Tetrahymenid ciliates as parasites of the gray garden slug
Author
Wayne M. BrooksAuthor Affiliations
Wayne M. Brooks was Junior Specialist in the Experiment Station, Berkeley, and is presently Assistant Professor of Entomology, North Carolina State University, Raleigh, North Carolina.Publication Information
Hilgardia 39(8):205-276. DOI:10.3733/hilg.v39n08p205. June 1968.
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Abstract
The role of two species of holotrichous ciliates, Tetrahymena limacis and T. rostrata, as parasites of the gray garden slug, Deroceras reticulatum, was examined. Infectivity tests with each ciliate species demonstrated that T. rostrata was pathogenic for D. reticulatum, producing subacute, lethal infections. Infection with T. limacis was not fatal. The only noticeable effect was a significant difference in the size and weight of the newly hatched slugs that had been exposed to a heavy concentration of ciliates.
Histological examination of naturally and experimentally infected slugs revealed that T. limacis was confined to the lumen of the alimentary tract, primarily to the lumina of the liver lobules. No distinct cytopathologic effects were observed. In contrast, infection with T. rostrata was marked by extensive damage and inflammation, particularly in the kidney and other pulmonary organs and tissues. Ciliates were shown to enter a dorsal integumental pouch posterior to the mantle of the slug and penetrate to the loose, connective tissue of the body wall. Upon migration to the kidney via the venous system, the ciliates rapidly multiplied and eventually invaded most of the other slug tissues and organs.
Through parasitization of the albumen gland, T. rostrata was incorporated into eggs during their formation in the genital tract of D. reticulatum. A study of ciliare-infected eggs revealed that T. rostrata was transmitted trans-ovum. Embryos became infected when ciliates were apparently ingested during the aspiration of albumen. While some of the infected embryos freed themselves of ciliates after hatching, the others succumbed within the eggs or died soon after hatching.
Six new host records were discovered for T. limacis, and three were discovered for T. rostrata in the course of observations of slug parasitization in the field. Mixed infections were also found, and the free-living phase of each ciliate species was recovered from soil samples.
Ancillary observations of Colpoda steinii confirmed the general opinion that this ciliate is a harmless edaphic species, which occasionally occurs in the intestinal tracts of various snails and slugs.
Literature Cited
Anderson R. C. On the development and transmission of Cosmocercoides dukae of terrestrial molluscs in Ontario. Can. Jour. Zool. 1960. 38:801-25.
Arias R. O., Crowell H. H. A contribution to the biology of the gray garden slug. Bul. S. Calif. Acad. Sci. 1963. 62:83-97.
Baecker R. Die Mikromorphologie von Helix pomatia und einigen anderen Stylommatophoren. Ztschr. Ges. Anat. Abt. III. Ergeb. Anat. und Entwicklungsgesche. 1932. 29:449-585.
Barthélemy M. A. Études sur le développement et les migrations d’un nématoide parasite de l’oeuf de la limace grise. Ann. Sci. Nat. Zool. 1858. 9:41-48.
Berghe L. van den. Sur un ciliate parasite de pontes de mollusques d’eau douce, Glaucoma paedophthora n. sp. Compt. Rend. Soc. Biol. 1934. 115:1423-26.
Borden V. C. Ciliates from Deroceras agreste 1948. p.15. Unpublished master’s thesis, Univ. of Virginia.
Burch J. B. A soil protozoan infecting land snails. (Abstr.) 1961. Amer. Malacol. Union, Ann. Rept. No. 27.
Carrick R. The life history and development of Agriolimax agrestis L., the gray field slug. Trans. Roy. Soc. Edinburgh. 1938. 59:563-97.
Chernin E. Cultivation of the snail, Australorbis glabratus, under axenic conditions. Ann. N. Y. Acad. Sci. 1959. 77:237-45.
Chitwood B. G., Chitwood M. B. Snails as hosts and carriers of nematodes and nematomorpha. Nautilus. 1937. 50:130-35.
Conte A., Bonnet A. Sur un nématodes nouveau Angiostoma helicis n. sp. parasite de l’appareil genital d’Helix aspersa (Müller). Compt. Rend. Soc. Biol. 1903. 55:198-99.
Corliss J. O. Review of the genus Tetrahymena. (Abstr.) Proc. Soc. Protozool. 1952a. 3:3
Corliss J. O. Le cycle autogamique de Tetrahymena rostrata. Compt. Rend. Acad. Sci. 1952b. 235:399-402.
Corliss J. O. Nuclear reorganization (autogamy) in a species of Tetrahymena. (Abstr.). Proc. Soc. Protozool. 1952c. 3:4
Corliss J. O. Comparative studies on holotrichous ciliates in the Colpidium-Glaucoma-Leucophrys-Tetrahymena group. II. Morphology, life cycles, and systematic status of strains in pure culture. Parasitol. 1953. 43:49-87.
Corliss J. O. The literature on Tetrahymena: its history, growth, and recent trends. Jour. Protozool. 1954. 1:156-69.
Corliss J. O. Tetrahymena chironomi sp. nov., a ciliate from midge larvae, and the current status of facultative parasitism in the genus Tetrahymena. Parasitol. 1960. 50:111-53.
Corliss J. O. Facultative parasitism in protozoa and its possible evolutionary significance. Parasitol. 1962. 52:10
Corliss J. O. L’autogamie et la sénescense du cilié Hyménostome Tetrahymena rostrata (Kahl). Ann. Biol. 1965. 4:49-69.
Corliss J. O., Smith A. C., Foulkes J. A species of Tetrahymena from the British garden slug, Milax budapestensis. Nature. 1962. 196:1008-09.
De Leon W. Balantidium haughwouti, n. sp. parasitic in the intestinal tract of Ampullaria species, a morphological study. Phil. Jour. Sci. 1919. 15:389-409.
Dobrza?ska J. Investigations on ciliates living in lamellibranchiates of small water bodies. Bul. Acad. pol. Sci. Cl. II Sér. Sci. biol. 1958. 6:113-18.
Dobrza?ska J. The occurrence of ciliates of the genus Tetrahymena Furgason, 1940, in fresh-water mussels. Bul. Acad. pol. Sci. Cl. II Sér. Sci. biol. 1959. 7:377-83.
Hanitsch R. Contributions to the anatomy and histology of Limax agrestis. Proc. Liverpool Biol. Soc. 1888. 2:152-70.
Kahl A. Neue und wenig bekannte Formen der holotrichen und heterotrichen Ciliaten. Arch. Protistenk. 1926. 55:197-438.
Kazubski S. L. Trichia lubomirskii Slós (Helicidae), a new host of Tetrahymena limacis (Warren, 1932) Kozloff, 1946 (Ciliata) and Zonitoides nitidus Müll. (Zonitidae), a new host of T. rostrata (Kahl, 1926) Corliss, 1952, in Poland. Bul. Acad. pol. Sci. Cl. II Sér. Sci. biol. 1958. 6:247-52.
Kazubski S. L. Studies on the ciliate parasites of the land snails in Poland in the years 1956-1958. (Abstr.) Jour. Protozool. 1959. 6(Suppl.):24
Klein B. M. The “dry” silver method and its proper use. Jour. Protozool. 1958. 5:99-103.
Kozloff E. N. The morphology and systematic position of a holotrichous ciliate parasitizing Deroceras agresta (L.). Jour. Morphol. 1946. 79:445-65.
Kozloff E. N. Experimental infection of the gray garden slug, Deroceras reticulatum (Müller), by the holotrichous ciliate Tetrahymena pyriformis (Ehrenberg). Jour. Protozool. 1956a. 3:17-19.
Kozloff E. N. A comparison of the parasitic phase of Tetrahymena limacis (Warren) with clones in culture, with particular reference to variability in the number of primary ciliary meridians. Jour. Protozool. 1956b. 3:20-28.
Kozloff E. N. Tetrahymena limacis from the terrestrial pulmonate gastropods Monadenia fidelis and Prophysaon andersoni. Jour. Protozool. 1956c. 3:204-08.
Kozloff E. N. A species of Tetrahymena parasitic in the renal organ of the slug Deroceras reticulatum. Jour. Protozool. 1957. 4:75-79.
Krijgsman B. J. Arbeitsrhythmus der Verdauungsdrüsen bei Helix pomatia I. Teil: Die natuerlichen Bedingungen. Z. vergl. Physiol. 1925. 2:264-96.
Lovett A. L., Black A. B. The gray garden slug with notes on allied forms. Oregon Agr. Coll. Exp. Sta. Bul. 1920. 170:1-43.
McArdle E. W. A comparative investigation of clonal strains of the holotrich ciliate Tetrahymena rostrata 1960. p.68. Ph.D. Thesis. Univ. of Illinois.
Meggitt F. A. A contribution to the knowledge of the tapeworm of fowls and of sparrows. Parasitol. 1916. 8:390-409. DOI: 10.1017/S0031182000010684 [CrossRef]
Michelson E. H. Plistophora husseyi sp. n., a microsporidian parasite of aquatic pulmonate snails. Jour. Insect Pathol. 1963. 5:28-38.
Pan C. T. The general histology and topographic microanatomy of Australorbis glabratus. Bul. Mus. Comp. Zool. 1958. 119:238-99.
Pan C. T. Generalized and focal tissue responses in the snail Australorbis glabratus, infected with Schistosoma mansoni. Ann. N. Y. Acad. Sci. 1963. 113:475-85.
Pan C. T. Studies on the host-parasite relationship between Schistosoma mansoni and the snail Australorbis glabratus. Amer. Jour. Trop. Med. &; Hyg. 1965. 14:931-76.
Perez M. Recherches anatomiques et physiologiques sur l’Anguillule terrestre (Rhabditis terricola, Dujardin). Ann. Sci. Nat. Zool. 1866. 6:152-307.
Reynolds B. D. Colpoda steinii, a facultative parasite of the land slug. Agriolimax agrestis. Jour. Parasitol. 1936. 22:48-53.
Romeis B. Mikroskopische Technik. 1948. Munchen, Germany: R. Oldenbourg. 695p.
Stephenson J. W., Knutson L. V. A résumé of recent studies of invertebrates associated with slugs. Jour. Econ. Entomol. 1966. 59:356-60.
Stout J. C. The ecology, life history and parasitism of Tetrahymena (Paraglaucoma) rostrata (Kahl) Corliss. Jour. Protozool. 1954. 1:211-15.
Thompson J. C. Jr. Inoculation of various hosts with species of Tetrahymena (Abstr.). Bul. Assoc. Southeastern Biologists. 1955. 2:11
Thompson J. C. Jr. Experimental infections of various animals, with strains of the genus Tetrahymena. Jour. Protozool. 1958a. 5:203-05.
Thompson J. C. Jr. Tetrahymena rostrata as a facultative parasite in the gray garden slug. Virginia Jour. Sci. 1958b. 9:315-18.
Warren E. On a cilate protozoan inhabiting the liver of a slug. Ann. Natal Mus. 1932. 7:1-53.
Wilhelm W. E. The role of bacteria in the production of encystment and autogamy in Tetrahymena rostrata. (Abstr.). Jour. Protozool. 1960. 7(Suppl.):27
Windsor D. A. Colpoda steinii and Tetrahymena limacis in several terrestial pulmonate gastropods collected in Illinois. (Abstr.) Jour. Protozool. 1959. 6(Suppl.):33
Windsor D. A. Morphological changes exhibited by Tetrahymena limacis upon isolation from newly discovered hosts. (Abstr.) Jour. Protozool. 1960. 7(Suppl.):27
Zerling M. R. Une Astasia sans flagelle, Astasia doridis, n. sp., parasite des pontes de nudibranches. Compt. Rend. Soc. Biol. 1933. 112:643-44.