Abstract
Low pO2 values have been measured in the perivitelline fluids (PVF) of marine animal eggs on several occasions, especially towards the end of development, when embryonic oxygen consumption is at its peak and the egg case acts as a massive barrier to diffusion. Several authors have therefore suggested that oxygen availability is the key factor leading to hatching. However, there have been no measurements of PVF pCO2 so far. This is surprising, as elevated pCO2 could also constitute a major abiotic stressor for the developing embryo. As a first attempt to fill this gap in knowledge, we measured pO2, pCO2 and pH in the PVF of late cephalopod (Sepia officinalis) eggs. We found linear relationships between embryo wet mass and pO2, pCO2 and pH. pO2 declined from >12 kPa to less than 5 kPa, while pCO2 increased from 0.13 to 0.41 kPa. In the absence of active accumulation of bicarbonate in the PVF, pH decreased from 7.7 to 7.2. Our study supports the idea that oxygen becomes limiting in cephalopod eggs towards the end of development; however, pCO2 and pH shift to levels that have caused significant physiological disturbances in other marine ectothermic animals. Future research needs to address the physiological adaptations that enable the embryo to cope with the adverse abiotic conditions in their egg environment.
References
Brante A (2006) An alternative mechanism to reduce intracapsular hypoxia in ovicapsules of Fusitriton oregonensis (Gastropoda). Mar Biol (Berl) 149:269–274. doi:https://doi.org/10.1007/s00227-005-0199-7
Burggren W (1985) Gas-exchange, metabolis, and ventilation in gelatinous frog egg masses. Physiol Zool 58:503–514
Cameron JN (1986) Acid–base equilibria in invertebrates. In: Heisler N (ed) Acid-base regulation in animals. Elsevier, Amsterdam, pp 357–394
Chaffe C, Strathmann RR (1984) Constraints on egg mass. 1. Retarded development within thick egg masses. J Exp Mar Biol Ecol 84:73–83
Cohen CS, 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. doi:https://doi.org/10.2307/1542671
Cronin ER, Seymour RS (2000) Respiration of the eggs of the giant cuttlefish Sepia apama. Mar Biol (Berl) 136:863–870. doi:https://doi.org/10.1007/s002270000274
Decleir W, Lemaire J, Richard A (1971) The differentiation of blood proteins during ontogeny in Sepia officinalis L. J Comp Biochem Physiol 40B:923–930. doi:https://doi.org/10.1016/0305-0491(71)90038-1
Dejours P (1975) Principles of comparative respiratory physiology. North. Holl. Publ. Comp, Amsterdam
Dewachter B, Wolf G, Richard A, Decleir W (1988) Regulation of respiration during juvenile development of Sepia officinalis (Mollusca, Cephalopoda). Mar Biol (Berl) 97:365–371. doi:https://doi.org/10.1007/BF00397767
Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A 34:1733–1743. doi:https://doi.org/10.1016/0198-0149(87)90021-5
Diez JM, Davenport J (1987) Embryonic respiration in the spiny dogfish (Scyliorhinus canicula L.). J Mar Biol Assoc UK 67:249–261
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432. doi:https://doi.org/10.1093/icesjms/fsn048
Fernandez M, Bock C, Portner HO (2000) The cost of being a caring mother: the ignored factor in the reproduction of marine invertebrates. Ecol Lett 3:487–494. doi:https://doi.org/10.1046/j.1461-0248.2000.00172.x
Fernandez M, Pardo LM, Baeza JA (2002) Patterns of oxygen supply in embryo masses of brachyuran crabs throughout development: the effect of oxygen availability and chemical cues in determining female brooding behavior. Mar Ecol Prog Ser 245:181–190. doi:https://doi.org/10.3354/meps245181
Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457
Gutowska MA, Pörtner HO, Melzner F (2008). Growth and calcification in the cephalopod Sepia officinalis under elevated seawater pCO2. Mar Ecol Progress Ser (accepted)
Heisler N (1986) Acid–base regulation in fishes. In: Heisler N (ed) Acid–base regulation in animals. Elsevier, Amsterdam, pp 309–356
Johansen K, Brix O, Lykkeboe G (1982) Blood gas transport in the cephalopod Sepia officinalis. J Exp Biol 99:331–338
Kress A (1972) Changes in egg-capsule volumes during development of different opisthobranch species (Mollusca, Gastropoda). Mar Biol 16:236
Kugel B, Peterson RH (1989) Perivitelline fluid of rainbow trout (Oncorhynchus mykiss) eggs in relation to ambient pH. Can J Fish Aquat Sci 46:2070–2073
Lemaire J (1970) Table de développement embryonnaire de Sepia officinalis L. (Mollusque Céphalopode). Bull Soc Zool Fr 95:773–782
Lenfant C, Aucutt C (1966) Measurement of blood gases by gas chromatography. Respir Physiol 1(4):398–407. doi:https://doi.org/10.1016/0034-5687(66)90007-7
Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory. U.S. Department of Energy, Oak Ridge
Mehrbach C, Culberso Ch, Hawley JE, Pytkowic Rm (1973) Measurement of apparent dissociation constants of carbonic acid in seawter at atmospheric pressure. Limnol Oceanogr 18:897–907
Melzner F (2005) Systemic investigations on the physiology of temperature tolerance in the common cuttlefish Sepia officinalis. PhD Thesis, University of Bremen, Bremen, Germany. urn:nbn: de:gbv:46-diss000106137
Melzner F, Mark FC, Pörtner HO (2007) Role of blood-oxygen transport in thermal tolerance of the cuttlefish, Sepia officinalis. Integr Comp Biol 47:645–655. doi:https://doi.org/10.1093/icb/icm074
Michaelidis B, Ouzounis C, Paleras A, Portner HO (2005) Effects of long-term moderate hypercapnia on acid–base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar Ecol Prog Ser 293:109–118. doi:https://doi.org/10.3354/meps293109
Pörtner HO, Boutilier RG, Tang Y, Toews DP (1990) Determination of intracellular pH and pCO2 after metabolic inhibition by fluoride and nitrilotriacetic acid. Respir Physiol 81:255–274. doi:https://doi.org/10.1016/0034-5687(90)90050-9
Pörtner HO, Webber DM, Boutilier RG, Odor RK (1991) Acid–base regulation in exercising squid (Illex illecebrosus, Loligo pealei). Am J Physiol 261:R239–R246
Rombough PJ (1988) Growth, aerobic metabolism, and dissolved oxygen requirements of embryos and alevins of steelhead, Salmo gairnderi. Can J Zool Revue Can De Zool 66:651–660. doi:https://doi.org/10.1139/z88-097
Seymour RS (1994) Oxygen diffusion through the jelly capsules of amphibian eggs. Isr J Zool 40:493–506
Seymour RS, Bradford DF (1995) Respiration of amphibian eggs. Physiol Zool 68:1–25
Sikes CS, Okazaki K, Fink RD (1981) Respiratory CO2 and the supply of inorganic carbon for calcification of sea urchin embryos. Comp Biochem Physiol Physiol 70:285–291. doi:https://doi.org/10.1016/0300-9629(81)90181-X
Wolf G, Verheyen E, Vlaeminck A, Lemaire J, Decleir W (1985) Respiration of Sepia officinalis during embryonic and early juvenile life. Mar Biol (Berl) 90:35–39. doi:https://doi.org/10.1007/BF00428212
Vleck CM, Hoyt DF (1991) Metabolism and energetics of reptilian and avian embryos. In: Ferguson MWJ, Deeming DC (eds) Egg incubation its effects in embryonic development in birds, reptiles. Cambridge Univ Press, Cambridge, pp 285–306
Acknowledgments
We thank M.P. and R. Chichery, Universite de Caen, France, for provision of cuttlefish eggs. M.A.G. was supported by the German Academic Exchange Service (DAAD) and the AWI MARCOPOLI Program. F.M. was supported by the DFG Excellence Cluster ‘Future Ocean’.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by U. Sommer.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary movie S1 (AVI 37797 kb)
Rights and permissions
About this article
Cite this article
Gutowska, M.A., Melzner, F. Abiotic conditions in cephalopod (Sepia officinalis) eggs: embryonic development at low pH and high pCO2 . Mar Biol 156, 515–519 (2009). https://doi.org/10.1007/s00227-008-1096-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-008-1096-7