (in press)Google Scholar
- Mueller CA, Joss JMP, Seymour RS (2011) The energy cost of embryonic development in fishes and amphibians, with emphasis on new data from the Australian lungfish, Neoceratodus forsteri. J Comp Physiol B 181:43–52PubMedCrossRefGoogle Scholar
- Oppen-Bernsten DO, Bogsnes A, Walther BT (1990) The effects of hypoxia, alkalinity and neurochemicals on hatching of Atlantic salmon (Salmo salar) eggs. Aquaculture 86:417–430CrossRefGoogle Scholar
- Petranka JW, Just JJ, Crawford EC (1982) Hatching of amphibian embryos: the physiological trigger. Science 217:257–259PubMedCrossRefGoogle Scholar
- Prosser CL (1973) Comparative animal physiology. WB Saunders Company, PhiladelphiaGoogle Scholar
- Rombough PJ (1988) Respiratory gas exchange, aerobic metabolism, and effects of hypoxia during early life. In: Hoar WS, Randall DJ (eds) The physiology of developing fish. Academic Press, San Diego, pp 59–161CrossRefGoogle Scholar
- Rombough PJ (1989) Oxygen conductance values and structural characteristics of the egg capsules of pacific salmonids. Comp Biochem Physiol A 92:279–283CrossRefGoogle Scholar
- Salthe SN (1963) The egg capsules in the Amphibia. J Morphol 113:161–171PubMedCrossRefGoogle Scholar
- Salthe SN (1965) Increase in volume of the perivitelline chamber during development of Rana pipiens Schreber. Physiol Zool 38:80–98Google Scholar
- Seymour RS (1994) Oxygen diffusion through the jelly capsules of amphibian eggs. Israel J Zool 40:493–506Google Scholar
- Seymour RS, Bradford DF (1987) Gas exchange through the jelly capsule of the terrestrial eggs of the frog, Pseudophryne bibronii. J Comp Physiol B 157:477–481CrossRefGoogle Scholar
- Seymour RS, Bradford DF (1995) Respiration of amphibian eggs. Physiol Zool 68:1–25Google Scholar
- Seymour RS, Roberts JD (1995) Oxygen uptake by the aquatic eggs of the Australian frog Crinia georgiana. Physiol Zool 68:206–222Google Scholar
- Seymour RS, Geiser F, Bradford DF (1991) Gas conductance of the jelly capsule of terrestrial frog eggs correlates with embryonic stage, not metabolic demand or ambient PO2. Physiol Zool 64:673–687Google Scholar
- Tucker VA (1967) Method for oxygen content and dissociation curves on microliter blood samples. J Appl Physiol 23:410–414PubMedGoogle Scholar
- Warkentin KM (2002) Hatching timing, oxygen availability, and external gill regression in the treefrog, Agalychnis callidryas. Physiol Biochem Zool 75:155–164PubMedCrossRefGoogle Scholar