Abstract
Electron microscopic examination of thin-sectioned Limnoria tripunctata from creosoted and untreated wood substrates from Panama, Florida, and laboratory aquaria, coupled with limnorian behavioral studies revealed that bacteria may contribute to the wood boring, nutrition, and creosote-resistance of these isopods. Ingested along with wood fragments and encased in a peritrophic membrane in the isopod intestine, these bacteria, upon lysis, may provide supplemental nutrition to the nitrogen-poor wood diet of L. tripunctata. Ingested material has never been observed in the digestive diverticula of limnorians and the presence of the peritrophic membrane in the isopod intestine has been correlated with feeding. Isopods from creosoted wood differed from those inhabiting untreated wood in that the former contained relatively larger and more diverse bacterial populations both on their exoskeletons and in their gut contents. These isopods harbored bacteria, which apparently bypassed the peritrophic membrane and lived in association with the isopod intestinal lining. These gut-associated bacteria were lost when laboratory isopods reared on creosoted wood were transferred to untreated wood. Laboratory isopods reared solely on creosoted or untreated wood were exposed to creosoted and untreated wood substrates, both sterilized and unsterilized. Boring and mortality data from these studies indicated that the creosote-reared population had a microbial flora whose activity facilitated isopod colonization of creosoted substrates. We present the hypothesis that creosote hydrocarbons provide nutrition for isopod-associated bacterial populations and that L. tripunctata may benefit from a concomitant bacterial detoxification of the creosote.
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Literature cited
Becker, B.: Determination of the formation rate of peritrophic membranes in some Diptera. J. Insect Physiol. 24, 529–533 (1978)
Becker, B., W. Peters and U. Zimmerman: The fine structure of peritrophic membranes of the blowfly Calliphora erythocephala grown in vitro under different conditions. J. Insect Physiol. 22, 337–345 (1976)
Becker, G.: Holzzerstörende Tiere und Holzschutz in Meerwasser. Holz Roh- Werkst. 16, 204–213 (1958)
Becker, G.: Physiological influence on wood-destroying insects of wood compounds and substances produced by microorganisms. Wood Sci. Tech. 5, 236–246 (1971)
Becker, G., W. Kampf and J. Kohlmeyer: Zur Ernährung der Holzbohrasseln der Gattung Limnoria. Naturwissenschaften 44, 473–474 (1957)
Belas, M. R., A. Zachary, D. Allen, B. Austin and R. R. Colwell: Microbial colonization of naphthalene/creosote treated wood pilings in a tropical marine environment. Proc. Am. Wood-Preserv. Assoc. 75, 20–27 (1979)
Boyle, P. J. and R. Mitchell: Absence of microorganisms in crustacean digestive tracts. Science, N.Y. 200, 1157–1159 (1978)
Boyle, P. J. and R. Mitchell: Interaction between microorganisms and wood boring crustaceans. In: Biodeterioration. pp 179–186. Ed. by T. S. Oxley, D. Allsopp and G. Becker. Proc. of the Fourth inter. Biodeterioration Symp., Berlin. London: Pitman Publishing Co. 1980
Boyle, P. J. and R. Mitchell: External flora of a marine wood-boring isopod. Appl. environ. Microbiol. 42, 720–729 (1981)
Brandt, C. R., M. J. Adang and K. D. Spence: The peritrophic membrane: ultrastructural analysis and function as a mechanical barrier to microbial infection in Orgyia pseudotsugata. J. Invert. Pathol. 32, 12–24 (1978)
Colley, R. H.: Observations on experimental evidence of the effectiveness of creosote-coal tar solution in preventing attack on marine piling by Limnoria tripunctata. Proc. Am. Wood-Preserv. Assoc. 63, 151–162 (1967)
Costerton, J. W., G. G. Geesey and K. J. Cheng: How bacteria stick. Sci. Am. 238, 86–95 (1977)
Davidson, E. W.: Ultrastructure of midgut events in the pathogenesis of Bacillus sphaericus strain SSII-1 infections of Culex pipiens quinquefasciatus larvae. Can. J. Microbiol. 25, 178–184 (1979)
Drisko, R. W. and H. Hochman: Amino acid content of marine borers. Biol. Bull. mar. biol. Lab., Woods Hole 112, 325–329 (1957)
Drisko, R. W. and T. B. O'Neill: Microbiological metabolism of creosote. For. Prod. J. 16, 31–34 (1966)
Eltringham, S. K.: Environmental factors influencing the settlement, activity and reproduction of the wood boring isopod Limnoria. Mater. Org. I. Holz Org. 465–478 (1965)
Eltringham, S. K.: Marine borers and fungi. In: Marine borers, fungi and fluling organisms of wood, 321–338. Ed. by E. B. G. Jones, and S. K. Eltringham. 367 pp. Paris: Organization for Economic Cooperation and Development 1971
Hochman, H.: Creosoted wood in a marine environment — a summary report. Proc. Am. Wood-Preserv. Assoc. 63, 138–150 (1967)
Hochman, H., H. Vind, T. Roe, J. Muraoka and J. Casey: The role of Limnoria tripunctata in promoting early failure of creosoted piling. Tech. Memorandum Rpt M-109. Naval Civil Engineering Laboratory, Port Hueneme, CA. 43 pp. 1956
Kalnins, M. A.: Characterization of the attack on wood by the marine borer Limnoria tripunctata (Menzies). Proc. Am. Wood-Preserv. Assoc. 72, 1–13 (1976)
Kaplan, D. L. and R. Hartenstein: Studies on monooxygenases and dioxygenases in soil macroinvertebrates and bacterial isolates from the gut of the terrestrial isopod Oniscus asellus. Comp. Biochem. Physiol. 60 B, 47–50 (1978)
Kester, D. R., I. W. Deudall, D. N. Connors and R. M. Pytkowicz: Preparation of artificial seawater. Limnol. Oceanogr. 12(1), 176–179 (1967)
Kohlmeyer, J., G. Becker and W. D. Kampf: Versuche zur Kenntnis der Ernährung der Holzbohrassel Limnoria tripunctata und ihre Beziehung zu holzzerstörenden Pilzen. Z. angew. Zool. 46, 457–489 (1959)
Kuhne, H.: On the nutritional requirements of wood boring crustacea. In: Proc. Third International Congress on Marine Coatings and Fouling, pp 814–821. Ed. by R. F. Acker, B. F. Brown, J. R. DePalma and W. P. Iverson. Gaithersburgh, Maryland, USA: Northwestern University Press 1973
Lane, C. E.: The general histology and nutrition of Limnoria. In: Marine boring and fouling organisms, pp 34–45. Ed. by D. L. Ray. 536 pp. Seattle: University of Washington Press 1959
Larkin, F. T.: Cellulose utilization of Limnoria. Proc. Conf. on Marine Borers, pp L1-L4. Naval Civil Engineering Laboratory, Port Hueneme, CA 1951
Menzies, R. J.: A new species of Limnoria (Crustacea: Isopoda) from southern California. Bull. South. Calif. Acad. Sci. 50, 86–88 (1951)
Mercer, E. H. and M. F. Day: The fine structure of the peritrophic membranes of certain insects. Biol. Bull. mar. biol. Lab., Woods Hole 103, 384–394 (1952)
Meyers, S. P. and E. S. Reynolds: Incidence of marine fungi in relation to wood borer attack. Science, N.Y. 129, 969 (1957)
Oliver, A. C.: An account of the biology of Limnoria. J. Inst. Wood Sci. 9, 32–91 (1962)
Parrish, K. K. and J. D. Bultman: Navy research on marine borers and the laboratory culturing of limnorians. Proc. Fourth Annual Combined MTs-IEEE Conference. Oceans '78. Washington, D. C. September, 1978
Parrish, K. K., W. R. Barger and J. D. Bultman: Exposure of creosote-naive and creosote-conditioned Limnoria tripunctata (Menzies) to untreated and creosote-treated wood. Final Report. Naval Res. Lab., Wash. D. C. (In press)
Paschke, J. D. and M. D. Summers: Early events in the infection of the arthropod gut by pathogenic insect viruses. In: Invertebrate immunity, pp 75–112. Ed. by K. Maramorosch and R. E. Shope. New York: Academic Press 1975
Ray, D. L.: Nutritional physiology of Limnoria. In: Marine boring and fouling organisms, pp 40–60. Ed. by D. L. Ray. Seattle: University of Washington Press 1959
Ray, D. L. and J. R. Julian: Occurrence of cellulase in Limnoria. Nature, Lond. 169, 32 (1952)
Reyes, V. G. and J. M. Tiedge: Ecology of the gut microbiota of Tracheoniscus rathkei (Crustacea:Isopoda). Pedobiologia 16, 67–74 (1976)
Richards, A. G. and P. A. Richards: Origin and composition of the peritrophic membrane of the mosquito Aedes aegypti. J. Insect Pathol. 17, 2253–2257 (1971)
Schafer, R. D. and C. E. Lane: Some preliminary observations bearing on the nutrition of Limnoria. Bull. mar. Sci. Gulf Carrib. 7, 289–296 (1957)
Siefert, K.: Über den Abbau der Holzsubstanz durch die Bohrassel Limnoria. Holz Roh- Werkst. 22, 209–215 (1964)
Sleeter, T. D., P. J. Boyle, A. M. Cundell and R. Mitchell: Relationships between marine microorganisms and the wood boring isopod Limnoria tripunctata. Mar. Biol. 45, 329–336 (1978)
Vind, H., H. Hochman and J. Muraoka: The protein requirements of Limnoria, 32 pp. Non-Tech. Abstract #8. Naval Civil Engineering Laboratory, Port Hueneme, CA, USA 1956
Younge, C. M.: The absence of cellulase in Limnoria. Nature, Lond. 119, 885 (1927)
Zachary, A. and R. R. Colwell: Gut-associated microflora of Limnoria tripunctata in marine creosote-treated wood pilings. Nature, Lond. 282, 716–717 (1979)
Zhuzikov, D. P.: Function of the peritrophic membrane in Musca domestica L. and Calliphora erythrocephala Meig. J. Insect Physiol. 10, 273–278 (1964)
Zhuzikov, D. P.: Permeability of the peritrophic membrane in larvae of Aedes aegypti. J. Insect Physiol. 16, 1193–1202 (1970)
Zimmerman, U., D. Mehlan and W. Peters: Investigations on the transport function and structure of peritrophic membranes V. Amino acid analysis and electronmicroscopic investigations of the peritrophic membranes of adult Calliphora erythrocephala Mg. Comp. Biochem. Physiol. 51 B, 181–186 (1975)
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Communicated by S. K. Pierce, College Park
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Zachary, A., Parrish, K.K. & Bultman, J.D. Possible role of marine bacteria in providing the creosote-resistance of Limnoria tripunctata . Mar. Biol. 75, 1–8 (1983). https://doi.org/10.1007/BF00392624
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DOI: https://doi.org/10.1007/BF00392624