2014 • In Journal of Crustacean Biology: A Quarterly of the Crustacean Society for the Publication of Research on Any Aspect of the Biology of Crustacea, 34 (5), p. 539-551
[en] On the basis of macroscopic aspects (body and eye colour, lipid droplets), it was possible to sort specimens of Gammarus pulex (Linnaeus, 1758) into five categories that correspond to moult periods and stages (A, B, C, D1 and D2) based on integument features (tergite cuticle stiffness, layers and thickness). These stages also correspond to changes in digestive tract histology (gut content, cell ultrastructure, and lipid storage). With reference to the pereion tergite integument, this makes it possible to standardize moulting stage terminology and criteria with those applied to decapods while validating a quick, simple, moult-staging method that avoids injury and informs us about the physiology of the whole organism. The moult cycle was very short (about 12-15 days), with a "virtual," practically non-existent, anecdysis or "integument resting period" between post-ecdysis and pre-ecdysis. The pore canals previously known to be "open to the outside" appeared closed at early post-ecdysis by a lipid-rich fillng material that could be responsible for the cuticular waterproofing barrier allowing mineral deposition. In the digestive tract, the main structural changes were late post-ecdysial loss of midgut cells and digestive gland B-cells (probably by extrusion) when restarting the feeding cycle. Pre-ecdysial increase and post-ecdysial decrease in storage lipids are also obvious. We present a quick moult-staging method to sort a great number of G. pulex for physiological or toxicological assays investigating how animals at specific periods of their moult cycle respond to both natural and anthropogenic environmental changes.
Trevisan, Mélissa ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire de Morphologie fonctionnelle et évolutive
Leroy, Delphine; Université de Liège - ULiège > Biologie, Ecologie & Evolution > Laboratoire d'Ecologie Animale et d'Ecotoxicologie
Decloux, Nicole ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire de Morphologie Fonctionnelle et Evolutive
Thomé, Jean-Pierre ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Compère, Philippe ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire de Morphologie Fonctionnelle et Evolutive
Title :
Moult-related changes in the integument, midgut, and digestive gland in the freshwater amphipod gammarus pulex
Publication date :
10 September 2014
Journal title :
Journal of Crustacean Biology: A Quarterly of the Crustacean Society for the Publication of Research on Any Aspect of the Biology of Crustacea
Al-Mohanna, S. Y., and J. A. Nott. 1986. B-cells and digestion in the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda). Journal of the Marine Biological Associations of the United Kingdom 66: 403-414.
Al-Mohanna, S. Y., and J. A. Nott. 1987. R-cells and the digestive cycle in Penaeus semisulcatus (Crustacea: Decapoda). Marine Biology 95: 129-137.
Al-Mohanna, S. Y., and J. A. Nott. 1989. Functional cytology of the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda) during the moult cycle. Marine Biology 101: 535-544.
Al-Mohanna, S. Y., and J. A. Nott D. J. W. Lane. 1985. Mitotic E and secretory F-cells in the hepatopancreas of the shrimp Penaeus semisulcatus (Crustacea: Decapoda). Journal of the Marine Biological Associations of the United Kingdom 65: 901-910.
Ashauer, R., I. Caravatti, A. Hintermeister, and B. I. Escher. 2010. Bioaccumulation kinetics of organic xenobiotic pollutants in the freshwater invertebrate Gammarus pulex modeled with prediction intervals. Environmental toxicology and chemistry 29: 1625-1636.
Bollache, L., and F. Cezilly. 2004. State-dependent pairing behavior in male Gammarus pulex (L.) (Crustacea, Amphipoda): effects of time left to molt and prior pairing status. Behavioural Processes 66: 131-137.
Brunet, M., J. Arnaud, and J. Mazza. 1994. Gut structure and digestive cellular processes in marine crustacean. Oceanography and Marine Biology 32: 335-367.
Ceccaldi, H. J. 2006. The digestive tract: anatomy, physiology and biochemistry, pp. 85-203. In, J. Forest and J. C. von Vaupel Klein (eds.), Treatise on Zoology-Anatomy, Taxonomy, Biology, The Crustacea. Vol. 2. Brill, Leiden.
Chang, E. S. 1995. Physiological and biochemical changes during the molt cycle in decapod crustaceans: an overview. Journal of Experimental Marine Biology and Ecology 193: 1-14.
Chang, E. S. D. L. Mykles. 2011. Regulation of crustacean molting: a review and our perspectives. General and Comparative Endocrinology 172: 323-330.
Charmantier-Daurès, M., and G. Vernet. 2004. Moulting, autonomy and regeneration, pp. 161-254. In, J. Forest and J. C. von Vaupel Klein (eds.), Treatise on Zoology-Anatomy, Taxonomy, Biology, The Crustacea. Vol. 1. Brill, Leiden.
Compère, P. 1995. Fine structure and morphogenesis of the sclerite epicuticle in the Atlantic shore crab, Carcinus maenas. Tissue Cell 27: 525-538.
Compère, P. G. Goffinet. 1987. Ultrastructural shape and tree-dimensional organization of the intracuticular canal systems in the mineralized cuticle of the green crab Carcinus maenas. Tissue Cell 19: 839-857.
Compère, P., C. Jeuniaux, and G. Goffinet. 2004. The integument morphology and biochemistry, pp. 1-85. In, J. Forest and J. C. von Vaupel Klein (eds.), Treatise on Zoology-Anatomy, Taxonomy, Biology, The Crustacea. Vol. 2. Brill, Leiden.
Compère, P., A. Thorez, and G. Goffinet. 1998. Fine structural survey of the old cuticle degradation during pre-ecdysis in two European Atlantic crabs. Tissue Cell 30: 41-56.
Corbari, L., M. Zbinden, M.-A. Cambon-Bonavita, F. Gaill, and P. Compere. 2008. Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle. Aquatic Biology 1: 225-238.
Cornet, S., G. Luquet, and L. Bollache. 2012. Influence of female moulting status on pairing decisions and size-assortative mating in amphipods. Journal of Zoology 286: 312-319.
de Oliveira Cesar, J. R., B. Zhao, S. Malecha, H. Ako, and J. Yang. 2006. Morphological and biochemical changes in the muscle of the marine shrimp Litopenaeus vannamei during the molt cycle. Aquaculture 261: 688-694.
Demeusy, N. 1979. Etude de la sécrétion de la couche membraneuse et de l'apolyse au niveau de l'épiderme de la carapace des jeunes Carcinus (Crustacés Décapodes). Compte rendus de l'Académie des Sciences Paris 289: 667-670.
Dick, J. T. A., D. E. Irvine, and R. W. Elwood. 1990. Differential predation by males on moulted females may explain the competitive displacement of Gammarus duebeni by G. pulex (Amphipoda). Behavior Ecology and Sociobiology 26: 41-45.
Dillaman, R., R. Roer, T. Shafer, and S. Modla. 2013. Chapter 5: the crustacean integument: structure and function, pp. 140-166. In, L. Watling and M. Thiel (eds.), The Natural History of Crustacea. Functional Morphology and Diversity. Oxford University Press, Oxford.
Drach, P. 1939. Mue et cycle d'intermue chez les crustacés Décapodes. Annales de l'Institut Océanographique 19: 103-392.
Drach, P. C. Tcherginovtzeff. 1967. Sur la méthode de détermination des stades d'intermue et son application générale aux crustacés. Vie et Milieu. Serie A. Biologie Marine 18: 595-609.
Giraud-Guille, M.-M. 1984. Fine structure of the chitin-protein system in the crab cuticle. Tissue Cell 16: 75-92.
Gnatzy, W., and F. Romer. 1984. Arthropods: cuticle: formation, moulting and control, pp. 638-684. In, J. Bereiter-Hahn, A. G. Matoltsy, and K. S. Richards (eds.), Biology of the Integument. Vertebrates, 2. Springer, Berlin.
Graf, F. 1986. Fine determination of the molt cycle stages in Orchestia cavimana Heller (Crustacea: Amphipoda). Journal of Crustacean Biology 6: 666-678.
Green, J. P., and M. R. Neff. 1972. A survey of the fine structure of the integument of the fiddler crab. Tissue and Cell 4: 137-171.
Halcrow, K. 1978. Modified pore canals in the cuticle of Gammarus (Crustacea: Amphipoda); a study by scanning and transmission electron microscopy. Tissue Cell 10: 659-670.
Halcrow, K.. 1985. The fine structure of the pore canals of the talitrid amphipod Hyale Nilssoni Rathke. Journal of Crustacean Biology 5: 606-615.
Halcrow, K.. 1987. Scanning electron microscopy of surface microstructure of some gammaridean amphipod crustaceans. Journal of Crustacean Biology 7: 274-287.
Halcrow, K.. 1993. Pore canal systems and associated cuticular microstructures in amphipod crustaceans, pp. 39-77. In, M. N. Horst and J. A. Freeman (eds.), The Crustacean Integument, Morphology and Biochemistry. CRC Press, Boca Raton, FL.
Halcrow, K. C. V. L. Powell. 1992. Ultrastructural diversity in the pore canal system of amphipod crustaceans. Tissue and Cell 24: 417-436.
Heller, C. 1865. Kleine Beitrage zur Kentniss der Susswasser-Amphipoden. Verhandlungen der Kaiserlich-Koniglichen zoologische-botanischen Gessellschaft in Wien 15: 979-984, pl. 17.
Hild, S., O. Marti, and A. Ziegler. 2008. Spatial distribution of calcite and amorphous calcium carbonate in the cuticle of the terrestrial crustaceans Porcellio scaber and Armadillidium vulgare. Journal of Structural Biology 163: 100-108.
Icely, J. D., and J. A. Nott. 1984. On the morphology and fine structure of the alimentary canal of Corophium volutator (Pallas) (Crustacea: Amphipoda). Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences 306: 49-78.
Icely, J. D., and J. A. Nott. 1992. Digestion and absorption: digestive system and associated organs, pp. 147-201. In, F. W. Harrison and A. G. Humes (eds.), Microscopic Anatomy of Invertebrates: Decapoda, Crustacea. Vol. 10. Wiley-Liss, New York, NY.
Leroy, D., E. Haubruge, E. De Pauw, J.-P. Thomé, and F. Francis. 2010. Development of ecotoxicoproteomics on Gammarus pulex amphipod: identification of PCB biomarkers in glycolysis and glutamate pathways. Ecotoxicology and Environmental Safety 73: 343-352.
Linnaeus, C. 1758. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonimis, locis. Tomus I. Editio decimal, reformata. Laurentii Salvii, Holmiae.
Locke, M. 1970. The molt/intermolt cycle in the epidermis and other tissues of an insect Calpodes ethlius (Lepidoptera, Hesperiidae). Tissues Cell 2: 197-223.
McCahon, C. P., and D. Pascoe. 1988. Cultures techniques for three freshwater macro-invertebrate species and their use in toxicity tests. Chemosphere 17: 2471-2480.
Miller, T. W., and D. G. Hankin. 2004. Descriptions and durations of premolt setal stages in female Dungeness crabs, Cancer magister. Marine Biology 144: 101-110.
Mulliss, R. M., D. M. Revitt, and R. B. E. Shutes. 1996. The determination of the toxic influences to Gammarus pulex (amphipoda) caged in urban receiving waters. Ecotoxicology 5: 209-215.
Neville, A. C., and C. W. Berg. 1971. Cuticle ultrastructure of a Jurassic crustacean (Eryma stricklandi). Palaeontology 14: 201-205.
Pallas, P. S. 1766. Miscellanea Zoologica, Hagae Comitum, 224 p., 14 pls. (amphipods, p. 190-194, plate 14 partim).
Richards, A. G. 1951. The Integument of Arthropods. University of Minnesota Press, Minneapolis, MN.
Roer, R. D., and R.M. Dillaman. 1993. Molt-related change in integumental structure and function, pp. 1-37. In,M. N. Horst and J. A. Freeman (eds.), The Crustacean Integument: Morphology and Biochemistry. CRC Press, Boca Raton, FL.
Schmitz, E. H. 1992. Amphipoda, pp. 443-528. In, F. W. Harrison and A. G. Humes (eds.), Microscopic Anatomy of Invertebrates. Vol. 9. Wiley-Liss, New York, NY.
Sousa, L. G., and A. M. Petriella. 2001. Changes in the hepatopancreas histology of Palaemonetes argentinus (Crustacea, Caridea) during moult. Biocell 25: 275-281.
Sousa, L. G. E. I. Cuartas, and A. M. Petriella. 2005. Fine structural analysis of the epithelial cells in the hepatopancreas of Palaemonetes argentinus (Crustacea, Decapoda, Caridea) in intermoult. Biocell 29: 25-31.
Stevenson, J. R. 1985. Dynamics of the integument, pp. 1-42. In, D. E. Bliss and L. H. Mantel (eds.), The Biology of Crustacean. Vol. 9. Academic Press, New York.
Thomas, P. C., C. Turner, and D. Pascoe. 1991. An assessment of field and laboratory methods for evaluating the toxicity of ammonia to Gammarus pulex (L) - effects of water velocity, pp. 353-363. In, D. W. Jeffrey and B. Madden (eds.), Bioindicators and Environmental Management. Academic Press, San Diego, CA.
Tian, Z., X. Kang, and S.Mu. 2012. The molt stages and the hepatopancreas contents of lipids, glycogen and selected inorganic elements during the molt cycle of the Chinese mitten crab Eriocheir sinensis. Fisheries Science 78: 67-74.
Vogt, G. 1993. Differentiation of B-cells in the hepatopancreas of the prawn Penaeus monodon. Acta Zoologica 74: 51-60.
Vogt, G.. 1994. Life-cycle and functional cytology of the hepatopancreatic cells of Astacus astacus (Crustacea, Decapoda). Zoomorphology 114: 83-101.
Vogt, G., V. Storch, E. T. Quinitio, and F. P. Pascual. 1985. Midgut gland as monitor organ for the nutritional value of diets in Penaeus monodon (Decapoda). Aquaculture 48: 1-12.
Williams, A. B., and P. A. Rona. 1986. Two new caridean shrimp (Bresiliidae) from a hydrothermal field on the Mid-Atlantic Ridge. Journal of Crustacean Biology 6: 446-462.
