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Microbial Flora Associated with the Digestive System of Upogebia Stellata (Crustacea: Decapoda: Thalassinidea)

Published online by Cambridge University Press:  11 May 2009

E.H. Pinn ,
A. Rogerson  and
R.J.A. Atkinson
E.H. Pinn
Affiliation:
University Marine Biological Station Millport, Isle of Cumbrae, KA28 OEG.
A. Rogerson
Affiliation:
University Marine Biological Station Millport, Isle of Cumbrae, KA28 OEG.
R.J.A. Atkinson
Affiliation:
University Marine Biological Station Millport, Isle of Cumbrae, KA28 OEG.
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Extract

The digestive system of the thalassinidean mud-shrimp Upogebia stellata was investigated using scanning electron microscopy (SEM). Within the lumen of the midgut both filamentous and rod-shaped bacteria were observed. The hindgut microbial populations were dominated by dense mats of epimural rod-shaped bacteria. The gut contents were often dominated by diatoms but also contained bacteria, dinoflagellates, plant and algal fragments. Direct bacterial counts by epifluorescence microscopy along the length of the gut revealed a slight decrease in numbers within the midgut moving from the anterior to the posterior regions, and then a dramatic rise in numbers within the hindgut. Numbers decreased again in the posterior regions of the hindgut. Common in the transient / resident samples (bacterial population when gut contents were present) were enterobacteria and an unidentified fermenter conforming to an isolate named X-ferm. However, nearly 30% of the bacterial isolates remained unidentified. The resident-only bacterial isolates from the gut (determined when the gut was empty) were dominated by the X-ferm bacteria and to a lesser extent by the genera Vibrio and Aeromonas. With respect to the enzyme capabilities of the gut bacteria, the resident-only collection of bacterial isolates showed much higher levels of amylase, cellulase, chitinase, protease and lipase activity than the transient/resident bacterial isolate collections, suggesting that the indigenous bacteria are likely to play a significant role in the digestion of the gut contents. Thalassinidean shrimps are likely to play an important role in the breakdown of plant and detrital material, and the recycling of nutrients in marine benthic systems.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 77 , Issue 4 , November 1997 , pp. 1083 - 1096
Copyright
Copyright © Marine Biological Association of the United Kingdom 1997

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References

Bianchi, M.A.G. & Bianchi, A.J.M., 1982. Statistical sampling of bacterial strains and its use in bacterial diversity measurement. Microbial Ecology, 8, 61–69.Google Scholar
Boyle, P.J. & Mitchell, R., 1978. Absence of microorganisms in crustacean digestive tracts. Science, New York, 200, 1157–1159.CrossRefGoogle ScholarPubMed
Buchanan, J.B., 1963. The biology of Calocaris macandreae (Crustacea: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom, 43, 729–747.CrossRefGoogle Scholar
Buchanan, R.E. & Gibbons, N.E., 1974. Bergey's manual of determinative bacteriology. Baltimore: The Williams & Wilkins Company.Google Scholar
Colorni, A., 1985. A study on the bacterial flora of the giant prawn Macrobrachium rosenbergii larvae fed with Artemia salina nauplii. Aquaculture, 49, 1–10.CrossRefGoogle Scholar
Cowan, S.T. & Steel, K.J., 1970. Manual for the identification of medical bacteria. London: Cambridge University Press.Google Scholar
Deming, J.W., Tabor, P.S. & Colwell, P.R., 1981. Barophilic growth of bacteria from intestinal tracts of deep-sea invertebrates. Microbial Ecology, 7, 85–94.Google Scholar
Dempsey, A.C. & Kitting, C.L., 1987. Characteristics of bacteria isolated from penaeid shrimp. Crustaceana, 52, 90–94.CrossRefGoogle Scholar
Dworschak, P.C., 1987. Feeding behaviour of Upogebia pusilla and Callianassa tyrrhena (Crustacea, Decapoda, Thalassinidea). Investigatión Pesquera. Barcelona, 51, supplement 1, 421–429.Google Scholar
Egidius, E., 1972. On the intestinal flora of the European lobster (Homarus vulgaris, L.) and its susceptibility of Gaffkaemia. Aquaculture, 1, 193–197.CrossRefGoogle Scholar
Felder, D.L. & Felgenhauer, B.E., 1993. Morphology of the midgut-hindgut juncture in the ghost shrimp Lepidophthalmus louisianensis (Schmitt) (Crustacea: Decapoda: Thalassinidea). Acta Zoologica, 74, 263–276.Google Scholar
Fong, W. & Mann, K.H., 1980. Role of gut flora in the transfer of amino acids through a marine food chain. Canadian Journal of Fisheries and Aquatic Science, 37, 88–96.CrossRefGoogle Scholar
Grémare, A., 1988. Feeding, tube-building and particle-size selection in the terebellid polychaete Eupolymnia nebulosa. Marine Biology, 97, 243–252.CrossRefGoogle Scholar
Harris, J.M., 1993a. The presence, nature and role of gut microflora in aquatic invertebrates: a synthesis. Microbial Ecology, 25, 195–231.CrossRefGoogle ScholarPubMed
Harris, J.M., 1993b. Widespread occurrence of extensive epimural rod bacteria in the hindguts of marine Thalassinidae and Brachyura (Crustacea: Decapoda). Marine Biology, 116, 615–629.Google Scholar
Harris, J.M., Seiderer, L.J. & Lucus, M.I., 1991. Gut microflora of two saltmarsh detritivore thalassinid prawns, Upogebia africana and Callianassa kraussi. Microbial Ecology, 21, 277–296.Google Scholar
Holding, A.J. & Collee, J.G., 1971. Routine biochemical tests. In Methods in microbiology, vol. 6A (ed. J.R., Norris and D.W., Ribbons), pp. 1–32. London: Academic Press.Google Scholar
Hood, M.A. & Meyers, S.P., 1977. Microbial and chitinoclastic activities associated with Penaeus setiferus. Journal of Oceanography, Japan, 33, 235–241.CrossRefGoogle Scholar
Jolly, J.M., Lappin-Scott, H.M., Anderson, J.M. & Clegg, C.D., 1993. Scanning electron microscopy of the gut microflora of two earthworms:Lumbricus terrestris and Octolasion cyaneum. Microbial Ecology, 26, 235–245.CrossRefGoogle ScholarPubMed
Kaneko, T., Krichevsky, M.T. & Atlas, R.M., 1979. Numerical taxonomy of bacteria from the Beaufort Sea. Journal of General Microbiology, 110, 111–125.CrossRefGoogle Scholar
Kumar, A. & Dube, H.C., 1990. Aerobic bacteria flora of two commercial crustaceans from Bhavnager muddy coast. Indian Journal of Microbiology, 30, 197–200.Google Scholar
Laycock, R.A., 1974. The detrital food chain based on seaweeds. 1. Bacteria associated with the surface of Laminaria fronds. Marine Biology, 25, 223–231.CrossRefGoogle Scholar
Mead, L.J., Khachatourians, G.G. & Jones, G. A., 1988. Microbial ecology of the gut in laboratory stocks of the migratory grasshopper Melanoplus sanguinipes (Fab.) (Orthoptera: Acridae). Applied and Environmental Microbiology, 54, 1174—1181.Google Scholar
Mitra, T., 1987. Study of the intestinal microflora of the penaeid prawn Penaeus monodon Fabricius. Indian Journal of Microbiology, 27, 85–86.Google Scholar
Moriarty, D.J.W., 1990. Interactions of micro-organisms and aquatic animals. In Microbiology in poecilotherms (ed. R., Lesel), pp. 217–222. New York: Elsevier Science Publishers.Google Scholar
Nagasawa, S. & Nemoto, T., 1988. Presence of bacteria in guts of marine crustaceans and their fecal pellets. Journal of Plankton Research, 10, 559–564.Google Scholar
Ngoc-Ho, N., 1984. The functional anatomy of the foregut of Porcellana platyceles and a comparison with Galathea squamifera and Upogebia deltaura (Crustacea: Decapoda). Journal of Zoology, 203, 511–535.Google Scholar
Nickell, L. A., 1992 Deep bioturbation in organically enriched marine sediments. PhD thesis, University of London.Google Scholar
Nickell, L.A., Hughes, D.J. & Atkinson, R.J.A., 1995. Megafaunal bioturbation in organically enriched Scottish sea lochs. In Biology and ecology of shallow coastal waters. Proceedings of the 28th European Marine Biological Symposium, Hersonissos, Crete, Greece, 1993 (ed. A., Eleftheriou et al.), pp. 315–322. Fredensborg: Olsen & Olsen.Google Scholar
Ninawe, A. & Banik, S., 1987. Chitinolytic bacteria in Penaeus indicus. Journal of Aquaculture in the Tropics, 2, 89–92.Google Scholar
Oliver, J.D., 1982. Taxonomic scheme for the identification of marine bacteria. Deep-Sea Research, 29, 795–798.CrossRefGoogle Scholar
Ott, J.A., Fuchs, B., Fuchs, R. & Malasek, A., 1976. Observations on the biology of Callianassa stebbinigi Borrodaille and Upogebia litoralis Risso and their effect upon the sediment. Senckenbergiana Maritima. Frankfurt-am-Main, 8, 61–79.Google Scholar
Payne, D.W., Thorpe, N.A. & Donaldson, E.M., 1972. Cellulytic activity and a study of the bacterial population in the digestive tract of Scrobicularia plana (Da Costa). Proceedings of the Malacological Society of London, 40, 147–160.Google Scholar
Pillai, R.S., 1960. Studies on the shrimp Caridina laevis Heller. 1. Digestive system. Journal of the Marine Biological Association of India, 2, 57–75.Google Scholar
Pinn, E.H., 1995. Studies on the feeding biology of thalassinidean mud-shrimps. PhD thesis, University of London.Google Scholar
Plante, C.J., Jumars, P.A. & Baross, J.A., 1990. Digestive associations between marine detritivores and bacteria. Annual Review of Ecology and Systematics, 21, 93–127.CrossRefGoogle Scholar
Pohl, M.E., 1946. Ecological observations on Callianassa major Say at Beaufort, North Carolina. Ecology, 27, 71–80.Google Scholar
Powell, R.R., 1974. Functional morphology of the foreguts of the thalassinid crustaceans Callianassa californiensis and Upogebia pugettensis. University of California Publications in Zoology, 102, 1–41.Google Scholar
Prim, P. & Lawrence, J.M., 1975. Utilization of marine plants and their constituents by bacteria isolated from the gut of echinoids (Echinodermata). Marine Biology, 33, 167–173.Google Scholar
Reichenbach, I.T. & Dworkin, M., 1981. The order Myxobacteriales. In The prokaryotes, vol. 1 (ed. M.P., Starr et al.), pp. 328–355. New York: Springer-Verlag.CrossRefGoogle Scholar
Schaefer, N., 1970. The functional morphology of the foregut of three species of decapod Crustacea: Cyclograpus punctatus Milne-Edwards, Digenes brevirostris Stimpson and Upogebia africana (Ortmann). Zoologica Africana. Cape Town, 5, 309–326.CrossRefGoogle Scholar
Schallenberg, M., Kalff, J. & Rasmussen, J.B., 1989. Solutions to problems in enumerating sediment bacteria by direct counts. Applied and Environmental Microbiology, 55, 1214–1219.Google Scholar
Scheraga, M., Meskill, M. & Litchfield, C.D., 1979. Analysis methods for the quantitative recovery of bacteria sorbed onto marine sediments. In Methodology for biomass determinations and microbial activities in sediments (ed. C.D., Litchfield and P.L., Seyfield), pp. 21–39. Philadelphia: American Society for Testing and Materials. [ASTM Special Technical Publication no. 673.]CrossRefGoogle Scholar
Schwartz, J.R., Yayanos, A.A. & Colwell, R.R., 1976. Metabolic activities of the intestinal microflora of a deep-sea invertebrate. Applied and Environmental Microbiology, 31, 46–18.Google Scholar
Seiderer, L.J., Davis, C.L., Robb, F.T. & Newell, R.C., 1984. Utilisation of bacteria as a nitrogen resource by the kelp-bed mussel Choromytilus meridionalis. Marine Ecology Progress Series, 15, 109–116.Google Scholar
Seiderer, L.J. & Newell, R.C., 1988. Exploitation of phytoplankton as a food resource by the kelp bed ascidian Pyura stolonifera. Marine Ecology Progress Series, 50, 107–115.Google Scholar
Smith, D.C. & Douglas, A.E., 1987. The biology of symbiosis. London: Edward ArnoldGoogle Scholar
Sochard, M.R., Wilson, D.F., Austin, B. & Colwell, R.R., 1979. Bacteria associated with the surface and gut of marine copepods. Applied and Environmental Microbiology, 37, 750–759.Google Scholar
Sugita, H., Ueda, R., Berger, L.R. & Deguchi, Y., 1987. Microflora in the gut of Japanese coastal Crustacea. Nippon Suisan Gakkaishi, 53, 1647–1655.Google Scholar
Teather, R.M. & Wood, P.J., 1982. Use of Congo red polysaccharide interactions in enumeration and characterisation of cellulytic bacteria from the bovine rumen. Applied and Environmental Microbiology, 43, 777–780.CrossRefGoogle Scholar
Ueda, R., Yasuhara, T., Sugita, H. & Deguchi, Y., 1989. Gut Microflora Of The Japanese Giant Crab Macrocheira Kaempferi. Nippon Suisan Gakkaishi, 55, 181.Google Scholar
Venkateswaran, K., Sethwamalingam, G. & Natarajan, R., 1981. Gut microflora of some edible crabs from the Porto Nova coast. Journal of Indian Marine Science, 10, 399–401.Google Scholar
Vitalis, T.Z., Spence, M.J. & Carefoot, T.H., 1988. The possible role of gut bacteria in nutrition and growth of the seahare Aplysia. Veliger, 30, 333–341.Google Scholar