Abstract
Current knowledge of the involvement of chemical stimuli in the reproductive and ingestive physiology of zooparasitic nematodes is reviewed. The habitat of zooparasitic nematodes, coupled with their sensory reduction, indicates that chemical stimuli may modulate most aspects of their behavioral physiology. Nematodes respond to the feeding status of the host so that the helminth's pharyngeal pumping, site selection, and sexual activity may be altered. Biogenic amines from the host, such as histamine, dopamine, or serotonin, may synchronize host and helminth ingestion. Octopamine, which is released by nematodes, depresses ingestion by male, but not female, worms. Biogenic amines may also regulate ovipositioning by female helminths. Nematodes release pheromones that enable precopulatory location of a mate. The male helminth is activated by both components of the female's pheromone while movement by the female is probably arrested by male-produced chemicals. Continuation of spectral analyses may allow future identification of female pheromone. The male's pheromone receptor binds lectin that is specific for mannose residues. Host immunity also alters the behavior of nematodes. Ingestion by nematodes is depressed by serum, particularly IgG1, from infected animals. Similar results occur after immunization of noninfected hosts. Immune serum has no effect on pheromone communication between the sexes of helminth, but depresses ovipositional behavior of female worms. Exploitation of these chemical signals and the helminths' responses may allow novel techniques for disease control.
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References
Alphey, T.J.W. 1983. Effect of nutritional stress on control ofLongiodorus elongatus by nematocidal chemicals.Ann. Appl. Biol. 103:131–138.
Ballantyne, A.J., Sharpe, M.J., andLee, D.L. 1978. Changes in the adenylate energy charge ofNippostrongylus brasiliensis andNematodirus battus during the development of immunity to these nematodes in their hosts.Parasitology 76:211–220.
Belosevic, M., andDick, T.A. 1980. Chemical attraction in the genusTrichinella.J. Parasitol. 66:88–93.
Bone, L.W. 1982. Reproductive chemical communication of helminths. II. Aschelminthes.Int. J. Invert. Reprod. 5:311–321.
Bone, L.W., andBottjer, K.P. 1984. Characterization of and male adaptation to pheromone of femaleTrichostrongylus colubriformis (Nematoda).J. Chem. Ecol. 10:1749–1758.
Bone, L.W., andBottjer, K.P. 1985a. Stimulation of ingestion inTrichostrongylus colubriformis (Nematoda).Proc. Helminthol. Soc. Wash. 52:80–84.
Bone, L.W., andBottjer, K.P. 1985b. Cuticular carbohydrates of three nematode species and chemoreception byTrichostrongylus colubriformis.J. Parasitol. 71:235–238.
Bone, L.W., andShorey, H.H. 1977. Disruption of sex pheromone communication in a nematode.Science 197:694–695.
Bone, L.W., andShorey, H.H. 1978. Nematode sex pheromones.J. Chem. Ecol. 4:595–612.
Bone, L.W., Markiw, A., andBottjer, K.P. 1985. Feeding ofNippostrongylus brasiliensis in oxygen and serum.J. Parasitol. 71:126–128.
Bottjer, K.P., andBone, L.W. 1984. Ingestion of dye by the sexes ofTrichostrongylus colubriformis.J. Parasitol. 70:671–676.
Bottjer, K.P., andBone, L.W. 1985a.Nippostrongylus brasiliensis: In vitro feeding activity.Int. J. Parasitol. 15:15–19.
Bottjer, K.P., andBone, L.W. 1985b.Nippostrongylus brasiliensis: Feeding activity in the mouse.Int. J. Parasitol. 15:9–14.
Bottjer, K.P., andBone, L.W. 1985c. In vitro ingestion byTrichostrongylus colubriformis (Nematoda) in sera, bacteria and media.Proc. Helminthol. Soc. Wash. 53:134–136.
Bottjer, K.P., Klesius, P.H., andBone, L.W. 1986. Effects of host serum on feeding byTrichostrongylus colubriformis (Nematoda).Parasite Immunol. 7:1–9.
Charley-Poulain, J., Luffau, G., andPery, P. 1984. Serum and abomasal antibody response of sheep to infections withHaemonchus contortus.Vet. Parasitol. 14:129–141.
Chen, S.N., andHowells, R.E. 1979. The uptake in vitro of dyes, monosaccharides and amino acids by the filarial wormBrugia pahangi.Parasitology 78:343–354.
Croll, N.A. 1975. Indolealkylamines in the coordination of nematode behavioral activities.Can. J. Zool. 53:894–903.
Croll, N.A. 1977. Sensory mechanisms in nematodes.Annu. Rev. Phytopathol. 15:76–89.
Croll, N.A., andSukhdeo, M.V.K. 1981. Hierarchies in nematode behavior, pp. 227–251,in B.M. Zuckerman and R.A. Rohde (eds.). Plant Parasitic Nematodes, Vol. 3. Academic Press, New York.
Dusenbery, D.B. 1975. The avoidance ofd-tryptophan by the nematodeCaenorhabditis elegans.J. Exp. Zool. 193:413–418.
Fernando, N.A., andWong, H.A. 1964. Metabolism of hookworms. II. Glucose metabolism and glycogen synthesis in adult femaleAncylostoma caninum.Exp. Parasitol. 15:284–292.
Fleming, M.W., andFetterer, R.H. 1984.Ascaris suum: Continuous perfusion of the pseudocoelom and nutrient absorption.Exp. Parasitol. 57:142–148.
Glassburg, G.H., Zalisko, E., andBone, L.W. 1981. In vivo pheromone activity inNippostrongylus brasiliensis (Nematoda).J. Parasitol. 67:898–905.
Glassburg, G.H., Shanahan, T., andBone, L.W. 1983. Behavior of single- and mixed-sex infections ofNippostrongylus brasiliensis in fed and fasted mice.J. Parasitol. 69:883–889.
Honde, C., andBueno, L. 1982.Haemonchus contenus: Egg laying influenced by abomasal pH in lambs.Exp. Parasitol. 54:371–378.
Horvitz, H.R., Chalfie, M., Trent, C., Sulston, J.E., andEvans, P.O. 1982. Serotonin and octopamine in the nematodeCaenorhabditis elegans.Science 216:1012–1014.
Howells, R.E., andChen, S.N. 1981.Brugia pahangi: Feeding and nutrient uptake in vitro and in vivo.Exp. Parasitol. 51:42–58.
Huang, S.P., Tatter, T.A., Rohde, R.A., andZuckerman, B.M. 1982.Caenorhabditis elegans: Effects of 5-hydroxytryptophan and dopamine on behavior and development.Exp. Parasitol. 54:72–79.
Jansson, H.-B., Jeyaprakash, A., Damon, R.A., Jr., andZuckerman, B.M. 1984.Caenorhabditis elegans andPanagrellus redivivus: Enzyme-mediated modification of chemotaxis.Exp. Parasitol. 58:270–277.
Jones, V.E., andOgilvie, B.M. 1972. Protective immunity toNippostrongylus brasiliensis in the rat. III. Modulation of worm acetylcholinesterase by antibodies.Immunology 22:119–129.
Kennedy, M.W., andBruce, R.G. 1981. Reversibility of the effects of the host immune response on the intestinal phase ofTrichinella spiralis in the mouse, following transplantation to a new host.Parasitology 82:39–48.
Lee, D.L. 1969. Changes in adultNippostrongylus brasiliensis during the development of immunity to this nematode in rats. I. Changes in ultrastructure.Parasitology 59:29–39.
Mettrick, W.F., andCho, C.H. 1981. Migration ofHymenolepis diminuta (Cestoda) and changes in 5-HT (serotonin) levels in the rat host following parenteral and oral 5-HT administration.Can. J. Zool. 59:281–286.
Ogilvie, B.M., andHockley, D.J. 1968. Effects of immunity onNippostrongylus brasiliensis adult worms: Reversible and irreversible changes in infectivity, reproduction, and morphology.J. Parasitol. 54:1073–1084.
Phillipson, R.F. 1974. Intermittent egg release byAspiculuris tetraptera in mice.Parasitology 69:207–213.
Pritchard, D.I., Williams, D.J.L., Behuke, J.M., andLee, T.D.G. 1983. The role of IgG1 hypergammaglobulinaemia in immunity to the gastrointestinal nematodeNematospiroides dubius: The immunochemical purification, antigen specificity, and in vivo antiparasite effect of IgG1 from immune serum.Immunology 49:353–365.
Reddington, J.J., Stewart, G.L., Kramar, G.W., andKramer, M.A. 1981. The effects of host sex and hormones onTrichinella spiralis in the mouse.J. Parasitol. 67:548–555.
Roberts, L.W., andFairbairn, W. 1965. Metabolic studies on adultNippostrongylus brasiliensis (Nematoda: Trichostrongyloidea).J. Parasitol. 51:129–138.
Roberts, T.M., andThorson, R.E. 1977. Pairing between adults ofNippostrongylus brasiliensis and other species of nematodes in vitro.J. Parasitol. 63:764–766.
Rothwell, T.L.W., andMerritt, G.C. 1974. Acetylcholinesterase secretion by parasitic nematodes. IV. Antibodies against the enzyme inTrichostrongylus colubriformis infected sheep.Int. J. Parasitol. 4:63–71.
Rothwell, T.L.W., Adams, D.B., Love, R.J., Love, D.N., andMcLaren, D.J. 1980. Immunity againstTrichostrongylus colubriformis infection in guinea pigs and sheep: Some comparisons withNippostrongylus brasiliensis infection in the rat.Int. J. Parasitol. 10:43–49.
Samoiloff, M.R., McNicholl, P., Cheng, P., andBalakanich, S. 1973. Regulation of nematode behavior by physical means.Exp. Parasitol. 33:253–262.
Swanson, J.A., Falvo, R., andBone, L.W. 1984.Nippostrongylus brasiliensis: Effects of testosterone on reproduction and establishment.Int. J. Parasitol. 14:241–247.
Techasoponmani, R., andSirisinha, S. 1980. Use of excretory and secretory products from adult female worms to immunize rats and mice againstAngiostrongylus cantonensis infection.Parasitology 80:457–469.
Wagland, B.M., Steel, J.W., Windon, R.G., andDinun, J.K. 1984. The response of lambs to vaccination and challenge withTrichostrongylus colubriformis: Effect of plane of nutrition on, and the interrelationship between, immunological responsiveness and resistance.Int. J. Parasitol. 14:39–44.
Ward, S. 1973. Chemotaxis by the nematodeCaenorhabditis elegans: Identification of attractants and analysis of the response by use of mutants.Proc. Natl. Acad. Sci. U.S.A. 70:817–821.
Ward, J.B., andBone, L.W. 1983a.Nippostrongylus brasiliensis: Environmental influences on pheromone production by females.Int. J. Parasitol. 13:499–502.
Ward, J.B., andBone, L.W. 1983b. Chromatography and isolation of the Kav 1.0 pheromone of femaleNippostrongylus brasiliensis (Nematoda).J. Parasitol. 69:302–306.
Wright, K.A. 1983. Nematode chemosensilla: Form and function.J. Nematol. 15:151–158.
Zuckerman, B.M., andJansson, H.-B. 1984. Nematode chemotaxis and possible mechanisms of host/prey recognition.Annu. Rev. Phytopathol. 22:95–113.
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Bone, L.W. Nematode reproductive and ingestive responses to helminth and host chemical stimuli. J Chem Ecol 12, 1641–1650 (1986). https://doi.org/10.1007/BF01022370
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DOI: https://doi.org/10.1007/BF01022370