Hostname: page-component-7c8c6479df-7qhmt Total loading time: 0 Render date: 2024-03-27T00:28:12.126Z Has data issue: false hasContentIssue false

A Study on the Digestive Physiology of a Marine Polychaete (Eulalia viridis) through Microanatomical Changes of Epithelia During the Digestive Cycle

Published online by Cambridge University Press:  12 November 2014

Ana P. Rodrigo
Affiliation:
MARE—Marine and Environmental Sciences Centre/IMAR—Instituto do Mar, Departamento de Ciências e Engenharia do Ambiente, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa, 2829-516 Caparica, Portugal
Maria H. Costa
Affiliation:
MARE—Marine and Environmental Sciences Centre/IMAR—Instituto do Mar, Departamento de Ciências e Engenharia do Ambiente, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa, 2829-516 Caparica, Portugal
António Pedro Alves de Matos
Affiliation:
Centro de Estudos do Ambiente e do Mar (CESAM)/Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Quinta da Granja, Monte de Caparica, 2829-511 Caparica, Portugal
Francisco Carrapiço
Affiliation:
Centro de Biologia Ambiental (CBA), Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, 1749-016 Lisboa, Portugal
Pedro M. Costa*
Affiliation:
MARE—Marine and Environmental Sciences Centre/IMAR—Instituto do Mar, Departamento de Ciências e Engenharia do Ambiente, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa, 2829-516 Caparica, Portugal
*
*Corresponding author. pmcosta@fct.unl.pt
Get access

Abstract

As for many invertebrates, the gut of marine polychaete species has key physiological functions. However, studies integrating microanatomical descriptions with physiological processes are scarce. The present investigates histological, histochemical and cytological changes in the alimentary canal during the digestive cycle of the marine annelid Eulalia viridis, a species that combines opportunist scavenging, predation and cannibalistic behavior. The gut is comprised of an eversible pharynx, esophagus, intestine and rectum. Three main phases of digestion were identified, namely, resting/secretory, absorptive and excretory. The intestinal epithelium is complex and exhibited the most significant changes regarding intracellular digestion, excretion and storage. Conversely, the pharynx and esophagus were chiefly important for enzyme secretion. The results also indicate the existence of two distinct types of secretory cells in the intestine, with likely distinct physiological roles. Some similarities have been found between the intestinal epithelia and the molluscan (especially cephalopod) digestive gland, as, for instance, the shedding of apical corpuscles by digestive cells at posterior stages of digestion. The findings indicate that the digestive process in this worm is complex and related to the many physiological roles that cells need to play in the presence of reduced organ differentiation.

Type
SPMicros Special Section
Copyright
© Microscopy Society of America 2014 

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

Bartolomaeus, T., Purschke, G. & Hausen, H. (2005). Polychaete phylogeny based on morphological data—A comparison of current attempts. Hydrobiologia 535/536, 341356.Google Scholar
Boucaud-Camou, E. & Yim, M. (1980). Fine structure and function of the digestive cell of Sepia officinalis (Mollusca: Cephalopoda). J Zool Lond 191, 89105.Google Scholar
Costa, P.M., Carrapiço, F., Alves De Matos, A.P. & Costa, M.H. (2013). A microscopical study of the “chlorophylloid” pigment cells of the marine polychaete Eulalia viridis (L.). Microsc Microanal 19, 1516.Google Scholar
Costa, P.M. & Costa, M.H. (2012). Development and application of a novel histological multichrome technique on whole-body clam histopathology. J Invert Pathol 110, 411414.Google Scholar
Costa, P.M., Rodrigo, A.P. & Costa, M.H. (2014). Microstructural and histochemical advances on the digestive gland of the common cuttlefish, Sepia officinalis L. Zoomorphology 133, 5969.Google Scholar
Emson, R.H. (1977). The feeding and consequent role of Eulalia viridis (O. F. Muller) (Polychaeta) in intertidal communities. J Mar Biol Ass UK 57, 9396.Google Scholar
Fauchald, K. & Jumars, P.A. (1979). The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol Ann Rev 17, 193284.Google Scholar
Fisher, D.B. (1968). Protein staining of ribboned Epon sections for light microscopy. Histochem Cell Biol 16, 9296.Google Scholar
Gram, C. (1884). Ueber die isolirte färbung der schizomyceten in schnitt-und trockenpräparaten. Fortschr Med 2, 185189.Google Scholar
Jenkins, C.D., Ward, M.E., Turnipseed, M., Osterberg, J. & Van Dover, C.L. (2002). The digestive system of the hydrothermal vent polychaete Galapagomystides aristata (Phyllodocidae): evidence for hematophagy? Invertebr Biol 121, 243254.CrossRefGoogle Scholar
Kennedy, G.Y. & Nicol, J.A.C. (1959). Pigments of Chaetopterus variopedatus (Polychaeta). Proc R Soc Lond B 150, 509538.Google Scholar
Kiernan, J.A. (2008). Histological and Histochemical Methods. Theory and Practice. 4th ed. Bloxham: Scion Publishing.Google Scholar
Marsden, J.R. (1968). Routes of excretion of particulate waste in the polychaete, Hermodice carunculata . Can J Zool 46, 619624.CrossRefGoogle Scholar
Martoja, R. & Martoja, M. (1967). Initiation aux Techniques de l’Histologie Animal. Paris, France: Masson.Google Scholar
Michel, C. (1964). Histologie, histochimie et innervation de la trompe d'Eulalia viridis (Müller), (Polychètes Errantes Phyllodocidae). Bull Lab Mar Dinard 49–50, 6295.Google Scholar
Michel, C. (1968). Enzymes digestives de la trompe d'Eulalia viridis (Müller) (Phyllodocidae) et de Glycera convoluta (Keferstein) (Glyceridae) annélides polychètes errantes. Ann Histochim 13, 123134.Google Scholar
Michel, C. (1969 a). Ultrastructure et histochimie de la cuticule pharyngienne chez Eulalia viridis Müller, (Annélide Polychète Errante, Phyllodocidae): Étude de ses rapports avec l'épithélium sous-jacent dans le cycle digestif. Z Zellforsch 98, 5473.Google Scholar
Michel, C. (1969 b). Enzymes digestives intestinales d'Eulalia viridis (Müller) (Phyllodocidae) et de Glycera convoluta (Keferstein) (Glyceridae) annélides polychètes errantes. Ann Histochim 14, 6778.Google Scholar
Michel, C. (1970). Rôle physiologique de la trompe chez quatre annélides polychétes appartenent aux genres: Eulalia, Phyllodoce, Glycera et Notomastus . Cah Biol Mar 9, 209228.Google Scholar
Michel, C. (1977). Tissular localization of the digestive proteases in the sedentary polychaetous annelid Sabellaria alveolata . Mar Biol 44, 265273.CrossRefGoogle Scholar
Moltschaniwskyj, N.A. & Johnston, D. (2006). Evidence that lipid can be digested by the dumpling squid Euprymna tasmanica, but is not stored in the digestive gland. Mar Biol 149, 565572.Google Scholar
Morton, B. (2011). Predator-prey-scavenging interactions between Nucella lapillus, Carcinus maenas and Eulalia viridis all exploiting Mytilus galloprovincialis on a rocky shore recovering from tributyl-tin (TBT) pollution. J Nat Hist 45, 23972417.Google Scholar
Olive, P.J.W. (1975). Reproductive biology of Eulalia viridis (Müller) (Polychaeta: Phyllodocidae) in the North Eastern U.K. J Mar Biol Ass UK 55, 313326.Google Scholar
Pilgrim, M. (1965). The functional anatomy and histology of the alimentary canal of the maldanid polychaetes Clymenella torquata and Euclymene oerstedi . J Zool 147, 387405.Google Scholar
Rouse, G.W. (1988). An ultrastructural study of the spermatozoa of Eulalia sp. (Phyllodocidae), Lepidonotus sp. (Polynoidae), Lumbrineris sp. (Lumbrineridae) and Owenia fusiformis (Oweniidae). Helgolander Meeresun 42, 6778.Google Scholar
Saulnier-Michel, C. (1992). Polychaeta: Digestive system. In Microscopic Anatomy of Invertebrates Vol. 7: Annelida, Harrison, F.W. & Gardiner, S.L. (Eds.), pp. 5369. Hoboken, NJ, USA: Wiley-Liss.Google Scholar
Saulnier-Michel, C., Gail, F., Hily, A., Alberic, P. & Cosson-Manney, M.A. (1990). Structure and functions of the digestive tract of Alvinella pompejana, a hydrothermal vent polychaete. Can J Zool 68, 722732.Google Scholar
Semmens, J.M. (2002). Changes in the digestive gland of the loliginid squid Sepioteuthis lessoniana (Lesson 1830). J Exp Mar Biol Ecol 274, 1939.Google Scholar
Sutton, M.F. (1957). The feeding mechanism, functional morphology and histology of the alimentary canal of Terebella lapidaria L. (Polychaeta). Proc Zool Soc Lond 129, 487523.CrossRefGoogle Scholar
Swift, K., Johnston, D. & Moltschaniwskyj, N. (2005). The digestive gland of the southern dumpling squid (Euprymna tasmanica): structure and function. J Exp Mar Biol Ecol 315, 177186.Google Scholar
Tzetlin, A. & Purschke, G. (2005). Pharynx and intestine. In Morphology, Molecules, Evolution and Phylogeny in Polychaeta and Related Taxa, Bartolomaeus, T. & Purschke, G. (Eds.), pp. 199225. Dordrecht, The Netherlands: Springer.Google Scholar
Tzetlin, A.B., Purschke, G., Westheidet, W. & Saphonov, M.V. (1992). Ultrastructure of enteronephridia and general description of the alimentary canal in Trochonerilla mobilis and Nerillidium troglochaetoides (Polychaeta, Nerillidae). Acta Zool Stockholm 73, 163176.Google Scholar
Weigert, A., Helm, C., Meyer, M., Nickel, B., Arendt, D., Hausdorf, B., Santos, S.R., Halanych, K.M., Purschke, G., Bleidorn, C. & Struck, T.H. (2014). Illuminating the base of the annelid tree using transcriptomics. Mol Biol Evol 31, 13911401.Google Scholar
Welsch, U. & Storch, V. (1970). Histochemical and fine structural observations on the alimentary tract of Aphroditidae and Nephtyidae (Polychaeta Errantia). Mar Biol 6, 142147.Google Scholar