Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-28T07:28:37.301Z Has data issue: false hasContentIssue false
  • English
  • Français

The protozoa occurring in the hind-gut of cockroaches. III. Factors affecting the dispersion of Nyctotherus ovalis

Published online by Cambridge University Press:  06 April 2009

H. M. D. Hoyte
H. M. D. Hoyte
Affiliation:
Molteno Institute, University of Cambridge*
Get access Rights & Permissions [Opens in a new window]

Extract

The only mode of transmission of Nyctotherus ovalis from one cockroach to another was shown experimentally to be by way of ingestion of the encysted stage of the ciliate. The cysts were remarkably resistant, being able to remain viable for 21 weeks at −18°C. if kept in dry faeces, or for 20 weeks in wet faeces at 4°–25°C. Their life was much shorter if kept at 37°, 25°, or 4°C. under dry conditions, or at −18°C. under wet. The cysts could withstand freeze-drying, or storage in pure oxygen, carbon dioxide or nitrogen, at least for short periods.

Nyctotherus ovalis could excyst in any of the four species of cockroach which were tested (Periplaneta americana, Blatta orientalis, Blattella germanica, Blaberus giganteus), irrespective of the species of origin. The ciliate could establish an infection in a very young host; in a host which had ingested infected faeces once only; in hosts which were in a very dry or a very humid environment; in a host maintained at a temperature far below that required for in vitro excystation, subject only to the temperature being high enough for it to be possible for the cockroach to digest its meal; but Nyctotherus could not establish an infection in cockroaches which were about to moult, because there was no movement nor digestion of food in the gut. There was no evidence of an instinctive drive on the part of the cockroach to eat infected faeces. There was some evidence that the Blatta and Blattella types of trophozoite and cyst were associated with the presence or absence respectively of a type of flora typically associated with the hind-gut of Blatta.

The process of excystation took as little as 3 hr. for completion in vivo, but this time was increased if faecal material was ingested along with cysts. The process was most rapid in the smallest cockroach (Blattella) and slowest in the largest (Blaberus). The process, once started, could be completed in vitro, but at a considerably slower pace. Digestion of the knob on the cyst by the cockroach's enzymes seemed to be necessary if the ciliate was to emerge.

A small proportion of cysts hatched after passage through the gut of a locust, but no means were found of increasing this proportion, and an infection was never established. Excystation did not occur in any other arthropod, nor in the frog, which were tested.

Cysts recovered from the mid-gut of a cockroach completed the process of excystation in vivo more rapidly if they were put in a buffer medium of pH approximating that of the mid-gut than if they were put in saline. Passage of the cysts through the foregut of the cockroach had no function in stimulating excystation: the agent seemed to be the trypsin secreted by the mid-gut caeca, or the products of its activity. The many failures in the series of experiments which are reported here can probably be attributed to contaminating bacteria.

The complete process of excystation could occur in vitro if the cysts were incubated with faecal matter from the cockroach. The optimum temperature was 32°C., and 2 days were needed for a significant number to hatch. No means were found of shortening this time, nor any agents which could be substituted for the faecal matter. The stimulus seemed to be provided by particular anaerobic bacteria of the faeces which were present in some cockroaches, but absent in others.

Work by other authors on excystation in other Protozoa is reviewed. It was concluded that in vivo excystation of Nyctotherus ovalis occurs as a result of stimulation of the cyst by the digestive trypsin of the cockroach, and not by the products of the unidentified bacterium which is active in vitro. Cysts originating from Blaberus seemed to be less sensitive to this bacterial factor than some of those from Periplaneta or Blatta.

This work was done during the tenure of a Research Studentship awarded by by the Agricultural Research Council. I am deeply indebted to Dr P. Tate for his encouragement and counsel at all stages of the work.

Type
Research Article
Information
Parasitology , Volume 51 , Issue 3-4 , November 1961 , pp. 465 - 495
Copyright
Copyright © Cambridge University Press 1961

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

REFERENCES

Allen, E. A. (1926). Excystment of Councilmania lafleuri Kofoid and Swezy in culture in vitro. Univ. Calif. Publ. Zool. 29, 175–8.Google Scholar
Andrews, J. (1942). The transmission of Endamoeba histolytica and amebic diseases. Sth Med. J., Nashville, 35, 693–9.CrossRefGoogle Scholar
Annear, D. I. (1956). Freeze-drying. Part III. The preservation of micro-organisms. Lab. Practice, (1956). 102–5.Google Scholar
Becker, E. (1928). Streaming and polarity in Mastigina hylae (Frenzel). Biol. Bull., Woods Hole, 54, 109–16.Google Scholar
Becquerel, P. (1936). La vie latente de quelques algues et animaux inferieurs aux basses temperatures et la conservation de la vie dans l'univers. C.R. Acad. Sci., Paris, 202, 978–81.Google Scholar
Breed, R. S., Murray, E. G. D. & Hitchens, A. P. (1948). Bergey's Manual of Determinative Bacteriology, 6th ed. London: Baillière, Tindall and Cox.Google Scholar
Chang, S. L., (1943). Studies on Endamoeba histolytica. II. Observations concerning encystation, maturation and excystation of E. histolytica, and on the longevity of culture-induced cysts in various fluids and at different temperatures. J. Infect. Dis. 72, 232–41.CrossRefGoogle Scholar
Chang, S. L. (1946). Studies on Endamoeba histolytica. IV. The relation of oxidation-reduction potentials to the growth, encystation and excystation of Endamoeba histolytica in culture. Parasitology, 37, 101–12.CrossRefGoogle Scholar
Chang, S. L. (1955). Survival of cysts of Endamoeba histolytica in human faeces under low temperature conditions. Amer. J. Hyg. 61, 103–20.Google ScholarPubMed
Chang, S. L. & Fair, G. M. (1941). Viability and destruction of the cysts of Endamoeba histolytica. J. Amer. Wat. Wks. Ass. 33, 1705–15.Google Scholar
Child, C. M. (1914). The axial gradient in ciliate infusoria. Biol. Bull., Woods Hole, 26, 36–54.CrossRefGoogle Scholar
Cloudsley-Thompson, J. L. (1953). Studies in diurnal rhythyms. III. Photoperiodism in the cockroach Periplaneta americana (L.) Ann. Mag. Nat. Hist. (12) 6, 705–12.Google Scholar
Day, M. F. & Powning, R. F. (1949). A study of the processes of digestion in certain insects. Aust. J. Sci. Res. B, 2, 175–215.Google Scholar
Dobell, C. (1927). Further observations and experiments on the cultivation of Entamoeba histolytica from cysts. Parasitology, 19, 288–313.CrossRefGoogle Scholar
Dobell, C. (1928). Researches on the intestinal Protozoa of monkeys and man. I. General introduction. II. Description of the whole life-cycle of Entamoeba histolytica in cultures. Parasitology, 20, 357–412.CrossRefGoogle Scholar
Dobell, C. (1938 a). Researches on the intestinal Protozoa of monkeys and man. IX. The life history of Entamoeba coli, with special reference to metacystic development. Parasitology, 30, 195–238.CrossRefGoogle Scholar
Dobell, C. (1938 b). Dr O. Uplavici (1887–1938). Parasitology, 30, 239–41.CrossRefGoogle Scholar
Dobell, C. (1952). (completed by Neal, R. A.; edited by Hoare, C. A.). Researches on the intestinal Protozoa of monkeys and man. XII. Bacterial factors influencing the life history of Entamoeba histolytica in cultures. Parasitology, 42, 16–39.CrossRefGoogle Scholar
Fauré-Fremiet, E. (1948). Les mécanismes de la morphogénèse chez les Ciliés. Folia Biotheoretica, B3, 25–58.Google Scholar
Geiman, Q. M. & Ratcliffe, H. L. (1936). Morphology and life-cycle of an amoeba producing amoebiasis in reptiles. Parasitology, 28, 208–28.CrossRefGoogle Scholar
Goetsch, W. (1936). Beiträge zur Biologie des Termitenstaates. Z. Morph. Ökol. Tiere, 31, 490–560.CrossRefGoogle Scholar
Gunn, D. L. (1940). The daily rhythm of activity of the cockroach, Blatta orientalis L. I. Aktograph experiments, especially in relation to light. J. Exp. Biol. 17, 267–77.CrossRefGoogle Scholar
Haagen-Smit, A. J. & Thimann, K. V. (1938). The excystment of Colopoda cucullus. I. The chemical nature of the excysting factors in hay infusion. J. Cell. Comp. Physiol. 11, 389–407.CrossRefGoogle Scholar
Halpern, B. & Dolkart, R. E. (1954). The effect of cold temperatures on the viability of cysts of Endamoeba histolytica. Amer. J. Trop. Med. Hyg. 3, 276–82.CrossRefGoogle ScholarPubMed
Harker, J. E. (1956). Factors controlling the diurnal rhythm of activity of Periplaneta americana L. J. Exp. Biol. 33, 224–34.CrossRefGoogle Scholar
Hatcher, E. (1939). The consortes of certain North Carolina Blattids. J. Elisha Mitchell Sci. Soc. 55, 329–34.Google Scholar
Hegner, R. (1927 a). Excystation in Iodamoeba williamsi in vivo and in vitro. Science, 65, 69–70.Google Scholar
Hegner, R. (1927 b). Excystation in vitro of human intestinal Protozoa. Science, 65, 577–8.CrossRefGoogle ScholarPubMed
Hoyte, H. M. D. (1961 a). The Protozoa occurring in the hind-gut of cockroaches. I. Responses to changes in the environment. Parasitology, 51, 415–436.CrossRefGoogle Scholar
Hoyte, H. M. D. (1961 b). The Protozoa occurring in the hind-gut of cockroaches. II. Morphology of Nyctotherus ovalis. Parasitology. 51, 437–463.Google Scholar
Jansen, W. A. & Wedberg, S. E. (1952). The common house roach, Blattella germanica Linn., as a potential vector of Salmonella typhimurium and Salmonella typhosa. Amer. J. Trop. Med. Hyg. 1, 337–43.CrossRefGoogle Scholar
Jones, W. R. (1946). The experimental infection of rats with Entamoeba histolytica; with a method for evaluating the anti-amoebic properties of new compounds. Ann. trop. Med. Parasit. 40, 130–40.CrossRefGoogle ScholarPubMed
Kidder, G. W. (1937). The intestinal Protozoa of the wood-feeding roach Panesthia. Parasitology, 29, 163–205.Google Scholar
Lom, J. (1956). Experiments with the cultivation of our three species of the genus Nyctotherus and of Balantidium entozoon and B. coli. Vést. Českoslov. Zool. Spol. 20, 16–61.Google Scholar
Lucas, C. L. T. (1927). Two new species of ameoba found in cockroaches; with notes on the cysts of Nyctotherus ovalis Leidy. Parasitology, 19, 223–35.CrossRefGoogle Scholar
Lucas, C. L. T. (1928). A study of excystation in Nyctotherus ovalis, with notes on other intestinal Protozoa of the cockroach. J. Parasit. 14, 161–75.CrossRefGoogle Scholar
Mellanby, K. (1940). The daily rhythm of activity of the cockroach, Blatta orientalis L. II. Observations and experiments on a natural infestation. J. Exp. Biol. 17, 278–85.Google Scholar
Pai, K.-T. & Wang, C.-C. (1948). The variation of Nyctotherus ovalis Leidy and its fibrillar system. Sinensia, 18, 43–58.Google Scholar
Polge, C. & Soltys, M. A. (1957). Preservation of trypanosomes in the frozen state. Trans. Roy. Soc. Trop. Med. Hyg. 51, 519–26.Google Scholar
Poynter, D. (1956). Effect of a coliform organism (Escherichia) on the second ecdysis of nematode larvae parasitic in the horse. Nature, Lond., 177, 481–2.CrossRefGoogle Scholar
Reardon, L. V., Verder, E. & Rees, C. W. (1952). The cultural requirements of Endamoeba coli and the comparative effects of drying on the cysts of E. coli and E. histolytica. Amer. J. Trop. Med. Hyg. 1, 155–61.CrossRefGoogle ScholarPubMed
Rees, C. W. (1942). The construction of a micromanipulator for the isolation of Protozoa. Amer. J. Trop. Med. 22, 487–92.Google Scholar
Rees, C. W., Reardon, L. V. & Bartgis, I. L. (1950). The excystation of Entamoeba histolytica without bacteria in microculture. Parasitology, 40, 338–42.Google Scholar
Rees, C. W., Reardon, L. V., Jones, F. E. & Griffen, A. M. (1947). Observations on the excystation of Endamoeba histolytica. J. Parasit. 33, 385.Google Scholar
Rendtorff, R. C. (1953). A method of exposing flies to infectious material. J. Parasit. 39, 672–3.CrossRefGoogle Scholar
Reusse, U. (1956). Konservierung einiger tierpathogener Protozoen durch aufberwarhung bei tiefen Temperaturen. Z. Tropenmed. u. Parasit. 7, 99–109.Google Scholar
Rosenberg, L. E. (1937). The neuromotor system of Nyctotherus hylae. Univ. Calif. Publ. Zool. 41, 249–76.Google Scholar
Scholander, P. F., Claff, C. L. & Sveinsson, S. L. (1952). Respiratory studies of single cells. II. Observations on the oxygen consumption in single protozoans. Biol. Bull., Woods Hole, 102, 178–84.CrossRefGoogle Scholar
Simitch, T., Petrovitch, Z. & Chibalitch, D. (1954). La vitalité des kystes de Entamoeba dysenteriae en dehors de l'organisme de l'hôte. Arch. Inst. Pasteur d'Algérie, 32, 223–31.Google Scholar
Singh, B. N. (1941). Selectivity in bacterial food by soil amoebae in pure mixed culture in sterilized soil. Ann. Appl. Biol. 28, 52–64.CrossRefGoogle Scholar
Singh, B. N., Mathew, S. & Sreenivasaya, M. (1956). Occurrence and nature of an amoeba excystment factor produced by Aerobactor sp. Nature, Lond., 177, 621–2.Google Scholar
Smith, S. C. (1927). Excystation in Iodamoeba williamsi in vivo and in vitro. Science, 65, 69–70.Google Scholar
Snyder, T. L. & Meleney, H. E. (1941). The excystation of Endamoeba histolytica in bacteriologically sterile media. Amer. J. Trop. Med. 21, 63–73.Google Scholar
Spector, B. K. & Buky, F. (1934). Viability of Endamoeba histolytica and Endamoeba coli. U.S. Publ. Health Rep. 49, 379–86.Google Scholar
Stein, F. R. (1867). Der Organismus der Infusionsthiere, Vol. 3. Leipzig.Google Scholar
Stephenson, M. (1949). Bacterial Metabolism, 3rd ed. London: Longmans.Google Scholar
Strickland, A. G. R. & Haagen-Smit, A. J. (1947). Chemical substances inducing excystment of the resting cysts of Colpoda duodenaria. J. Cell. Comp. Physiol. 30, 381–90.Google Scholar
Strickland, A. G. R. & Haagen-Smit, A. J. (1948). The excystment of Colpoda duodenaria Science, 107, 204–5.Google Scholar
Swingle, H. S. (1925). Digestive enzymes of an insect. Ohio. J. Sci. 25, 209–18.Google Scholar
Taylor, C. V. & Strickland, A. G. R. (1936). Effects of high vacua and extreme temperatures on cysts of Colpoda cucullus. Physiol. Zool. 9, 15–26.CrossRefGoogle Scholar
van Wagtendonk, W. J. (1955). Encystment and excystment of Protozoa. Pp. 85–91 in Biochemistry and Physiology of Protozoa, ed. by Hutner, S. H. & Lwoff, A.New York: Academic Press Inc.Google Scholar
Weinman, D. & McAllister, J. (1947). Prolonged storage of human pathogenic Protozoa with conservation of virulence: observations on the storage of helminths and leptospiras. Amer. J. Hyg. 45, 102–21.Google Scholar
Wigglesworth, V. B. (1927). Digestion in the cockroach. 1. The hydrogen ion concentration in the alimentary canal. Biochem. J. 21, 791–6.CrossRefGoogle ScholarPubMed
Wigglesworth, V. B. (1928). Digestion in the cockroach. 3. The digestion of proteins and fats. Biochem. J. 22, 150–61.CrossRefGoogle Scholar
Wollman, E. (1926). Observations sur une lignée aseptique de blattes (Blattella germanica) datant de cinq ans. C.R. Soc. Biol., Paris, 95, 164–5.Google Scholar
Yorke, W. & Adams, A. R. D. (1926). Observations on Entamoeba histolytica. II. Longevity of the cysts in vitro, and their resistance to heat and to various drugs and chemicals. Ann. Trop. Med. Parasit. 20, 317–27.Google Scholar