Morphology of the digestive gland of the marine panpulmonate limpet Siphonaria lessonii: A cytological, histochemical, and ultrastructural description.


Journal

Journal of morphology
ISSN: 1097-4687
Titre abrégé: J Morphol
Pays: United States
ID NLM: 0406125

Informations de publication

Date de publication:
10 2019
Historique:
received: 18 03 2019
revised: 19 06 2019
accepted: 03 07 2019
pubmed: 18 7 2019
medline: 2 5 2020
entrez: 18 7 2019
Statut: ppublish

Résumé

The molluskan digestive gland has been widely studied and its structural and ultrastructural descriptions have allowed the understanding of its several functions. Despite siphonarids are broadly distributed around the world, morphological studies on their digestive system are poorly represented. The panpulmonate limpet Siphonaria lessonii is the most abundant gastropod and the dominant herbivore in the rocky intertidal coast of Buenos Aires. The aim of this study was to describe the morphology, histology, ultrastructure, and histochemistry of the digestive gland of this gastropod as well as the cycle of activity of digestion. For that, different histochemical techniques along with light microscopy, transmission electron microscopy, and scanning electron microscopy were employed. This study revealed a complex epithelium, composed of a simple layer with five cell types. Digestive cells and vacuolated cells are responsible for intracellular digestion and energy accumulation; basophilic cells, secrete substances that would be involved in extracellular digestion; pigmented cells might have an excretory function and thin cells would correspond to undifferentiated cells. In addition, the tubules present a changing morphology according to the digestive activity that they undergo. As S. lessonii is a grazer that feeds continuously, the cycle of activity of the digestive gland seems to be daily.

Identifiants

pubmed: 31313864
doi: 10.1002/jmor.21043
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1475-1484

Informations de copyright

© 2019 Wiley Periodicals, Inc.

Références

Abolins-Krogis, A. (1961). The histochemistry of the hepatopancreas of Helix pomatia (L). In relation to the regeneration of the shell. Arkiv for Zoologi, 13, 159-201.
Adami, M. L. (2008). Efectos de la herbivoría de la lapa Siphonaria lessoni Blainville, 1824 (Gastropoda) sobre la comunidad asociada a Brachidontes rodriguezii (d'Orbigny, 1846) (Bivalvia). Revista Museo Argentino de Ciencias Naturales, 10, 309-317.
Almendros, A., & Porcel, l. D. (1992). Phosphatase activity in the hepatopancreas of Helix aspersa. Comparative Biochemistry and Physiology A, 103, 455-460.
Aranda, D., & Frenkiel, L. (2012). Digestive gland structure as a feed index for juveniles of the queen conch, Strombus gigas, reared with formulated food. Aquaculture Nutrition, 18, 581-588.
Arrighetti, F., Teso, V., & Penchaszadeh, P. E. (2015). Ultrastructure and histochemistry of the digestive gland of the giant predator Adelomelon beckii (Caenogastropoda: Voludidae) from the SW Atlantic. Tissue and Cell, 47, 171-177.
Bancroft, J. D., Layton, C., & Suvarna, S. K. (2013). Bancroft's theory and practice of histological techniques (7th ed.). London, UK: Churchill Livingstone, Elsevier.
Baqueiro Cárdenas, E., Frenkiel, L., Zetina Zarate, A., & Aldana Aranda, D. (2007). Coccidian (Apicomplexa) parasite infecting Strombus gigas Linne, 1758 digestive gland. Journal of Shellfish Research, 26, 1-3.
Bastida, R., Capezzani, A., & Torti, M. R. (1971). Fouling organisms in the port of Mar del Plata (Argentina). I. Siphonaria lessoni: Ecological and biometric aspects. Marine Biology, 10, 297-307.
Beshr, S. M. (2000). Ecotoxicological studies on two species of snails and associated insects, infesting fruit trees, in three Egyptian governorates. (Marine science thesis). Alexandria University.
Billett, F., & McGee-Russell, S. M. (1955). The histochemical localization of β-glucuronidase in the digestive gland of the Roman snail (Helix pomatia). Journal of Cell Science, 3, 35-48.
Boghen, A., & Farley, J. (1974). Phasic activity in the digestive gland cells of the intertidal prosobranch, Littorina saxatilis (Olivi) and its relations to the tidal cycle. Proceedings of the Malacological Society of London, 41, 41-56.
Carriker, M. R. (1946). Observations on the functioning of the alimentary system of the snail Lymnaea stagnalis appressa Say. Biological Bulletin, 91, 88-111.
Chabicovsky, M., Klepal, W., & Dallinger, R. (2004). Mechanisms of cadmium toxicity in terrestrial pulmonates: Programmed cell death and metallothionein overload. Environmental Toxicology and Chemistry, 23, 648-655.
Costa, P., Rodrigo, A., & Costa, M. H. (2013). Microstructural and histochemical advances on the digestive gland of the common cuttlefish, Sepia officinalis L. Zoomorphology, 133, 59-69. https://doi.org/10.1007/s00435-013-0201-8
Dellagnola, F., Vega, I., & Castro-Vazquez, A. (2017). Evidence for a prokaryotic origin of intracellular corpuscles in the digestive gland of the queen conch Lobatus gigas (Linnaeus, 1758) (Gastropoda: Strombidae). Journal of Molluscan Studies, 83, 186-193.
Di Giorgio, G., Gilardoni, C., & Ituarte, C. (2014). Pathology of Haplosporidium patagon affecting siphonariid gastropods in Patagonia. Diseases of Aquatic Organisms, 112, 59-67.
Dimitriadis, V. K., & 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.
Dimitriadis, V. K., & Hondros, D. (1992). Effect of starvation and hibernation on the fine structural morphology of digestive gland cells of the snail Helix lucorum. Malacología, 34, 63-73.
Fackrell, D. G., & Ali, S. M. (2018). Effects of bacteria Bacillus thuringiensis (Bt) on the digestive system of the land snail Eobania vermiculata. International Journal of Ecotoxicology and Ecobiology, 3, 17-21.
Fretter, V. (1952). Experiments with P32 and I131 on species of Helix, Arion, and Agriolimax. Quarterly Journal Microscopical Science, 93, 135-146.
Fretter, V. (1975). Introduction. In V. Fretter & J. Peake (Eds.), Pulmonates. Functional anatomy and physiology (pp. 11-29). London: Academic Press.
Griebel, R. (1993). Fine structure of the three cell types found in the digestive gland of Elysia viridis (Opisthobranchia: Sacogloss). The Veliger, 63, 10-114.
Gros, O., Frenkiel, L., & Aldana Aranda, D. (2009). Structural analysis of the digestive gland of the queen conch Strombus gigas in relation with the presence of intracellular parasites. Journal of Molluscan Studies, 75, 59-68.
Güller, M., Zelaya, D. G., & Ituarte, C. (2016). How many Siphonaria species (Gastropoda: Euthyneura) live in southern South America? Journal of Molluscan Studies, 82, 80-96.
Hamed, S. S., Abdelmeguied, N. E., Essawy, A. E., Radwan, M. A., & Hegazy, A. E. (2007). Histological and ultrastructural changes induced by two carbamate molluscicides on the digestive gland of Eobania vermiculata. Journal of Biological Sciences, 7, 1017-1037.
Heiba, F. N., Al-Sharkawy, I. M., & Al-Batal, A. A. (2002). Effects of the insecticide lannate, on the land snails, Eobania vermiculata and Monacha contiana, under laboratory conditions. Journal of Biological Sciences, 2, 8-13.
Henry, M., Boucaud-Camou, E., & Lefort, Y. (1991). Functional micro-anatomy of the digestive gland of the scallop Pecten maximus (L.). Aquatic Living Resources, 4, 191-202.
Hödl, E., Felder, E., Chabicovsky, M., & Dallinger, R. (2010). Cadmium stress stimulates tissue turnover in Helix pomatia: Increasing cell proliferation from metal tolerance to exhaustion in molluscan midgut gland. Cell and Tissue Research, 341, 159-171.
Knack de Almeida, H., & Giménez, J. (2018). Gonad characterization and reproductive seasonality in Siphonaria lessonii (Gastropoda: Heterobranchia) from the southwestern Atlantic Ocean. Invertebrate Biology, 137, 264-277.
Koch, E., Vega, I. A., Albrecht, E. A., Ortega, H. H., & Castro-Vazquez, A. (2006). A light and electron microscopic study of pigmented corpuscles in the midgut gland and feces of Pomacea canaliculata (Caenogastropoda: Ampullariidae). The Veliger, 48, 17-25.
Kress, A., Schmekel, L., & Nott, J. A. (1994). Ultrastructure of the digestive gland in the opisthobranch mollusc, Runcina. The Veliger, 37, 358-373.
Laitano, M. V., & Fernández-Giménez, A. V. (2016). Are mussels always the best bioindicators? Comparative study on biochemical responses of three marine invertebrate species to chronic port pollution. Bulletin of Environmental Contamination and Toxicology, 97, 50-55.
Laitano, M. V., Silva Barni, M. F., Costa, P. G., Cledón, M., Fillmann, G., Miglioranza, K. S. B., & Panarello, H. O. (2016). Different carbon sources affect PCB accumulation by marine bivalves. Marine Environmental Research, 113, 62-69.
Lobo-da-Cunha, A. (1999). Ultrastructural and cytochemical aspects of the basophilic cells in the hepatopanchreas of Aplysia depilans (Mollusca, Opisthobranchia). Tissue and Cell, 31, 8-16.
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.
Lobo-da-Cunha, A. (2001). Ultrastuctural histochemical study of the salivary glands of Aplysia depilans (Mollusca, Opisthobranchia). Acta Zoologica, 82, 201-212.
Lobo-da-Cunha, A., Alves, A., Oliveira, E., Guimarães, F., & Calado, G. (2018). Endocytosis, lysosomes, calcium storage and other features of digestive-gland cells in cephalaspidean gastropods (Euopisthobranchia). Journal of Molluscan Studies, 84, 451-462.
Martin, G. G., Bessette, T., Martin, A., Cotero, R., Vumbaco, K., & Oakes, C. (2010). Morphology of epithelial cells lining the digestive tract of the giant keyhole limpet, Megathura crenulata (Mollusca; Vetigastropoda). Journal of Morphology, 27, 1134-1151.
McQuiston, R. W. (1969). Cyclic activity in the digestive diverticula of Lasaea rubra (Montagu) (Bivalvia: Eulamellibranchia). Journal of Molluscan Studies, 38(6), 483-492.
Meenakshi, V. H. (1955). The excretory spherioles in the digestive gland of Pila virens. Journal of Animal Morphology and Physiology, 3(2), 75-78.
Merdsoy, B., & Farley, J. (1973). Phasic activity in the digestive gland cells of the marine prosobranch gastropod, Littorina littorea (L.). Proceedings of the Malacological Society of London, 40, 473-482.
Mersal, H. T. (1990). Changes induced in one land snail of agriculture importance in Egypt. (M.Sc. thesis). Faculty of Girls, Ain Shams University.
Morton, B. (1971). The diurnal rhythm and tidal rhythm of feeding and digestion in Ostrea edulis. Biological Journal of the Linnean Society, 3, 329-342.
Morton, B. (1979). The diurnal rhythm and the cycle of feeding and digestion in the slug Deroceras caruanae. Journal Zoology London, 187, 135-152.
Murty, K. V. R., Shameem, A., & Umadevi, K. (2013). Feeding, anatomy and digestive enzymes of false limpet Siphonaria guamensis. World Journal of Fish and Marine Science, 5, 104-109.
Nelson, L., & Morton, J. E. (1979). Cyclic activity and epithelial renewal in the digestive gland tubules of the marine prosobranch Maoricrypta monoxila (Lesson). Journal of Molluscan Studies, 45, 262-283.
Nuñez, J. D., Laitano, M. V., & Cledón, M. (2012). An intertidal limpet species as a bioindicator: Pollution effects reflected by shell characteristics. Ecological Indicators, 14, 178-183.
Ojeda, M., Arrighetti, F., & Giménez, J. (2015). Morphology and cyclic activity of the digestive gland of Zidona dufresnei (Caenogastropoda: Volutidae). Malacologia, 58, 157-165.
Olivier, S. R., & Penchaszadeh, P. E. (1968). Observaciones sobre la ecología y biología de Siphonaria (Pachysiphonaria) lessoni (Blainivlle, 1824) (Gastropoda, Siphonariidae) en el litoral rocoso de Mar del Plata (Buenos Aires). Cahiers de Biologie Marine, 9, 469-491.
Owen, G. (1970). The fine structure of the digestive tubules of the marine bivalve Cardium edule. Philosophical Transactions of the Royal Society, 258, 245-260.
Owen, G. (1973). The fine structure and histochemistry of the digestive diverticula of the protobranchiate bivalve Nucula sulcata. Proceeding of the Royal Society of London B, 183, 249-264.
Pal, S. G. (1972). The fine structure of the digestive tubules of Mya arenaria L. II. Digestive cell. Journal of Molluscan Studies, 40, 161-170.
Rodrigo, A. P., & Costa, P. M. (2017). The role of the cephalopod digestive gland in the storage and detoxification of marine pollutants. Frontiers in Physiology, 8(1-9), 232.
Ruthensteiner, B. (2006). Redescription and 3D morphology of Williamia gussonii (Gastropoda: Siphonariidae). Journal of Molluscan Studies, 72, 327-336.
Sumner, A. T. (1965). The cytology and histochemistry of the digestive gland cells of Helix. Quarterly Journal of Microscopical Science, 106, 173-192.
Tablado, A., & López Gappa, J. J. (2001). Morphometric diversity of the pulmonate limpet Siphonaria lessoni in different coastal environments. Scientia Marina, 65, 33-42.
Tablado, A., López Gappa, J. J., & Magaldi, N. H. (1994). Growth of the pulmonate limpet Siphonaria lessoni (Blainville) in a rocky intertidal area affected by sewagepollution. Journal of Experimental Marine Biology and Ecology, 175, 211-226.
Taïeb, N. (2001). Distribution of digestive tubules and fine structure of digestive cells of Aplysia punctata (Cuvier, 1803). Journal of Molluscan Studies, 67, 169-182.
Taïeb, N., & Vicente, N. (1999). Histochemistry and ultrastructure of the crypt cells in the digestive gland of Aplysia punctata (Cuvier, 1803). Journal of Molluscan Studies, 65, 385-398.
Thiele, G. (1953). Vergleichende Untersuchungen über den Feinbau und die Funktion der Mitteldarmdrüse einheimischer Gastropoden. Zeitschrift fürZellforschung und Mikroskopische Anatomie, 38, 87-138.
Vega, I. A., Damborenea, M. C., Gamarra-Luques, C., Koch, E., Cueto, J. A., & Castro-Vazquez, A. (2006). Facultative and obligate symbiotic associations of Pomacea canaliculata (Caenogastropoda, Ampullariidae). Biocell, 30, 367-375.
Volland, J. M., Frenkiel, L., Aldana Aranda, D., & Gros, O. (2010). Occurrence of Sporozoa-like microorganisms in the digestive gland of various species of Strombidae. Journal of Molluscan Studies, 76, 196-198.
Walker, G. (1970). The cytology, histochemestry, and ultrastructure of the cell types found in the digestive gland of the slug, Agriolimax reticulatus (Müller). Protoplasma, 71, 91-109.
Zaldibar, B., Cancio, I., Soto, M., & Marigómez, I. (2008). Changes in cell-type composition in digestive gland of slugs and its influence in biomarkers following transplantation between a relatively unpolluted and a chronically metal-polluted site. Environmental Pollution, 156, 367-379.

Auteurs

Sonia M Landro (SM)

Laboratorio de Ecosistemas costeros, plataforma y Mar profundo, Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Ciudad de Buenos Aires, Argentina.

Valeria Teso (V)

Laboratorio de Ecosistemas costeros, plataforma y Mar profundo, Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Ciudad de Buenos Aires, Argentina.

Florencia Arrighetti (F)

Laboratorio de Ecosistemas costeros, plataforma y Mar profundo, Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Ciudad de Buenos Aires, Argentina.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH