Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-24T01:43:10.709Z Has data issue: false hasContentIssue false
  • English
  • Français

The relationship between temperature, oxygen condition and embryo encapsulation in the marine gastropod Chorus giganteus

Published online by Cambridge University Press:  27 September 2010

Juan M. Cancino ,
José A. Gallardo  and
Antonio Brante
Juan M. Cancino*
Affiliation:
Departamento de Ecología Costera, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile, UCSC
José A. Gallardo
Affiliation:
Laboratorio de Genética Aplicada, Escuela de Ciencias del Mar, Pontificia Universidad Católica de Valparaíso, Avenida Altamirano 1480, Valparaíso, Chile
Antonio Brante
Affiliation:
Departamento de Ecología Costera, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile, UCSC
*
Correspondence should be addressed to: J.M. Cancino, Departamento de Ecología Costera, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Intracapsular oxygen availability is one of the main factors affecting embryo development of marine gastropod species with encapsulation. This is because the low solubility and diffusion rate of O2 in water, plus the low oxygen diffusion rate that the capsule wall presents, reduces oxygen inside capsules. In addition, temperature affects embryo development inside capsules through its effect on embryo metabolic rate and oxygen availability. In spite of both factors being highly correlated and that a synergic effect on embryo development may be expected, there are few studies evaluating temperature and intracapsular oxygen availability simultaneously. In this work we evaluated the role of the capsule wall of the marine gastropod Chorus giganteus as a barrier for oxygen diffusion and its interaction with temperature affecting intracapsular oxygen availability and embryonic development. For that, we cultivated capsules in seawater at three different temperatures, 9, 12 and 15°C, for a time to complete embryo development. Oxygen level was measured inside capsules with and without embryos, and outside capsules at all temperatures. The number of capsules successfully hatched at the end of the experiment, and early and late embryo mortality were recorded. Finally, we measured embryo metabolic rate at the three different temperatures assayed. We found that embryo mortality and abnormal morphological development were more frequent at higher temperatures. Intracapsular oxygen availability decreases at higher temperatures in capsules with and without embryos. These results may be explained by an increase in the total intracapsular embryo metabolic rate (per capsule) with temperature and an inadequate oxygen diffusion rate from seawater through the capsule wall and intracapsular fluid to the embryonic cells. Our findings suggest that encapsulation is constrained at high temperatures in C. giganetus affecting significantly its reproductive success. This may have important consequences in a scenario of global warming.

Keywords

egg capsulesembryonic developmentoxygen microelectrodenurse eggChorus giganteus
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 3 , May 2011 , pp. 727 - 733
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ahumada, R. (1976) Contribución al conocimiento de las condiciones hidrográficas de la Bahía de Concepción y áreas adyacentes (Chile). Tesis de Licenciatura. Universidad de Concepción.Google Scholar
Ahumada, R. (1994) Condiciones oceanográficas del Golfo de Arauco y Bahías adyacentes. In Della Croce, N. (ed.) El Río Biobío y el Area Marina Adyacente. Chile Central. (Contribuciones). N. Serie monografías científicas. Universidad de Genova, GenovaGoogle Scholar
Baker, S. and Mann, R. (1994) Description of metamorphic phases in the oyster Crassostrea virginica and effects of hypoxia on metamorphosis. Marine Ecology Progress Series 104, 91–99.Google Scholar
Booth, D. (1995) Oxygen availability and embryonic development in sand snail egg masses. Journal of Experimental Biology 198, 241–247.Google Scholar
Brante, A. (2005) An alternative mechanism to reduce intracapsular hypoxia in ovicapsules of Fusititron oregonensis (Gastropoda). Marine Biology 149, 269–274.Google Scholar
Brante, A., Viard, F. and Fernández, M. (2008) Does the intracapsular oxygen availability explain the developmental mode of encapsulated marine gastropods?: answers from the calyptraeid group. Marine Ecology Progress Series 368, 197–207.Google Scholar
Brante, A., Viard, F. and Fernández, M. (2009) Limiting factors to encapsulation: the combined effects of dissolved protein and oxygen availability on embryonic growth and survival of species with contrasting feeding strategies. Journal of Experimental Biology 212, 2287–2295.Google ScholarPubMed
Cancino, J.M., Gallardo, J.A., Torres, F.A., Leiva, G. and Navarro, J.M. (2000) Effects of sessile Protozoa on intracapsular oxygen tension and embryonic shell calcification in the muricid Chorus giganteus. Marine Ecology Progress Series 200, 141–148.Google Scholar
Cancino, J.M., Gallardo, J.A. and Torres, F.A. (2003) Combined effects of dissolved oxygen concentration and water temperature on embryonic development and larval shell secretion in the marine snail Chorus giganteus (Gastropoda: Muricidae). Marine Biology 142, 133–139.Google Scholar
Chaffee, C. and Strathmann, R. (1984) Constraints on egg masses. I. Retarded development within thick egg masses. Journal of Experimental Marine Biology and Ecology 84, 73–83.Google Scholar
Cronin, E.R. and Seymour, R.S. (2000) Respiration of the eggs of the giant cuttlefish Sepia apama. Marine Biology 136, 863–870.Google Scholar
Cohen, C. and Strathmann, R. (1996) Embryos at the edge of tolerance: effects of environment and structure of egg masses on supply of oxygen to embryos. Biological Bulletin. Marine Biological Laboratory, Woods Hole 190, 8–15.Google Scholar
Crump, M.L. (1996) Parental care among the Amphibia. In Rosenblatt, J.S. and Snowdon, C.T. (eds) Advances in the study of behavior. Amsterdam: Elsevier, pp. 109–144.Google Scholar
De Zwaan, A. (1983) Carbohydrate catabolism in bivalves. In Hochachka, P.H. (ed.) The Mollusca, Volume 1. New York: Academic Press, pp. 137–169.Google Scholar
Dick, J.T., Faloon, S.E. and Elwood, R.W. (1998) Active brood care in an amphipod: influences of embryonic development, temperature and oxygen. Animal Behaviour 56, 663–672.Google Scholar
Fernández, M., Bock, C. and Pörtner, H.O. (2000) The cost of being a caring mother: the ignored factor in the reproduction of marine invertebrates. Ecology Letters 3, 487–494.Google Scholar
Fernández, M., Calderón, R., Cancino, J.M. and Jeno, K. (2007) Effect of temperature on the development of encapsulated embryos of Concholepas concholepas along a latitudinal cline. Marine Ecology Progress Series 348, 229–237.Google Scholar
Gallardo, C. (1981) Posturas y estadios de eclosión del gastrópodo muricidae Chorus giganteus (Lesson, 1829). Studies on Neotropical Fauna and Environment 16, 35–44.Google Scholar
Gonzalez, K. and Gallardo, C. (1999) Embryonic and larval development of the muricid snail Chorus giganteus (Lesson, 1829) with an assessment of the development nutrition sourse. Ophelia 51, 77–92.Google Scholar
Hoegh-Guldberg, O. and Pearse, J.S. (1995) Temperature, food availability, and the development of marine invertebrate larvae. American Zoologist 35, 415–425.Google Scholar
Lardies, M.A. and Fernández, M. (2002) Effect of oxygen availability in determining clutch size in Acanthina monodon. Marine Ecology Progress Series 239, 139–146.Google Scholar
Lee, C.E. and Strathmann, R.R. (1998) Scaling of gelatinous clutches: effects of siblings' competition for oxygen on clutch size and parental investment per offspring. American Naturalist 151, 293–310.Google Scholar
Leiva, G.E., Muñoz, J.E. and Navarro, J.M. (1998) Desarrollo intracapsular y mecanismos de eclosión del caracol trumulco Chorus giganteus (Lesson, 1829) (Gastropoda: Muricidae), bajo condiciones de laboratorio. Revista Chilena de Historia Natural 71, 157–167.Google Scholar
Lima, G. and Pechenik, J. (1985) The influence of temperature on growth rate and length of larval life of the gastropod, Crepidula plana. Journal of Experimental Marine Biology and Ecology 90, 55–71.Google Scholar
Llancamil, L.A. (1982) Variación estacional invierno primavera de la temperatura, salinidad y oxígeno en Bahía Coliumo (36°32′S;72°57′W). Tesis de Licenciatura en Biología Marina. Universidad de Concepción.Google Scholar
Maeda-Martínez, A.N. (1985) Studies on the physiology of shell formation in molluscan larvae, with special reference to Crepidula fornicata. PhD thesis. Department of Oceanography, University of Southampton, Southampton.Google Scholar
Moran, A.L. and Woods, A.H. (2007) Oxygen in egg masses: interactive effects of temperature, age, and egg-mass morphology on oxygen supply to embryos. Journal of Experimental Biology 210, 722–731.Google Scholar
Osorio, C., Atria, J. and Mann, S. (1979) Moluscos marinos de importancia económica en Chile. Biología Pesquera 11, 3–47.Google Scholar
Palmer, A.R. (1994) Temperature sensitivity, rate of development and generation time: geographic variation in laboratory-reared Nucella and a cross-phyletic overview. In Wilson, W.H., Stricker, S.A. and Shinn, G.L. (eds) Reproduction and development of marine invertebrates. Baltimore, MD: Johns Hopkins University Press, pp. 177–194.Google Scholar
Pechenik, J. and Lima, G. (1984) Relationship between growth, differentiation, and length of larval life for individually reared larvae of the marine gastropod, Crepidula fornicata. Biological Bulletin. Marine Biological Laboratory, Woods Hole 166, 537–549.Google Scholar
Pörtner, H.O. (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 132, 739–761.Google Scholar
Przeslawski, R. (2004) A review of the effects of environmental stress on embryonic development within intertidal gastropod egg masses. Molluscan Research 24, 43–63.CrossRefGoogle Scholar
Roller, R. and Stickle, W. (1989) Temperature and salinity effects on the intracapsular development, metabolic rates, and survival to hatching of Thais haemastoma caniliculata (Gray) (Prosobranchia: Muricidae) under laboratory conditions. Journal of Experimental Marine Biology and Ecology 125, 235–251.Google Scholar
Strathmann, R.R. and Chaffee, C. (1984) Constraints on egg masses. II Effect of spacing, size and number of eggs on ventilation of masses of embryos in jelly, adherent groups, or thinwalled capsules. Journal of Experimental Marine Biology and Ecology 84, 85–93.Google Scholar
Strathmann, R.R. and Strathmann, M.F. (1982) The relationship between adult size and brooding in marine invertebrates. American Naturalist 119, 91–101.Google Scholar
Strathmann, R.R. and Strathmann, M.F. (1989) Evolutionary opportunities and constraints demonstrated by artificial gelatinous egg masses. In Ryland, J.S. and Tyler, P.A. (eds) Reproduction, genetics and distribution of marine organisms. Copenhagen: Olsen and Olsen, pp. 201–209.Google Scholar
Strathmann, R.R. and Strathmann, M.F. (1995) Oxygen supply and limits on aggregation of embryos. Journal of the Marine Biological Association of the United Kingdom 75, 413–428.Google Scholar