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Chemotactic behaviour of Strongyloides stercoralis infective larvae on a sodium chloride gradient

Published online by Cambridge University Press:  09 October 2003

W. M. FORBES
Affiliation:
Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, PA 19104, USA
F. T. ASHTON
Affiliation:
Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, PA 19104, USA
R. BOSTON
Affiliation:
Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, 382 West Street Road, Kennett Square, PA 19348, USA
G. A. SCHAD
Affiliation:
Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, PA 19104, USA

Abstract

Chemotactic responses of Strongyloides stercoralis infective larvae (L3) to sodium chloride (NaCl) were investigated by recording larval tracks on a saline gradient in agarose. On agarose, larvae migrated randomly, whereas when placed at 0·01 M NaCl larvae moved to approximately 1·1 M NaCl where they turned, headed down the gradient and eventually remained circling at a favoured salinity (0·03–0·07 M). Conversely, when placed at 2·85 M NaCl, the L3 larvae moved unidirectionally to lower, more favoured salt concentrations. Here they circled, changing directions frequently while making ‘loop-like’ tracks. Larvae were immobilized within 5 min at salt concentrations exceeding 3 M NaCl. When placed at 0·01 M NaCl, 51·1%±26·9 migrated to 1·1 M NaCl after 2 min, and 80%±18·7 did so after 8 min, at an average velocity of 4·1±1·4 mm/min. Larvae (53·6%±21·6) were repelled from 2·85 M NaCl to lower concentrations after 2 min. After 8 min, 95%±11·1 were repelled, moving at an average velocity of 6·2±1·1 mm/min. Using this bioassay, the influence of neuronal control over chemotactic behaviour of S. stercoralis and other parasitic nematodes can be elucidated.

Type
Research Article
Copyright
2003 Cambridge University Press

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References

REFERENCES

AFRICA, C. M. (1931). Studies on the activity of the infective larvae of the rat strongylid, Nippostrongylus muris. Journal of Parasitology 17, 196206.CrossRefGoogle Scholar
ASHTON, F. T., BHOPALE, V. M., FINE, A. E. & SCHAD, G. A. (1995). Sensory neuroanatomy of a skin-penetrating nematode parasite: Strongyloides stercoralis I. Amphidial neurons. Journal of Comparative Neurology 357, 281295.CrossRefGoogle Scholar
ASHTON, F. T., LI, J. & SCHAD, G. A. (1999). Chemo- and thermosensory neurons: structure and function in animal parasitic nematodes. Journal of Parasitology 84, 691695.CrossRefGoogle Scholar
BARGMANN, C. I. & MORI, I. (1997). Chemotaxis and thermotaxis. In C. elegans II (ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. & Priess, J. R.), pp. 717738. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
BHOPALE, V. M., KUPPRION, E. K., ASHTON, F. T., BOSTON, R. & SCHAD, G. A. (2001). Ancylostoma caninum: The finger cell neurons mediate thermotactic behavior by infective larvae of the dog hookworm. Experimental Parasitology 97, 7076.CrossRefGoogle Scholar
DOBSON, R. L. & SATO, K. (1972). The secretion of salt and water by the eccrine sweat gland. Archives of Dermatology 105, 366370.CrossRefGoogle Scholar
GENTA, R. M., SCHAD, G. A. & HELLMAN, M. E. (1986). Strongyloides stercoralis: parasitological, immunological and pathological observations in immunosuppressed dogs. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 3441.CrossRefGoogle Scholar
GRANZER, M. & HAAS, W. (1991). Host-finding and host recognition of infective Ancylostoma caninum larvae. International Journal for Parasitology 21, 429440.CrossRefGoogle Scholar
GRENOT, C. (2001). Adaptation of small Saharan vertebrates to arid conditions. Bulletin of the Zoological Society of France 126, 129167.Google Scholar
GROVE, D. I. (1989). Strongyloidiasis: a Major Roundworm Infection of Man. Taylor and Francis, London.
HOPE, I. A. (ed.) (1999). Caenorhabditis elegans – A Practical Approach. Oxford University Press, Oxford.
KENNEDY, W. R., SAKUTA, M. & QUICK, D. C. (1984). Rodent eccrine sweat glands: A case of multiple efferent innervation. Neuroscience 11, 741749.CrossRefGoogle Scholar
LI, J., XIAODONG, Z., BOSTON, R., ASHTON, F. T., GAMBLE, H. R. & SCHAD, G. A. (2000). Thermotaxis and thermosensory neurons in infective larvae of Haemonchus contortus, a passively ingested nematode parasite. The Journal of Comparative Neurology 424, 5873.3.0.CO;2-Z>CrossRefGoogle Scholar
MA, R. (1987). Chemoattraction of infective larvae of Ancylostoma braziliense to rodent plasmas and to salts. Acta Biologica Hungarica 61, 130146.Google Scholar
McPHERSON, R. K. (1960). Physiological responses to hot environments. Medical Research Council Special Report Series No. 298. H. M. Stationery, London.
MORI, I. & OHSHIMA, Y. (1995). Neural regulation of thermotaxis in Caenorhabditis elegans. Nature, London 376, 344347.CrossRefGoogle Scholar
PARKER, J. C. & HALEY, A. J. (1960). Phototactic and thermotactic responses of the filariform larvae of the rat nematode Nippostrongylus muris. Experimental Parasitology 9, 9297.CrossRefGoogle Scholar
PATTERSON, M. J., GALLOWAY, S. D. & NIMMO, M. A. (2000). Variations in regional sweat composition in normal human males. Experimental Physiology 85, 869875.CrossRefGoogle Scholar
PYE, A. E. & BURMAN, M. (1981). Neoplectana carpocapsae: nematode accumulation on chemical and bacterial gradients. Experimental Parasitology 51, 1320.CrossRefGoogle Scholar
RIDDLE, D. L. & BIRD, A. F. (1985). Responses of the plant parasitic nematodes Rotylenchulus reniformis, Anguina agrostis and Meloidogyne javanica to chemical attractants. Parasitology 91, 165195.CrossRefGoogle Scholar
SASA, M., SHIRASAKA, R., TANAKA, H., MIURA, A., YAMAMOTO, H. & KATAHIRA, K. (1960). Observation on the behavior of infective larvae of hookworm and related nematode parasites, with notes on the effect of carbon dioxide in the breath as the stimulant. Japanese Journal of Experimental Medicine 30, 433447.Google Scholar
SCHAD, G. A., HELLMAN, M. E. & MUNCEY, D. W. (1984). Strongyloides stercoralis: Hyperinfection in immunosuppressed dogs. Experimental Parasitology 57, 287296.CrossRefGoogle Scholar
SCIACCA, J., FORBES, W. M., ASHTON, F. T., LOMBARDINI, E., GAMBLE, H. R. & SCHAD, G. A. (2002 a). Response to carbon dioxide by the infective larvae of three species of parasitic nematodes. Parasitology International 51, 5362.Google Scholar
SCIACCA, J., KETSCHEK, A., FORBES, W. M., BOSTON, R., GUERRERO, J., ASHTON, F., GAMBLE, H. R. & SCHAD, G. A. (2002 b). Vertical migration by the infective larvae of three species of parasitic nematodes: Is the behavior really a response to gravity? Parasitology 125, 18.Google Scholar
TADA, I., KOGA, M., HAMANO, S., HIGO, H. & TANAKA, K. (1997). Strongyloides ratti: Accumulating behavior of the third stage larvae to sodium ion. Japanese Journal of Nematology 27, 2229.CrossRefGoogle Scholar
TOBATA-KUDO, H., HIGO, H., KOGA, M. & TADA, I. (2000 a). Chemokinetic behavior of the infective third-stage larvae of Strongyloides ratti on a sodium chloride gradient. Parasitology International 49, 183188.Google Scholar
TOBATA-KUDO, H., HIGO, H., KOGA, M. & TADA, I. (2000 b). Effects of various treatments on the chemokinetic behavior of third-stage larvae of Strongyloides ratti on a sodium chloride gradient. Parasitology Research 86, 865869.Google Scholar
WARD, S. (1973). Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by the use of mutants. Proceedings of the National Academy of Sciences, USA 70, 817821.CrossRefGoogle Scholar
WARD, S., THOMSON, N., WHITE, J. G. & BRENNER, S. (1975). Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. Journal of Comparative Neurology 160, 313338.CrossRefGoogle Scholar
ZUCKERMAN, B. & JANSSON, H. B. (1984). Nematode chemotaxis and possible mechanisms of host/prey recognition. Annual Review of Phytopathology 22, 95113.CrossRefGoogle Scholar