Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-28T00:14:12.059Z Has data issue: false hasContentIssue false
  • English
  • Français

Seasonal and starvation-induced changes on gonads and lipid reserves of the digestive gland of Nucella lapillus (Caenogastropoda)

Published online by Cambridge University Press:  30 August 2012

Catarina Inês Gonçalves  and
Alexandre Lobo-da-cunha
Catarina Inês Gonçalves
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, 4050-313 Porto, Portugal; Centre of Marine and Environmental Research (CIIMAR), 4050-123 Porto, Portugal
Alexandre Lobo-da-cunha*
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, 4050-313 Porto, Portugal; Centre of Marine and Environmental Research (CIIMAR), 4050-123 Porto, Portugal
*
Correspondence should be addressed to: A. Lobo-da-Cunha, Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), Rua Jorge, Viterbo Ferreira 28, 4050-313 Porto, Portugal email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This study was conceived to evaluate seasonal changes in the lipid reserves of the digestive gland of the carnivorous intertidal caenogastropod Nucella lapillus, using a stereological approach. Volume density of lipid droplets in the digestive gland, digestive gland weight and volume were assessed in animals collected in March, June, September and December on the Portuguese coast. Gonad development was evaluated to detect any relationship between lipid content in the digestive gland and the reproductive cycle. The quantitative light microscopic analysis demonstrates that lipid droplets are a major component of the digestive gland. In males, the digestive gland and its lipid reserves were quite stable without significant variations throughout the year. In females, the percentage of digestive gland volume occupied by lipid droplets was higher in June and December, coinciding with the highest values of digestive gland volume. Due to the conjugation of these two factors, in June and December the total amount of lipids in the digestive gland was substantially increased in females. In both males and females a relationship between the development status of the gonad and the lipid reserves of the digestive gland was not evident. However, significant differences in the digestive gland lipid reserves were detected between males and females in June and December, pointing to a sex related effect on lipid reserves. To evaluate the use of lipid reserves as energy source in N. lapillus, the consumption of digestive gland lipids was followed during a starvation experiment.

Keywords

Gastropodastereologyreproductionlipidsdigestive glandmicroscopy
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 3 , May 2013 , pp. 817 - 824
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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

Barber, B.J. and Blake, N.J. (1991) Reproductive physiology. In Shumway, S.E. (ed.) Scallops: biology, ecology and aquaculture. New York: Elsevier, pp. 377–428 Google Scholar
Crothers, J.H. (1985) Dog-whelks: an introduction to the biology of Nucella lapillus (L.). Field Studies 6, 291–360.Google Scholar
Da Silva, R.S.M. and Zancan, D.M. (1994) Seasonal variations of the carbohydrate and lipid metabolism in a land pulmonate gastropod, Megalobulimus oblongus . Comparative Biochemistry and Physiology, Part A: Physiology 108A, 337–341.Google Scholar
Dimitriadis, V.K. and Andrews, E.B. (2000) Ultrastructural and cytochemical study of the digestive gland cells of the marine prosobranch mollusc Nucella lapillus (L.) in relation to function. Malacologia 42, 103–112.Google Scholar
Dimitriadis, V.K. and Hondros, D. (1992) Effect of starvation and hibernation on the fine structural morphology of digestive gland cells of the snail Helix lucorum . Malacologia 34, 63–73.Google Scholar
Feare, C.J. (1970) The reproductive cycle of the dog whelk Nucella lapillus . Proceedings of the Malacological Society of London 39, 125–137.Google Scholar
Følsvik, N., Berge, J.A., Brevik, E.M. and Walday, M. (1999) Quantification of organotin compounds and determination of imposex in populations of dogwhelks (Nucella lapillus) from Norway. Chemosphere 38, 681–391.Google Scholar
Franchini, A. and Ottaviani, E. (1993) Histochemical and ultrastructural study of the digestive gland of the freshwater snail Panorbarius corneus (L.) (Gastropoda, Pulmonata). Animal Biology 2, 191–198.Google Scholar
Galante-Oliveira, S., Oliveira, I., Ferreira, N., Santos, J.A., Pacheco, M. and Barroso, C. (2011) Nucella lapillus L. imposex levels after legislation prohibiting TBT antifoulants: temporal trends from 2003 to 2008 along the Portuguese coast. Journal of Environmental Monitoring 13, 304–312.Google Scholar
Ganter, P. and Jollès, G. (1970) Histochimie normal et pathologique. Paris: Gauthier-Villars.Google Scholar
Hughes, R.N. (1972) Annual production of two Nova Scotian populations of Nucella lapillus (L.). Oecologia 8, 356–370.Google Scholar
Kress, A., Schmekel, L. and Nott, J.A. (1994) Ultrastructure of the digestive gland in the opisthobranch mollusk, Runcina . Veliger 37, 358–373.Google Scholar
Largen, M.J. (1967) The influence of water temperature upon the life of the dog-whelk Thais lapillus (Gastropoda: Prosobranchia). Journal of Animal Ecology 36, 207–214.CrossRefGoogle Scholar
Le Pennec, G., Le Pennec, M. and Beninger, G. (2001) Seasonal digestive gland dynamics of the scallop Pecten maximus in the Bay of Brest (France). Journal of the Marine Biological Association of the United Kingdom 81, 663–671.Google Scholar
Leung, K.M.Y. and Furness, R.W. (2001) Survival, growth, metallothionein and glycogen levels of Nucella lapillus (L.) exposed to sub-chronic cadmium stress: the influence of nutritional state and prey type. Marine Environmental Research 52, 173–194.Google Scholar
Litaay, M. and De Silva, S. (2003) Spawning season, fecundity and proximate composition of the gonads of wild-caught blacklip abalone (Haliotis rubra) from Port Fairy waters, south-eastern Australia. Aquatic Living Resources 16, 353–361.Google Scholar
Lobo-da-Cunha, A. (1999) Ultrastructural and cytochemical aspects of the basophilic cells in the hepatopancreas of Aplysia depilans (Mollusca, Opistobranchia). Tissue and Cell 31, 8–16.Google Scholar
Lobo-da-Cunha, A. (2000) The digestive cells of the hepatopancreas in Aplysia depilans (Mollusca, Opisthobranchia): ultrastructural and cytochemical study. Tissue and Cell 32, 49–57.Google Scholar
Lobo-da-Cunha, A., Kádár, E. and Serrão Santos, R. (2006) Histochemical and ultrastructural characterization of mantle storage cells in the hydrothermal-vent bivalve Bathymodiolus azoricus . Marine Biology 150, 253–260.Google Scholar
Morais, S., Boaventura, D., Narciso, L., Ré, P. and Hawkins, S.J. (2003) Gonad development and fatty acid composition of Patella depressa Pennant (Gastropoda: Prosobranchia) populations with different patterns of spatial distribution, in exposed and sheltered sites. Journal of Experimental Marine Biology and Ecology 294, 61–80.Google Scholar
Morton, B. (2009) Recovery from imposex by a population of the dogwhelk, Nucella lapillus (Gastropoda: Caenogastropoda), on the southeastern coast of England since May 2004: a 52-month study. Marine Pollution Bulletin 58, 1530–1538.Google Scholar
Pazos, A.J., Ruíz, C., García-Martin, O., Abad, M. and Sánchez, J.L. (1996) Seasonal variations of the lipid content and fatty acid composition of Crassostrea gigas cultured in El Grove, Galicia, N.W. Spain. Comparative Biochemistry and Physiology, Part B: Biochemistry and Molecular Biology 114, 171–179.Google Scholar
Pazos, A.J., Sánchez, J.L., Román, G., Pérez-Parallé, M.L. and Abad, M. (2003) Seasonal changes in lipid classes and fatty acid composition in the digestive gland of Pecten maximus . Comparative Biochemistry and Physiology, Part B: Biochemistry and Molecular Biology, 134, 367–380.Google Scholar
Plejdrup, J.K., Simonsen, V., Pertoldi, C., Schøyen, M. and Bayley, M. (2006) Genetic and morphological diversity in populations of Nucella lapillus (L.; neogastropoda) in response to tributyltin contamination. Ecotoxicology and Environmental Safety 64, 146–154.Google Scholar
Robinson, W.E., Wehling, W.E., Morse, M.P. and McLeod, G.C. (1981) Seasonal changes in soft-body component indices and energy reserves in the Atlantic deep-sea scallop, Placopecten magellanicus . Fishery Bulletin, US 79, 449–458.Google Scholar
Royet, J.P. (1991) Stereology: a method for analyzing images. Progress in Neurobiology 37, 433–474.Google Scholar
Santos, M.M., Castro, L.F., Vieira, M.N., Micael, J., Morabito, R., Massanisso, P. and Reis-Henriques, M.A. (2005) New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus . Comparative Biochemistry and Physiology, Part C: Toxicology and Pharmacology 141, 101–109.Google Scholar
Scherle, W. (1970) A simple method for volumetry of organs in quantitative stereology. Mikroskopie 26, 57–60.Google Scholar
Thiery, J.P. (1967) Mise en evidence des polysaccharides sur coupes fines en microscopic electronique. Journal de Microscopie 6, 987–1018.Google Scholar
Voltzow, J. (1994) Gastropoda: Prosobranchia. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates. Volume 5. New York: Wiley-Liss, pp. 111–252.Google Scholar