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Interactions involving intestinal nematodes of rodents: experimental and field studies

Published online by Cambridge University Press:  24 October 2011

J. M. BEHNKE
Affiliation:
School of Life and Environmental Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK
A. BAJER
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul.Krakowskie Przedmiescie 26/28, 00-927 Warszawa, Poland
E. SINSKI
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul.Krakowskie Przedmiescie 26/28, 00-927 Warszawa, Poland
D. WAKELIN
Affiliation:
School of Life and Environmental Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK

Abstract

Multiple species infections with parasitic helminths, including nematodes, are common in wild rodent populations. In this paper we first define different types of associations and review experimental evidence for different categories of interactions. We conclude that whilst laboratory experiments have demonstrated unequivocally that both synergistic and antagonistic interactions involving nematodes exist, field work utilizing wild rodents has generally led to the conclusion that interactions between nematode species play no, or at most a minor, role in shaping helminth component communities. Nevertheless, we emphasize that analysis of interactions between parasites in laboratory systems has been fruitful, has made a fundamental contribution to our understanding of the mechanisms underlying host-protective intestinal immune responses, and has provided a rationale for studies on polyparasitism in human beings and domestic animals. Finally, we consider the practical implications for transmission of zoonotic diseases to human communities and to their domestic animals, and we identify the questions that merit research priority.

Type
Research Article
Copyright
© 2002 Cambridge University Press

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References

ABU-MADI, M. A., BEHNKE, J. M., LEWIS, J. W. & GILBERT, F. S. (1998). Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 72, 93100.CrossRefGoogle Scholar
ABU-MADI, M. A., BEHNKE, J. M., LEWIS, J. W. & GILBERT, F. S. (2000). Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74, 716.Google Scholar
ADAMS, D. B., ANDERSON, B. H. & WINDON, R. G. (1989). Cross immunity between Haemonchus contortus and Trichostrongylus colubriformis in sheep. International Journal for Parasitology 19, 717722.CrossRefGoogle Scholar
ALGHALI, S. T. O., HAGAN, P. & ROBINSON, M. (1985). Hymenolepis citelli (Cestoda) and Nematospiroides dubius (Nematoda): interspecific interactions in mice. Experimental Parasitology 60, 369370.CrossRefGoogle Scholar
ALLEN, J. E. & MACDONALD, A. S. (1998). Profound suppression of cellular proliferation mediated by the secretions of nematodes. Parasite Immunology 20, 241247.CrossRefGoogle Scholar
AL SAQUR, I., ARMOUR, J., BAIRDEN, K., DUNN, A. M., JENNINGS, F. W. & MURRAY, M. (1984). Experimental studies on the interaction between infections of Ostertagia leptospicularis and other bovine Ostertagia species. Zeitschrift für Parasitenkunde 70, 809817.CrossRefGoogle Scholar
ASHFORD, R. W., CRAIG, P. S. & OPPENHEIMER, S. J. (1992). Polyparasitism on the Kenyan coast. 1. Prevalence and association between parasitic infections. Annals of Tropical Medicine and Parasitology 86, 671679.Google Scholar
BAJER, A., BEHNKE, J. M., BEDNARSKA, M., KANICKA, M. & SINSKI, E. (2000). The common vole (Microtus arvalis) as a competent host for Cryptosporidium parvum. (EMOP VIII, Poznan, 10–14 September, 2000.) Acta Parasitologica 45, 178.Google Scholar
BANCROFT, A. J., ELSE, K. J. & GRENCIS, R. K. (1994). Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response. European Journal of Immunology 24, 31133118.CrossRefGoogle Scholar
BARNARD, C. J. & BEHNKE, J. M. (Eds) (1990). Parasitism and Host Behaviour. London, Taylor & Francis.Google Scholar
BEDNARSKA, M., BAJER, A. & SINSKI, E. (1998). Calves as a potential reservoir of Cryptosporidium parvum and Giardia spp. Annals of Agricultural and Environmental Medicine 5, 135138.Google Scholar
BEHNKE, J. M. (1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 171.CrossRefGoogle Scholar
BEHNKE, J. M., ALI, N. M. H. & JENKINS, S. N. (1984). Survival to patency of low level infections with Trichuris muris in mice concurrently infected with Nematospiroides dubius. Annals of Tropical Medicine and Parasitology 78, 509517.CrossRefGoogle Scholar
BEHNKE, J. M., BLAND, P. W. & WAKELIN, D. (1977). The effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in mice. Parasitology 75, 7988.CrossRefGoogle Scholar
BEHNKE, J. M., CABAJ, W. & WAKELIN, D. (1992). The susceptibility of adult Heligmosomoides polygyrus to intestinal inflammatory responses induced by heterologous infection. International Journal for Parasitology 22, 7586.CrossRefGoogle Scholar
BEHNKE, J. M., KEYMER, A. E. & LEWIS, J. W. (1991). Heligmosomoides polygyrus or Nematospiroides dubius? Parasitology Today 7, 177179.Google Scholar
BEHNKE, J. M., LEWIS, J. W., MOHD ZAIN, S. N. & GILBERT, F. S. (1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 3144.Google Scholar
BEHNKE, J. M., LOWE, A., MENGE, D., IRAQI, F. & WAKELIN, D. (2000). Mapping the genes for resistance to gastrointestinal nematodes. Acta Parasitologica 45, 113.Google Scholar
BEHNKE, J. M., ROSE, R. & LITTLE, J. (1994). Resistance of the hookworms Ancylostoma ceylanicum and Necator americanus to intestinal inflammatory responses induced by heterologous infection. International Journal for Parasitology 24, 425431.CrossRefGoogle Scholar
BEHNKE, J. M., SINSKI, E. & WAKELIN, D. (1999). Primary infections with Babesia microti are not prolonged by concurrent Heligmosomoides polygyrus. Parasitology International 48, 183187.CrossRefGoogle Scholar
BEHNKE, J. M., WAHID, F. N., GRENCIS, R. K., ELSE, K. J., BENSMITH, A. W. & GOYAL, P. K. (1993). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): downregulation of specific cytokine secretion (IL-9 and IL-10) correlates with poor mastocytosis and chronic survival of adult worms. Parasite Immunology 15, 415421.CrossRefGoogle Scholar
BEHNKE, J. M. & WAKELIN, D. (1973). The survival of Trichuris muris in wild populations of its natural hosts Parasitology 67, 157164.Google Scholar
BEHNKE, J. M., WAKELIN, D. & WILSON, M. M. (1978). Trichinella spiralis: Delayed rejection in mice concurently infected with Nematospiroides dubius. Experimental Parasitology 46, 121130.CrossRefGoogle Scholar
BENTWICH, Z., KALINKOVICH, A. & WEISMAN, Z. (1995). Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunology Today 16, 187191.CrossRefGoogle Scholar
BOGGS, J. F., MCMURRAY, S. T., LESLIE, D. M. JR., ENGLE, D. M. & LOCHMILLER, R. L. (1991). Influence of habitat modification on the community of gastrointestinal helminths of cotton rats. Journal of Wildlife Diseases 27, 584593.CrossRefGoogle Scholar
BROPHY, P. M. & PRITCHARD, D. I. (1992). Immunity to helminths: ready to tip the biochemical balance? Parasitology Today 8, 419422.Google Scholar
BRUCE, R. G. & WAKELIN, D. (1977). Immunological interaction between Trichinella spiralis and Trichuris muris in the intestine of the mouse. Parasitology 74, 163173.CrossRefGoogle Scholar
, A. A., ANDERSON, R. I., MACRAE, A. A. & FAIN, A. (1978). Epidemiology of poly-parasitism. I. Occurrence, frequency and distribution of multiple infections in rural communities on Chad, Peru, Afganistan and Zaire. Tropical Medicine and Parasitology 29, 6170.Google Scholar
BUNDY, D. A. P. & BLUMENTHAL, U. J. (1990). Human behaviour and the epidemiology of helminth infections: the role of behaviour in exposure to infection. In Parasitism and Host Behaviour (ed. BARNARD, C. J. & BEHNKE, J. M.), pp. 264289. London, Taylor & Francis.
BUSH, A. O. & HOLMES, J. C. (1986). Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology 64, 142152.CrossRefGoogle Scholar
CHAN, L., BUNDY, D. A. P. & KAN, S. P. (1994). Genetic relatedness as a determinant of predispostition to Ascaris lumbricoides and Trichuris trichiura infection. Parasitology 108, 7780.CrossRefGoogle Scholar
CHRISTENSEN, N. O., NANSEN, P., FAGBEMI, B. O. & MONRAD, J. (1987). Heterologous antagonistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387410.CrossRefGoogle Scholar
CHRISTIE, P. R., WAKELIN, D. & WILSON, M. M. (1979). The effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in rats. Parasitology 78, 323330.CrossRefGoogle Scholar
CHUNGE, R. N., KARUMBA, N., OUMA, J. H., THIONGO, F. W., STURROCK, R. F. & BUTTERWORTH, A. E. (1995). Polyparasitism in two rural communities with endemic Schistosoma mansoni infection in Machakos District, Kenya. Journal of Tropical Medicine and Hygiene 98, 440444.Google Scholar
CROMPTON, D. W. T. (1973). Sites occupied by some parasitic helminths in the alimentary tract of vertebrates. Biological Reviews 48, 2783.CrossRefGoogle Scholar
CURRY, A. J., ELSE, K. J., JONES, F., BANCROFT, A., GRENCIS, R. K. & DUNNE, D. W. (1995). Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. Journal of Experimental Medicine 181, 769774.CrossRefGoogle Scholar
DEHLAWI, M. S. & WAKELIN, D. (1995). Dose dependency of mucosal mast cell responses in mice infected with Trichinella spiralis. Research and Reviews in Parasitology 55, 2124.Google Scholar
DEHLAWI, M. S., WAKELIN, D. & BEHNKE, J. M. (1987). Suppression of mucosal mastocytosis by infection with the intestinal nematode Nematospiroides dubius. Parasite Immunology 9, 187194.CrossRefGoogle Scholar
DOBSON, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317347.CrossRefGoogle Scholar
ELSE, K. J. & FINKELMAN, F. D. (1999). Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 11451158.Google Scholar
EMERY, D. L. & WAGLAND, B. M. (1991). Vaccines against gastrointestinal nematode parasites of ruminants. Parasitology Today 7, 347349.CrossRefGoogle Scholar
FERRETTI, G., GABRIELE, F., PALMAS, C. & WAKELIN, D. (1984). Interactions between Trichinella spiralis and Hymenolepis nana in the intestine of the mouse. International Journal for Parasitology 14, 2933.CrossRefGoogle Scholar
FLOWERDEW, J. R. (1985). The population dynamics of wood mice and yellow-necked mice. In The Ecology of Woodland Rodents, Bank Voles and Wood Mice (eds. Flowerdew, J. R., Gurnell, J. & Gipps, J. H. W.), pp. 315338 Symposia of the Zoological Society of London 55.
GLIWICZ, J. (1983). Survival and life span. In Ecology Of The Bank Vole (ed. Petrusewicz, K.) Acta Theriologica 28 (suppl 1), 161172.CrossRef
GREGORY, R. D., KEYMER, A. E. & CLARKE, J. R. (1990). Genetics, sex and exposure: the ecology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 59, 363378.CrossRefGoogle Scholar
GRENCIS, R. K. (1997). Th2-mediated host protective immunity in intestinal nematode infections. Philosophical Transactions of the Royal Society of London B 352, 13771384.CrossRefGoogle Scholar
HAUKISALMI, V. & HENTTONEN, H. (1993a). Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. Journal of Animal Ecology 62, 221229.Google Scholar
HAUKISALMI, V. & HENTTONEN, H. (1993b). Coexistence in helminths of the bank vole Clethrionomys glareolus. II. Intestinal distribution and interspecific interactions. Journal of Animal Ecology 62, 230238.Google Scholar
HAUKISALMI, V., HENTTONEN, H. & TENORA, F. (1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807825.CrossRefGoogle Scholar
HAUKISALMI, V. & TENORA, F. (1993). Catenotaenia henttoneni sp. n. (Cestoda: Catenotaeniidae), a parasite of voles Clethrionomys glareolus and C. rutilus (Rodentia). Folia Parasitologica 40, 2933.Google Scholar
HERMANEK, J., GOYAL, P. K. & WAKELIN, D. (1994). Lymphocyte, antibody and cytokine responses during concurrent infections between helminths that selectively promote T-helper-1 or T-helper-2 activity. Parasite Immunology 16, 111117.Google Scholar
HOBBS, R. P. (1980). Interspecific interactions among gastrointestinal helminths in pikas of North America. American Midland Naturalist 103, 1525.CrossRefGoogle Scholar
HOLLAND, C. (1987). Interspecific effects between Moniliformis (Acanthocephala), Hymenolepis (Cestoda) and Nippostrongylus (Nematoda) in the laboratory rat. Parasitology 94, 567581.CrossRefGoogle Scholar
HOLMES, J. C. (1961). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acantheocephala). I. General effects and comparison with crowding. Journal of Parasitology 47, 209216.Google Scholar
HOLMES, J. C. (1973). Site selection by parasitic helminths: interspecific interactions, site segregation and their importance to the development of the helminth communities. Canadian Journal of Zoology 51, 333347.CrossRefGoogle Scholar
HOPKINS, C. A. (1980). Immunity and Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. ARAI, H. P.), pp. 551614. New York, Academic Press.CrossRef
HOTEZ, P. J. & PRITCHARD, D. I. (1995). Hookworm infection. Scientific American June 1995, 4248.CrossRefGoogle Scholar
HOWARD, R. J., CHRISTIE, D., WAKELIN, D., WILSON, M. M. & BEHNKE, J. M. (1978). The effect of concurrent infection with Trichinella spiralis on Hymenolepis microstoma in mice. Parasitology 77, 273279.CrossRefGoogle Scholar
JAMES, S. L. (1997). Emerging parasitic infections. FEMS Immunology and Medical Microbiology 18, 313317.CrossRefGoogle Scholar
JENKINS, S. N. & BEHNKE, J. M. (1977). Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75, 7178.CrossRefGoogle Scholar
KALKOFEN, U. P. (1970). Attachment and feeding behaviour of Ancylostoma caninum. Zeitschirft für Parasitenkunde 33, 339354.CrossRefGoogle Scholar
KENNEDY, C. R, BUSH, A. O. & AHO, J. M. (1986). Patterns in helminth communities: why are birds and fish different? Parasitology 93, 205215.Google Scholar
KENNEDY, M. W. (1980). Immunologically mediated, non-specific interactions between the intestinal phases of Trichinella spiralis and Nippostrongylus brasiliensis in the mouse. Parasitology 80, 6172.CrossRefGoogle Scholar
KEUSCH, G. T. & MIGASENA, P. (1982). Biological implications of polyparasitism. Reviews of Infectious Diseases 4, 880882.CrossRefGoogle Scholar
KHAN, A. I., HORII, Y., TIURUA, R., SATO, Y. & NAWA, Y. (1993). Mucosal mast cells and the expulsive mechanisms of mice against Strongyloides venezuelensis. International Journal for Parasitology 23, 551555.CrossRefGoogle Scholar
KISIELEWSKA, K. (1970a). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). 1. Structure and seasonal dynamics of helminth groupings in a host population in the Białowieża National Park. Acta Parasitologica Polonica 18, 121147.Google Scholar
KISIELEWSKA, K. (1970b). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). V. Some questions concerning helminth groupings in the host individuals. Acta Parasitologica Polonica 17, 197208.Google Scholar
KLOOSTERMAN, A., PLOEGER, H. W. & FRANKENA, K. (1990). Increased establishment of lungworms after exposure to a combined infection of Ostertagia ostertagi and Cooperia oncophora. Veterinary Parasitology 36, 117122.CrossRefGoogle Scholar
KVALSVIG, J. D. (1988). The effects of parasitic infection on cognitive performance. Parasitology Today 4, 206208.CrossRefGoogle Scholar
LEE, T. D. G., GRENCIS, R. K. & WAKELIN, D. (1982). Specific cross-immunity between Trichinella spiralis and Trichuris muris: immunization with heterologous infections and antigens and transfer of immunity with heterologous immune mesenteric lymph node cells. Parasitology 84, 381389.CrossRefGoogle Scholar
LEWIS, J. W. (1968a). Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology, London 154, 287312.Google Scholar
LEWIS, J. W. (1968b). Studies on the helminth parasites of voles and shrews from Wales. Journal of Zoology, London 154, 313331.Google Scholar
LOTZ, J. M. & FONT, W. F. (1994). Excess positive associations in communities of intestinal helminths of bats: a refined null hypothesis and a test of the facilitation hypothesis. Journal of Parasitology 80, 398413.CrossRefGoogle Scholar
MARTIN, J. L. & HUFFMAN, D. G. (1980). An analysis of the community and population dynamics of the helminths of Sigmodon hispidus (Rodentia: Criceditae) from three central Texas vegetational regions. Proceedings of the Helminthological Society of Washington 47, 247255.Google Scholar
MESZAROS, F. (1977). Parasitic nematodes of Microtus arvalis (Rodentia) in Hungary. Parasitologica Hungarica 10, 6783.Google Scholar
MITCHELL, G. F. (1979). Effector cells, molecules and mechanisms in host-protective immunity to parasites. Immunology 38, 209223.Google Scholar
MOLLHAGEN, T. (1978). Habitat influence on helminth parasitism of the cotton rat in western Texas, with remarks on some of the parasites. The Southwestern Naturalist 23, 401408.CrossRefGoogle Scholar
MONROY, F. G. & ENRIQUEZ, F. J. (1992). Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitology Today 8, 4954.CrossRefGoogle Scholar
MONTGOMERY, S. S. J. & MONTGOMERY, W. I. (1988). Cyclic and non-cyclic dynamics in populations of the helminth parasites of wood mice Apodemus sylvaticus. Journal of Helminthology 62, 7890.CrossRefGoogle Scholar
MONTGOMERY, S. S. J. & MONTGOMERY, W. I. (1989). Spatial and temporal variation in the infracommunity structure of helminths of Apodemus sylvaticus (Rodentia: Muridae). Parasitology 98, 145150.CrossRefGoogle Scholar
MONTGOMERY, S. S. J. & MONTGOMERY, W. I. (1990). Structure, stability and species interactions in helminth communities of wood mice, Apodemus sylvaticus. International Journal for Parasitology 20, 225242.CrossRefGoogle Scholar
MOORE, J. & SIMBERLOFF, D. (1990). Gastrointestinal helminth communities of bobwhite quail. Ecology 71, 344359.CrossRefGoogle Scholar
NAWA, Y., ISHIKAWA, N., TSUCHIYA, K., HORII, Y., ABE, T., KHAN, A. I., BING-SHI, ITOH, H., IDE, H. & UCHIYAMA, F. (1994). Selective effector mechanisms for the expulsion of intestinal helminths. Parasite Immunology 16, 333338.CrossRefGoogle Scholar
NAWA, Y. & KORENAGA, M. (1983). Mast and goblet cell responses in the small intestine of rats concurrently infected with Nippostrongylus brasiliensis and Strongyloides ratti. Journal of Parasitology 69, 11681170.CrossRefGoogle Scholar
PENCE, D. B., CRUM, J. M. & CONTI, J. A. (1983). Ecological analyses of helminth populations in the black bear, Ursus americanus, from North America. Journal of Parasitology 69, 933950.CrossRefGoogle Scholar
PETNEY, T. N. & ANDREWS, R. H. (1998). Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28, 377393.CrossRefGoogle Scholar
PHILLIPS, R. S., SELBY, G. R. & WAKELIN, D. (1974). The effect of Plasmodium berghei and Trypanosoma brucei infections on the immune expulsion of the nematode Trichuris muris from mice. International Journal for Parasitology 4, 409415.CrossRefGoogle Scholar
PHILLIPS, R. S. & WAKELIN, D. (1976). Trichuris muris: effect of concurrent infections with rodent piroplasms on immune expulsion from mice. Experimental Parasitology 39, 95100.CrossRefGoogle Scholar
PRICE, P. W. (1980). Evolutionary biology of parasites. Monographs in Population Biology 15, Princeton University Press, Princeton, New Jersey, USA.Google Scholar
PRITCHARD, D. I. & BEHNKE, J. M. (1985). The suppression of homologous immunity by soluble adult antigens of Nematospiroides dubius. Journal of Helminthology 59, 251256.CrossRefGoogle Scholar
QUINNELL, R. J., BEHNKE, J. M. & KEYMER, A. E. (1991). Host specificity of and cross-immunity between two strains of Heligmosomoides polygyrus. Parasitology 102, 419427.CrossRefGoogle Scholar
ROBERTS-THOMSON, I. C., GROVE, D. I., STEVENS, D. P. & WARREN, K. S. (1976). Suppression of giardiasis during the intestinal phase of trichinosis in the mouse. Gut 17, 953958.CrossRefGoogle Scholar
ROBINSON, M., WAHID, F. N., BEHNKE, J. M. & GILBERT, F. S. (1989). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): dose-dependent expulsion of adult worms. Parasitology 98, 115124.CrossRefGoogle Scholar
ROHDE, K. (1979). A critical evaluation of intrinsic and extrinsic factors responsible for restriction in parasites. The American Naturalist 114, 648671.CrossRefGoogle Scholar
ROSE, M. E., WAKELIN, D. & HESKETH, P. (1994). Interactions between infections with Eimeria spp. and Trichinella spiralis in inbred mice. Parasitology 108, 6975.Google Scholar
SCHAD, G. A. (1963). Niche diversification in a parasitic species flock. Nature, London 198, 404406.CrossRefGoogle Scholar
SMITH, N. C. & BRYANT, C. (1986). The role of host generated free radicals in helminth infections: Nippostrongylus brasiliensis and Nematospiroides dubius compared. International Journal for Parasitology 16, 617622.CrossRefGoogle Scholar
SOMMERVILLE, R. I. (1963). Distribution of some parasitic nematodes in the alimentary tract of sheep, cattle and rabbits. Journal of Parasitology 49, 593599.CrossRefGoogle Scholar
STEWART, G. L., REDDINGTON, J. J. & HAMILTON, A. M. (1980). Eimeria nieschulzi and Trichinella spiralis in the rat. Experimental Parasitology 50, 115122.CrossRefGoogle Scholar
TELFORD, G., WHEELER, D. J., APPLEBY, P., BOWEN, J. G. & PRITCHARD, D. I. (1998). Heligmosomoides polygyrus immunomodulatory factor (IMF) targets T-lymphocytes. Parasite Immunology 20, 601611.CrossRefGoogle Scholar
TENORA, F. & MESZAROS, F. (1971). Nematodes of the genus Heligmosomum Railliet et Henry, 1909), sensu Durette-Desset, 1968), parasitizing rodents in Europe. Acta Zoologica Academiae Scientiarum Hungaricae 17, 397407.Google Scholar
TENORA, F. & MESZAROS, F. (1975). Nematodes of the genus Syphacia, Seurat, 1916) (Nematoda) – parasites of rodents (Rodentia) in Czechoslovakia and Hungary. Acta Universitatis Agriculturae, Brno 23, 537554.Google Scholar
TENORA, F. & STANEK, M. (1995). Changes of the helminthofauna in several muridae and Arvicolidae at Lednice in Moravia. II. Ecology. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 43, 5765.Google Scholar
WAID, D. D., PENCE, D. B. & WARREN, R. J. (1985). Effects of season and physical condition on the gastrointestinal community of white-tailed deer from Texas Edwards Plateau. Journal of Wildlife Diseases 21, 264273.CrossRefGoogle Scholar