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Aquatic molluscs as auxiliary hosts for terrestrial nematode parasites: implications for pathogen transmission in a changing climate

Published online by Cambridge University Press:  14 April 2010

N. J. MORLEY*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
*
*Corresponding author: Tel: +44 (0) 1784 443186. Fax: +44 (0) 1784 414224. E-mail: [email protected]

Summary

Nematodes are common parasites of molluscs but are often overlooked. Both metastrongyloid and rhabditoid species dominate the fauna within land snail and slug populations. Nevertheless, a key characteristic of many laboratory studies is the ability of these terrestrial nematodes to utilize aquatic molluscs as auxiliary hosts. The significance of this to the ecology of the parasite has never been evaluated. There is increasing concern as to the impact of climate change on the epidemiology of many parasitic diseases. In particular, it has been suggested that host switching may increase under the pressure of extreme climatic conditions. It is therefore timely to assess the role that aquatic molluscs may play in transmitting terrestrial nematodes, which include species of medical and veterinary importance such as Angiostrongylus cantonensis, A. vasorum, and Muellerius capillaris. The present review assesses the mechanisms of terrestrial nematode transmission through aquatic molluscs focusing on metastrongyloid and rhabditoid species, the importance of variable susceptibility of molluscan hosts, field studies on natural occurrence within aquatic habitats, and the impact of extreme climatic events (floods and droughts) that may increase in frequency under climate change.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Abo-Madyan, A. A., Morsy, T. A., Motawea, S. M., El Garhy, M. F. and Massoud, A. M. (2005). Spot light survey on freshwater snails of medical importance in Al Fayoum Governorate, Egypt. Journal of the Egyptian Society of Parasitology 35, 4958.Google ScholarPubMed
Alicata, J. E. and Jindrak, K. (1970). Angiostrongylosis in the Pacific and Southeast Asia. Charles C. Thomas, Springfield, Illinois, USA.Google Scholar
Anderson, R. C. (1962). The systematics and transmission of new and previously described Metastrongyles (Nematoda: Metastrongylidae) from Mustela vison. Canadian Journal of Zoology 40, 893920.CrossRefGoogle Scholar
Anderson, R. C. (1963 a). The incidence, development, and experimental transmission of Pneumostrongylus tenuis Dougherty (Metastrongloidea: Protostrongylidae) of the meninges of the white-tailed deer (Odocoileus virginianus borealis) in Ontario. Canadian Journal of Zoology 41, 775792.CrossRefGoogle Scholar
Anderson, R. C. (1963 b). Further studies on the taxonomy of metastrongyles (Nematoda: Metastrongyloidea) of Mustelidae in Ontario. Canadian Journal of Zoology 41, 801809.CrossRefGoogle Scholar
Anderson, R. C. (2000). Nematode Parasites of Vertebrates. 2nd Edn, CABI Publishing, Wallingford, UK.CrossRefGoogle Scholar
Arrinda, C., Perera, G. and Yong, M. (1989). Cuban oyster (Crassostrea rizophorae) as intermediate host of Angiostrongylus cantonensis. Journal of Medical & Applied Malacology 1, 133137.Google Scholar
Ash, L. R. (1968). The occurrence of Angiostrongylus cantonensis in frogs of New Caledonia with observations on paratenic host of metastrongyles. Journal of Parasitology 54, 432436.CrossRefGoogle Scholar
Azzam, K. M. (1998). First record of the snail parasitic nematode Rhabditis sp. isolated from Egyptian terrestrial snails and its capability to infect other pests. Egyptian Journal of Biological Pest Control 8, 2429.Google Scholar
Azzam, K. M. and Belal, M. H. (2006). Survey on the nematodes isolated from aquatic snails and their potential as biocontrol agents of snails. Bulletin of the Faculty of Agriculture, Cairo University 57, 185198.Google Scholar
Azzam, K. M. and Tawfik, M. F. S. (2003). Capability of the nematode Phasmarhabditis tawfiki Azzam to infect some snails, slugs and insect larvae in the laboratory. Journal of the Egyptian German Society for Zoology 42D, 2732.Google Scholar
Ballantyne, R. J. (1991). Life history and development of Pneumonema tiliquae (Nematoda: Rhabdiasidae). International Journal for Parasitology 21, 521533.CrossRefGoogle Scholar
Banevicius, N. M. S., Zanotti-Magalhaes, E. M., Magalhaes, L. A. and Linhares, A. X. (2006). Behavior of Angiostrongylus costaricensis in planorbids. Brazilian Journal of Biology 66, 199204.CrossRefGoogle ScholarPubMed
Barcante, T. A., Barcante, J. M. P., Dias, S. R. C. and Lima, W. S. (2003). Angiostrongylus vasorum (Baillet, 1866) Kamensky, 1905: Emergence of third-stage larvae from infected Biomphalaria glabrata snails. Parasitology Research 91, 471475.CrossRefGoogle ScholarPubMed
Bartlett, C. M. and Anderson, R. C. (1985). Larval nematodes (Ascaridida and Spirurida) in the aquatic snail, Lymnaea stagnalis. Journal of Invertebrate Pathology 46, 153159.CrossRefGoogle Scholar
Barus, V. (1964). Freshwater snails as reservoir hosts of invasive larvae of the nematode Syngamus trachea (Montagu 1811). In Parasitic Worms and Aquatic Conditions (ed. Ergens, R. and Rysavy, B.), pp. 8390. Czechoslovak Academy of Sciences, Prague, Czech Republic.Google Scholar
Barus, V. and Blazek, K. (1971). The life cycle and the pathogenicity of the nematode Crenosoma striatum. Folia Parasitologica 18, 215225.Google Scholar
Bathon, H. (1996). Impact of entomopathogenic nematodes on non-target hosts. Biocontrol Science & Technology 6, 421434.CrossRefGoogle Scholar
Boev, S. N. (1975). Protostrongylids. Fundamentals of Nematology 25, Academy of Science of the USSR. (Translated by Amerind Publishing Co., New Delhi, 1984).Google Scholar
Bolt, G., Monrad, J., Frandsen, F., Henriksen, P. and Dietz, H. H. (1993). The common frog (Rana temporaria) as a potential paratenic and intermediate host for Angiostrongylus vasorum. Parasitology Research 79, 428430.CrossRefGoogle ScholarPubMed
Boray, J. C. (1969). Experimental fascioliasis in Australia. Advances in Parasitology 7, 95210.CrossRefGoogle ScholarPubMed
Boray, J. C. (1973). The role of the relative susceptibility of snails to infection with helminths and of the adaptation of the parasites in the epidemiology of some helminthic diseases. Malacologia 14, 125127.Google ScholarPubMed
Boycott, A. E. (1934). The habitats of land mollusca in Britain. Journal of Ecology 22, 138.CrossRefGoogle Scholar
Brockelman, C. R. (1978). Effects of parasitism and stress in hemolymph protein of the African giant snail, Achatina fulica. Zeitschrift für Parasitenkunde 57, 137144.CrossRefGoogle ScholarPubMed
Brockelman, C. R. and Sithithavorn, P. (1980). Carbohydrate reserves and hemolymph sugars of the African giant snail, Achatina fulica in relation to parasitic infection and starvation. Zeitschrift für Parasitenkunde 62, 285291.CrossRefGoogle ScholarPubMed
Brooks, D. R. and Hoberg, E. P. (2007). How will global climate change affect parasite-host assemblages. Trends in Parasitology 23, 571574.CrossRefGoogle ScholarPubMed
Brown, F. M., Mohareb, E. W., Yousif, Y., Sultan, Y. and Girgis, N. I. (1996). Angiostrongylus eosinophilic meningitis in Egypt. The Lancet 348, 964965.CrossRefGoogle ScholarPubMed
Brunetti, O. A. (1969). Redescription of Parelaphostrongylus (Boev & Schuls, 1950) in California deer, with studies on its life history and pathology. California Fish & Game 55, 307316.Google Scholar
Cabaret, J. (1987). Age susceptibility of molluscan intermediate hosts to protostrongylid nematodes. Journal of Parasitology 73, 857858.CrossRefGoogle ScholarPubMed
Cabaret, J., Risye Riseani, S. and Baeza, E. (1991). Survival of sheep and goat first stage protostrongylid larvae in experimental conditions: influence of humidity and temperature. Journal of Helminthology 65, 201207.CrossRefGoogle ScholarPubMed
Cheng, T. C. (1966). Perivascular leucocytosis and other types of cellular reactions in the oyster Crassostrea virginica experimentally infected with the nematode Angiostrongylus cantonensis. Journal of Invertebrate Pathology 8, 5258.CrossRefGoogle ScholarPubMed
Cheng, T. C. (1967). Marine molluscs as hosts for symbioses, with a review of known parasites of commercially important species. Advance in Marine Biology 5, 1424.Google Scholar
Cheng, T. C. and Burton, R. W. (1965). The American oyster and clam as experimental intermediate hosts of Angiostrongylus cantonensis. Journal of Parasitology 51, 296.CrossRefGoogle Scholar
Clark, W. C. (1994). Origins of the parasitic habit in the nematoda. International Journal for Parasitology 24, 11171129.CrossRefGoogle ScholarPubMed
Croll, N. A. (1975). Behavioural analysis of nematode movement. Advances in Parasitology 13, 71122.CrossRefGoogle ScholarPubMed
Crook, J. R., Fulton, S. E. and Supanwong, K. (1971). The infectivity of third stage Angiostrongylus cantonensis larvae shed from drowned Achatina fulica snails and the effect of chemical agents on infectivity. Transactions of the Royal Society of Tropical Medicine & Hygiene 65, 602605.CrossRefGoogle ScholarPubMed
Daldorph, P. W. G. and Thomas, J. D. (1991). Snail cadavers as sources of short-chain carboxylic acids to scavenging freshwater invertebrates. Hydrobiologia 209, 133140.CrossRefGoogle Scholar
Davtjan, E. A. (1945). Comparative susceptibility of molluscs to invasion by larvae of nematodes, causative agents of pulmonary helminthoses in sheep and goats. Comptes Rendus (Doklady) de l'Academie des Sciences de l'URSS 46, 8687.Google Scholar
Doby, J. M. and Drozdz, J. (1971). Cycle evolutif de Angiostrongylus (Parastrongylus) dujardini Drozdz et Doby 1970 (Nematoda: Metastrongyloidea). Comptes rendus Hebdomadaires des séances de L'Academie des sciences. Serie D Sciences naturelles 272, 604607.Google Scholar
Dogiel, V. A. (1964). General Parasitology. Oliver & Boyd, Edinburgh, UK.Google Scholar
Domnich, I. F. (1984). [Rauschivingylus asiaticus n.sp. (Nematoda, Filaroididae) from rodents in north-eastern Asia and its life cycle.] Parazitologiya 18, 244247. [In Russian.]Google Scholar
Eckert, J. and Lammler, G. (1972). Angiostrongylose bei Mensch und Tier. Zeitschrift für Parasitenkunde 39, 303322.CrossRefGoogle Scholar
Egorov, Y. G. (1960). The biology of Muellerius capillaris. Trudy Issledovatelskogo Veterinarnogo Instituta 1, 160170 [In Russian, English translation- British Library, National Lending Library translating Programme, RTS 7357].Google Scholar
El-Shazly, A. M., El Hamshary, E. M., El Shewy, K. M., Rifaat, M. M. A. and El Sharkawy, I. M. A. (2002). Incidence of Parastrongylus cantonensis larvae in different fresh water snails in Dakahlia governorate. Journal of the Egyptian Society of Parasitology 32, 579588.Google ScholarPubMed
Faulkner, L. R. and Bolander, W. J. (1966). Occurrence of large nematode populations in irrigation canals of south central Washington. Nematologica 12, 591600.Google Scholar
Faulkner, L. R. and Bolander, W. J. (1970). Acquisition and distribution of nematodes in irrigation waterways of the Columbia basin in eastern Washington. Journal of Nematology 2, 362367.Google ScholarPubMed
Gaugler, R. and Boush, G. M. (1978). Effects of ultraviolet radiation and sunlight on the entomogenous nematode, Neoaplectana carpocapsae. Journal of Invertebrate Pathology 32, 291296.CrossRefGoogle Scholar
Glazer, I., Liran, N. and Steinberger, Y. (1991). A survey of entomopathogenic nematodes (rhabditida) in the Negev desert. Phytoparasitica 19, 291300.CrossRefGoogle Scholar
Georgiev, D. M., Kostadinova, A. and Georgiev, B. B. (2003). Land snails in the transmission of protostrongylids on pastures in southern Bulgaria: variability of infection levels related to environmental factors. Acta Parasitologica 48, 208217.Google Scholar
Gerichter, C. B. (1948). Observations on the life history of lung nematodes using snails as intermediate hosts. American Journal of Veterinary Research 9, 109112.Google Scholar
Green, P., Dussart, G. B. J. and Gibson, C. (1992). Surfacing and water leaving behaviour of the freshwater pulmonate snails Lymnaea peregra (Muller), Biomphalaria glabrata (Say) and Bulinus jousseaumei (Dautzenberg). Journal of Molluscan Studies 58, 169179.CrossRefGoogle Scholar
Grewal, S. K. and Grewal, P. S. (2003). Effect of osmotic desiccation on longevity and temperature tolerance of Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae). Journal of Parasitology 89, 434438.CrossRefGoogle ScholarPubMed
Grewal, P. S., Wang, X. and Taylor, R. A. J. (2002). Dauer juvenile longevity and stress tolerance in natural populations of entomopathogenic nematodes: is there a relationship? International Journal for Parasitology 32, 717725.CrossRefGoogle ScholarPubMed
Grewal, P. S., Grewal, S. K., Tan, L. and Adams, B. J. (2003). Parasitism of molluscs by nematodes: Types of associations and evolutionary trends. Journal of Nematology 35, 146156.Google ScholarPubMed
Guilhon, J. and de Gaalon, A. (1969). Evolution larvaire d'un nematode parasite de l'appareil circulatoire du chien dans l'organisme de mollusques dulçaquicoles. Compte Rendu Hebdomadaire des Seances de l'Academie des Sciences Serie D, 268, 612615.Google Scholar
Harris, K. R. and Cheng, T. C. (1975 a). The encapsulation process in Biomphalaria glabrata experimentally infected with the metastrongylid Angiostrongylus cantonensis: light microscopy. International Journal for Parasitology 5, 521528.CrossRefGoogle ScholarPubMed
Harris, K. R. and Cheng, T. C. (1975 b). The encapsulation process in Biomphalaria glabrata experimentally infected with the metastrongylid Angiostrongylus cantonensis: enzyme histochemistry. Journal of Invertebrate Pathology 26, 367374.CrossRefGoogle ScholarPubMed
Hernan-Camacho, V. and Camacho, V. H. (1987). Helisoma trivolvis: huesped intermediario de Angiostrongylus costaricensis. Brenesia 27, 7579.Google Scholar
Heyneman, D. and Lim, B.-L. (1967). Angiostrongylus cantonensis: proof of direct transmission with its epidemiological implications. Science 158, 10571058.CrossRefGoogle ScholarPubMed
Hoberg, E. P., Polley, L., Jenkins, E. J. and Kutz, S. J. (2008). Pathogens of domestic and free-ranging ungulates: global climate change in temperate to boreal latitudes across North America. OIE Revue de Scientifique et Technique 27, 511528.CrossRefGoogle ScholarPubMed
Horsak, M. and Cernohorsky, N. (2008). Mollusc diversity patterns in Central European fens: hotspots and conservation priorities. Journal of Biogeography 35, 12151225.CrossRefGoogle Scholar
Hourdin, P., Rondelaud, D. and Cabaret, J. (1990). Evolution of tissue lesions in Lymnaea truncatula infected by Muellerius capillaris and by Neostrongylus linearis (Nematoda: Protostrongylidae). Annales de Parasitologie Humaine et Comparée 65, 249254.CrossRefGoogle Scholar
Hourdin, P., Rondelaud, D. and Cabaret, J. (1991). Initial studies on infection of Lymnaea truncatula Muller by Muellerius capillaris Muller and Neostrongylus linearis Marotel (Nematoda: Protostrongylidae). Parasitology Research 77, 273274.CrossRefGoogle Scholar
Ibrahim, M. M. (2007). Prevalence and intensity of Angiostrongylus cantonensis in freshwater snails in relation to some ecological and biological factors. Parasite 14, 6170.CrossRefGoogle ScholarPubMed
IOM (2008). Global Climate Change and Extreme Weather Events: Understanding the Contributions to Infectious Disease Emergence. Washington DC: The National Academies Press, USA.Google Scholar
Ishii, A. I. (1984). Effects of temperature on the larval development of Angiostrongylus cantonensis in the intermediate host, Biomphalaria glabrata. Zeitschrift für Parasitenkunde 70, 375379.CrossRefGoogle ScholarPubMed
Jenkins, E. J., Veitch, A. M., Kutz, S. J., Hoberg, E. P. and Polley, L. (2006). Climate change and the epidemiology of protostrongylid nematodes in northern ecosystems: Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall's sheep (Ovis d. dalli). Parasitology 132, 387401.CrossRefGoogle ScholarPubMed
Kamiya, M., Oku, Y. and Katakura, K. (1980). Report on the prevalence and experimental infections of Angiostrongylus siamensis Ohbayashi, Kamiya et Bhaibulaya, 1979, parasitic in the mesenteric arteries of rodents in Thailand. Japanese Journal of Veterinary Research 28, 114121.Google ScholarPubMed
Kassai, T. (1957). Schnecken als Zwischenwirte der Protostrongyliden. Zeitschrift für Parasitenkunde 18, 519.CrossRefGoogle Scholar
Kates, K. C. (1965). Ecological aspects of helminth transmission in domesticated animals. American Zoologist 5, 95130.CrossRefGoogle ScholarPubMed
Knapp, S. E. and Alicata, J. E. (1967). Failure of certain clams and oysters to serve as intermediate hosts for Angiostrongylus cantonensis. Proceedings of the Helminthological Society of Washington 34, 13.Google Scholar
Kocan, A. A. (1972). Some common North American aquatic snails as experimental hosts of Angiostrongylus cantonensis- with special reference to Lymnaea palustris. Journal of Parasitology 58, 186187.CrossRefGoogle Scholar
Kontrimavichus, V. L. and Delyamure, S. L. (1979). Filaroids of Domestic and Wild Animals. Fundamentals of Nematology 29. Academy of Science of the USSR. (Translated by Amerind Publishing Co., New Delhi, India, 1985).Google Scholar
Kontrimavichus, V. L., Delyamure, S. L. and Boev, S. N. (1976). Metastrongyloids of Domestic and Wild Animals. Fundamentals of Nematology 26, Academy of Science of the USSR. (Translated by Amerind Publishing Co., New Delhi, India, 1985).Google Scholar
Kralka, R. A. and Samuel, W. M. (1984). Emergence of larval Protostrongylus boughtoni (Nematoda: Metastrongyloidea) from a snail intermediate host, and subsequent infection in the domestic rabbit (Oryctolagus cuniculus). Journal of Parasitology 70, 457458.CrossRefGoogle ScholarPubMed
Kutz, S. J., Hoberg, E. P. and Polley, L. (2000). Emergence of third-stage larvae of Umingmakstrongylus pallikuukensiss from three gastropod intermediate host species. Journal of Parasitology 86, 743749.CrossRefGoogle ScholarPubMed
Kutz, S. J., Hoberg, E. P. and Polley, L. (2001). A new lungworm in muskoxen: an exploration in Arctic parasitology. Trends in Parasitology 17, 276280.CrossRefGoogle ScholarPubMed
Kutz, S. J., Hoberg, E. P., Polley, L. and Jenkins, E. J. (2005). Global warming is changing the dynamics of Arctic host-parasite systems. Proceedings of the Royal Society of London, B 272, 25712576.Google ScholarPubMed
Lai, C.-H., Yen, C.-M., Chin, C., Chung, H.-C., Kuo, H.-C. and Lin, H.-H. (2007). Eosinophilic meningitis caused by Angiostrongylus cantonensis after ingestion of raw frogs. American Journal of Tropical Medicine & Hygiene 76, 399402.CrossRefGoogle ScholarPubMed
Lammler, G. and Saupe, E. (1968). Infektionsversuche mit dem Lungenwurm des Igels, Crenosoma striatum (Zeder, 1800). Zeitschrift für Parasitenkunde 31, 87100.CrossRefGoogle Scholar
Langford, G. J. and Janovy, J. Jr. (2009). Comparative life cycles and life histories of North American Rhabdias spp. (Nematoda: Rhabdiasidae): Lungworms from snakes and anurans. Journal of Parasitology 95, 11451155.CrossRefGoogle ScholarPubMed
Lapage, G. (1961). A list of the parasitic protozoa, helminths and arthropods recorded from species of the family Anatidae (Ducks, Geese and Swans). Parasitology 51, 1109.CrossRefGoogle ScholarPubMed
Lewis, E. E., Delvan, S., Campbell, J. F. and Gaugler, R. (1995). Changes in foraging behaviour during the infective stage of entomopathogenic nematodes. Parasitology 110, 583590.CrossRefGoogle Scholar
Li, P. S., Deng, C. S., Zhang, S. G. and Yang, H. W. (1986). Preliminary tests on Steinernema glaseri infecting the snail, Oncomelania hupensis, an intermediate host of Schistosoma japonica. Chinese Journal of Biological Control 2, 5052.Google Scholar
Liat, L. B., Fong, Y. L. and Krishnansamy, M. (1977). Studies of Angiostrongylus malaysiensis (Nematoda, Metastrongylidae) in peninsular Malaysia: Natural infection in freshwater snails and rodents in ricefields and infectivity experiments. Southeast Asian Journal of Tropical Medicine & Public Health 8, 2735.Google ScholarPubMed
Lim, B. L. and Ramachandran, C. P. (1979). Ecological studies on Angiostrongylus malaysiensis (Nematoda: Metastrongylidae) in Malaysia. In Studies on Angiostrongyliasis in Eastern Asia and Australia (ed. Cross, J. H.), pp. 2648. Special Publication No. 2 (NAMRU-2-SP-44), Taipei: US Naval Medical Research Unit.Google Scholar
Lima, L. C., Massara, C. L., de Souza, C. P., Vidigal, T. D., Lenzi, H. L. and Carvalho, O. S. (1992). Suscetibilidade de planorbideos da regiao metropolitana de Belo Horizonte, MG (Brasil) ao Angiostrongylus costaricensis (Nematoda, Angiostrongylidae). Revista do Instituto de Medicina Tropical de Sao Paulo 34, 399402.CrossRefGoogle Scholar
Lorentzen, G. and Halvorsen, O. (1986). Survival of the first stage larva of the metastrongyloid nematode Elaphostrongylus rangiferi under various conditions of temperature and humidity. Holarctic Ecology 9, 301304.Google Scholar
Lv, S., Zhang, Y., Steinmann, P. and Zhou, X.-N. (2008). Emerging Angiostrongyliasis in Mainland China. Emerging Infectious Diseases 14, 161164.CrossRefGoogle ScholarPubMed
Lv, S., Zhou, X.-N., Zhang, Y., Liu, H.-X., Zhu, D., Yin, W.-G., Steinmann, P., Wang, X.-H. and Jia, T.-W. (2006). The effect of temperature on the development of Angiostrongylus cantonensis (Chen, 1935) in Pomacea canaliculata (Lamarck, 1822). Parasitology Research 99, 583587.CrossRefGoogle ScholarPubMed
Malvy, D., Ezzedine, K., Receveur, M.-C., Pistone, T., Crevon, L., Lemardeley, P., and Josse, R. (2008). Cluster of esinophilic meningitis attributable to Angiostrongylus cantonensis infection in French policemen troop returning from the Pacific Islands. Tropical Medicine & Infectious Disease 6, 301304.CrossRefGoogle Scholar
Mas-Coma, S., Valero, M. A., and Bargues, M. D. (2008). Effects of climate change on animal and zoonotic helminthiases. OIE Revue de Scientifique et Technique 27, 443452.CrossRefGoogle ScholarPubMed
Mitskevich, V. Y. (1964). [Life-cycle of Elaphostrongylus rangiferi Mitskeyich, 1958.]. Parasites of Farm Animals in Kazakhstan 3, 4960. [In Russian]Google Scholar
Monge, E., Arroyo, R. and Solano, E. (1978). A new definitive natural host of Angiostrongylus costaricensis (Morera & Cespedes 1971). Journal of Parasitology 64, 34.CrossRefGoogle ScholarPubMed
Morand, S. and Guegan, J.-F. (2008). How the biodiversity sciences may aid biological tools and ecological engineering to assess the impact of climatic changes. OIE Revue Scientifique et Technique 27, 355366.CrossRefGoogle ScholarPubMed
Morand, S., Wilson, M. J. and Glen, D. M. (2004). Nematodes (Nematoda) parasitic in terrestrial gastropods. In Natural Enemies of Terrestrial Molluscs (ed. Barker, G. M.), pp. 525557. CABI International, Wallingford, UK.CrossRefGoogle Scholar
Morgan, E. R., Jefferies, R., Krajewski, M., Ward, P. and Shaw, S. E. (2009). Canine pulmonary angiostrongylosis: The influence of climate on parasite distribution. Parasitology International 58, 406410.CrossRefGoogle ScholarPubMed
Morley, N. J. and Lewis, J. W. (2008). The influence of climatic conditions on long term changes in the helminth fauna of terrestrial molluscs and the implications for parasite transmission in southern England. Journal of Helminthology 82, 325335.CrossRefGoogle ScholarPubMed
Morley, N. J. and Morritt, D. (2006). The effects of the slug biological control agent, Phasmarhabditis hermaphrodita (Nematoda), on non-target aquatic molluscs. Journal of Invertebrate Pathology 92, 112114.CrossRefGoogle ScholarPubMed
Mott, J. B. and Harrison, A. D. (1983). Nematodes from river drift and surface water supplies in southern Ontario. Hydrobiologia 102, 2738.CrossRefGoogle Scholar
Noda, S. and Sato, A. (1990). Effects of infection with Angiostrongylus cantonensis on the circulating haemocyte population and the haematopoietic organ of the host snail M-line Biomphalaria glabrata. Journal of Helminthology 64, 239247.CrossRefGoogle ScholarPubMed
Noda, S., Matayoshi, S., Uchikawa, R. and Sata, A. (1985). Acquisition of Angiostrongylus cantonensis infection in Achatina fulica under natural field conditions and localization of Angiostrongylus cantonensis third stage larvae in Achatina fulica and Laevicaulis alte. Japanese Journal of Parasitology 34, 457463. [In Japanese.]Google Scholar
O'Roke, E. C. and Cheatum, E. L. (1950). Experimental transmission of the deer lungworm Leptostrongylus alpenae. Cornell Veterinarian 40, 315323.Google ScholarPubMed
Peake, J. (1978). Distribution and ecology of Stylommatophora. In Pulmonates Vol. 2A (ed. Fretter, V. and Peake, J.), pp. 429526. Academic Press, London, UK.Google Scholar
Petter, A. J. (1974). Le cycle evolutif de Morestrongylus andersoni (Petter 1972). Annales de Parasitologie Humaine et Comparée 49, 6982.CrossRefGoogle Scholar
Plum, N. (2005). Terrestrial invertebrates in flooded grassland: a literature review. Wetlands 25, 721737.CrossRefGoogle Scholar
Poinar, G. O. (1989). Non-insect hosts for the entomogenous rhabditoid nematodes Neoaplectana (Steinernematidae) and Heterorhabditis (Heterorhabditidae). Revue de Nematologie 12, 423428.Google Scholar
Poulin, R. (2005). Relative infection levels and taxonomic distances among the host species used by a parasite: insights into parasite specialization. Parasitology 130, 109115.CrossRefGoogle ScholarPubMed
Rachford, F. W. (1975). Potential intermediate and paratenic hosts for Angiostrongylus cantonensis. Journal of Parasitology 61, 11171119.CrossRefGoogle ScholarPubMed
Rachford, F. W. (1976 a). Host parasite relationship of Angiostrongylus cantonensis in Lymnaea palustris. I. Intramolluscan larval growth and development. Experimental Parasitology 39, 377381.CrossRefGoogle Scholar
Rachford, F. W. (1976 b). Host parasite relationship of Angiostrongylus cantonensis in Lymnaea palustris. II. Histopathology. Experimental Parasitology 39, 382392.CrossRefGoogle ScholarPubMed
Rachford, F. W. (1976 c). Host parasite relationship of Angiostrongylus cantonensis in Lymnaea palustris. III. Oxygen uptake of Lymnaea palustris. Experimental Parasitology 39, 393400.CrossRefGoogle ScholarPubMed
Rae, R. G., Robertson, J. F. and Wilson, M. J. (2008). Susceptibility and immune response of Deroceras reticulatum, Milax gagates and Limax pseudoflavus exposed to the slug parasitic nematode Phasmarhabditis hermaphrodita. Journal of Invertebrate Pathology 97, 6169.CrossRefGoogle Scholar
Rae, R., Verdun, C., Grewal, P. S., Robertson, J. F. and Wilson, M. J. (2007). Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita–progress and prospects. Pest Management Science 63, 11531164.CrossRefGoogle ScholarPubMed
Ratanarat-Brockelman, C. (1975). Inhibition of Rhabditis maupasi (Rhabditidae: Nematoda) maturation and reproduction by factors from the snail host, Helix aspersa. Journal of Invertebrate Pathology 25, 229237.CrossRefGoogle ScholarPubMed
Ratanarat-Brockelman, C. (1977). Isolation of nematode inhibitor from hemolymph of the snail, Helix aspersa. Biological Bulletin 152, 406414.CrossRefGoogle ScholarPubMed
Rezac, P. (1991). Preliminary observation of the susceptibility of some freshwater snails to the infection with Varestrongylus sagittatus (Nematoda: Protostrongylidae). Folia Parasitologica 38, 375378.Google Scholar
Richards, C. S. (1967). Estivation of Biomphalaria glabrata (Basommatophora: Planorbidae): associated characteristics and relation to infection with Schistosoma mansoni. American Journal of Tropical Medicine & Hygiene 16, 797802.CrossRefGoogle ScholarPubMed
Richards, C. S. and Merritt, J. W. (1967). Studies on Angiostrongylus cantonensis in molluscan intermediate hosts. Journal of Parasitology 53, 382388.CrossRefGoogle ScholarPubMed
Rose, J. H. (1957). Observations on the larval stages of Muellerius capillaris within the intermediate hosts Agriolimax agrestis and A. reticulates. Journal of Helminthology 31, 116.CrossRefGoogle Scholar
Rosen, L., Loison, G., Laigret, J. and Wallace, G. D. (1967). Studies on eosinophilic meningitis. 3. Epidemiologic and clinical observations on Pacific islands and the possible etiologic role of Angiostrongylus cantonensis. American Journal of Epidemiology 85, 1744.CrossRefGoogle ScholarPubMed
Schjetlein, J. and Skorping, A. (1995). The temperature threshold for development of Elaphostrongylus rangiferi in the intermediate host: an adaptation to winter survival? Parasitology 111, 103110.CrossRefGoogle ScholarPubMed
Shiota, T., Arizono, N., Yamada, M., Kurimoto, H., Shimada, Y. and Yoshida, Y. (1980). [Experimental infections with 13 species of Japanese freshwater mollusks with Angiostrongylus cantonensis larvae.]. Japanese Journal of Parasitology 29, 2738. [In Japanese.]Google Scholar
Shostak, A. W. and Samuel, W. M. (1984). Moisture and temperature effects on survival and infectivity of first-stage larvae of Parelaphostrongylus odocoilei and P. tenuis (Nematoda: Metastrongyloidea). Journal of Parasitology 70, 261269.CrossRefGoogle ScholarPubMed
Skorping, A. (1982). Elaphostrongylus rangiferi: Influence of temperature, substrate, and larval age on the infection rate in the intermediate snail host, Aarianta arbustorum. Experimental Parasitology 54, 222228.CrossRefGoogle ScholarPubMed
Skorping, A. (1985). Lymnea stagnalis as experimental intermediate host for the protostrongylid nematode Elaphostrongylus rangiferi. Zeitschrift für Parasitenkunde 71, 265270.CrossRefGoogle Scholar
Solomon, A., Paperna, I. and Alkon, P. U. (1996 a). The suitability of Trochoidea seetzenii of different ages as snail intermediate hosts of Muellerius cf. capillaris (Nematoda: Protostrongylidae). International Journal for Parasitology 26, 13171319.CrossRefGoogle ScholarPubMed
Solomon, A., Paperna, I. and Markovics, A. (1996 b). The influence of aestivation in land snails on the larval development of Muellerius capillaris (Metastrongyloidea: Protostrongylidae). International Journal for Parasitology 26, 363367.CrossRefGoogle ScholarPubMed
Sprent, J. F. A. (1963). The life history and development of Amplicaecum robertsi, an ascaridoid nematode of the carpet python (Morelia spilotes variegatus). II. Growth and host specificity of larval stages in relation to the food chain. Parasitology 53, 321337.CrossRefGoogle Scholar
Stewart, G. L., Ubelaker, J. E. and Curtis, D. (1985). Pathophysiologic alterations in Biomphalaria glabrata infected with Angiostrongylus costaricensis. Journal of Invertebrate Pathology 45, 152157.CrossRefGoogle ScholarPubMed
Sullivan, J. T., Ratanapitaksa, S. and Palmieri, J. R. (1978). Comparative host reaction to Angiostrongylus malaysiensis (Nematoda) in three species of snails. Journal of Invertebrate Pathology 32, 359367.CrossRefGoogle Scholar
Svarc, R. and Zmoray, I. (1974). The development of Muellerius tenuispiculatus Gebauer, 1932 in the intermediate host under experimental conditions. II. Localization of the larval stages of M. tenuispiculatus during maturation in the intermediate host. Biologia (Bratislava) 29, 121127.Google Scholar
Szmidt-Adjide, V., Rondelaud, D., Dreyfuss, G. and Cabaret, J. (1996). The effect of parasitism by Fasciola hepatica and Muellerius capillaris on the nerve ganglia of Lymnaea truncatula, Journal of Invertebrate Pathology 67, 300305.CrossRefGoogle ScholarPubMed
Tesana, S., Srisawangwong, T., Sithithaworn, P., Laha, T. and Andrews, R. (2009). Prevalence and intensity of infection with third stage larvae of Angiostrongylus cantonensis in molluscs from Northeast Thailand. American Journal of Tropical Medicine & Hygiene 80, 983987.CrossRefGoogle ScholarPubMed
Thobois, S., Broussolle, E., Aimard, G. and Chazot, G. (1996). L'ingestion du poisson cru: une cause de méningite à éosinophile due à Angiostrongylus cantonensis après un voyage à Tahiti. Presse Médicale 25, 508.Google Scholar
Thurston, G. S., Ni, Y. and Kaya, H. K. (1994). Influence of salinity on survival and infectivity of entomopathogenic nematodes. Journal of Nematology 26, 345351.Google ScholarPubMed
Trushin, I. N. (1976). [Fresh-water snails in the life-cycle of Muellerius capillaris.]. Byulleten Vsesoyuznogo Instituta Gel'mintologii im K.I. Skryabina 18, 9095. [In Russian.]Google Scholar
Ubelaker, J. E., Caruso, J. and Pena, A. (1981). Experimental infection of Sigmodon hispidus with third stage larvae of Angiostrongylus costaricensis. Journal of Parasitology 67, 219221.CrossRefGoogle ScholarPubMed
Urban, E. (1980). Studies on lung nematodes (Protostrongylidae, Dictyocaulidae) in sheep of the Podhale region, Tatra highlands. II. Intermediate hosts of Protostrongylidae. Acta Parasitologica Polonica 27, 6374.Google Scholar
Van Dijk, J., Louw, M. D. E., Kalis, L. P. A. and Morgan, E. R. (2009). Ultraviolet light increases mortality of nematode larvae and can explain patterns of larval availability at pasture. International Journal for Parasitology 39, 11511156.CrossRefGoogle ScholarPubMed
Wallace, G. D. and Rosen, L. (1966). Studies on eosinophilic meningitis. 2. Experimental infection of shrimp and crabs with Angiostrongylus cantonensis. American Journal of Epidemiology 84, 120131.CrossRefGoogle ScholarPubMed
Wallace, G. D. and Rosen, L. (1967). Studies on eosinophilic meningitis. 4. Experimental infection of fresh-water and marine fish with Angiostrongylus cantonensis. American Journal of Epidemiology 85, 395402.CrossRefGoogle Scholar
Wallace, G. D. and Rosen, L. (1970). Maintenance of two feline lungworms in aquatic snails (Biomphalaria glabrata). American Journal of Veterinary Research 31, 809810.Google ScholarPubMed
Wang, L.-C., Chao, D. and Chen, E.-R. (1991). Experimental infection routes of Angiostrongylus cantonensis in mice. Journal of Helminthology 65, 296300.CrossRefGoogle ScholarPubMed
Webbe, G. (1971). The significance of infra-specific variations of hosts and parasites in the epidemiology of helminths of medical importance. Journal of Helminthology 65, 327335.CrossRefGoogle Scholar
Witoonpanich, R., Chuahirun, S., Soranastaporn, S. and Rojanasunan, P. (1991). Eosinophilic myelomeningoencephalitis caused by Angiostrongylus cantonensis: a report of three cases. Southeast Asian Journal of Tropical Medicine & Public Health 22, 262267.Google ScholarPubMed
Yen, C.-M., Chen, E.-R. and Cheng, C.-W. (1990). A survey of Ampullarium canaliculatus for natural infection of Angiostrongylus cantonensis in south Taiwan. Journal of Tropical Medicine & Hygiene 93, 347350.Google ScholarPubMed
Yousif, F., Blahser, S. and Lammler, G. (1980). The cellular responses in Marisa cornuarietis experimentally infected with Angiostrongylus cantonensis. Zeitschrift für Parasitenkunde 62, 179190.CrossRefGoogle Scholar
Yousif, F. and Ibrahim, A. (1978). The first record of Angiostrongylus cantonensis from Egypt. Zeitschrift für Parasitenkunde 56, 7380.CrossRefGoogle ScholarPubMed
Yousif, F. and Lammler, G. (1975 a). The effect of some biological and physical factors on infection of Biomphalaria glabrata with Angiostrongylus cantonensis. Zeitschrift für Parasitenkunde 47, 191201.CrossRefGoogle ScholarPubMed
Yousif, F. and Lammler, G. (1975 b). The suitability of several aquatic snails as intermediate hosts for Angiostrongylus cantonensis. Zeitschrift für Parasitenkunde 47, 203210.CrossRefGoogle ScholarPubMed
Yousif, F. and Lammler, G. (1977). The mode of infection with and distribution of Angiostrongylus cantonensis larvae in the experimental intermediate host Biomphalaria glabrata. Zeitschrift für Parasitenkunde 53, 247250.CrossRefGoogle Scholar
Zdzitowiecki, K. (1976). An experimental study on the infection of terrestrial and aquatic snails with Muellerius capillaris (Mueller, 1889) larvae (Nematoda, Protostrongylidae). Acta Parasitologica Polonica 24, 159163.Google Scholar