Hostname: page-component-76fb5796d-25wd4 Total loading time: 0 Render date: 2024-04-25T09:41:40.071Z Has data issue: false hasContentIssue false
  • English
  • Français

Navigation within host tissues: cues for orientation of Diplostomum spathaceum (Trematoda) in fish towards veins, head and eye

Published online by Cambridge University Press:  22 February 2007

W. HAAS ,
C. WULFF ,
K. GRABE ,
V. MEYER  and
S. HAEBERLEIN
W. HAAS*
Affiliation:
Institute for Zoology I, University Erlangen-Nuernberg, Staudtstrasse 5, D-91058 Erlangen, Germany
C. WULFF
Affiliation:
Institute for Zoology I, University Erlangen-Nuernberg, Staudtstrasse 5, D-91058 Erlangen, Germany
K. GRABE
Affiliation:
Institute for Zoology I, University Erlangen-Nuernberg, Staudtstrasse 5, D-91058 Erlangen, Germany
V. MEYER
Affiliation:
Institute for Zoology I, University Erlangen-Nuernberg, Staudtstrasse 5, D-91058 Erlangen, Germany
S. HAEBERLEIN
Affiliation:
Institute for Zoology I, University Erlangen-Nuernberg, Staudtstrasse 5, D-91058 Erlangen, Germany
*
*Corresponding author: Tel: +49 9131 8528064. Fax: +49 9131 8528040. E-mail: whaas@biologie.uni-erlangen.de
Get access Rights & Permissions [Opens in a new window]

Summary

Cercariae of Diplostomum spathaceum penetrate the skin of fish, and then migrate along blood vessels and tissues towards the head and the eye-lens. We studied their orientation behaviour in tail fins of guppies and in chemical concentration gradients within agar-filled choice chambers. In fins, they entered veins and orientated cranially, independent of the blood flow and living cells. In choice chambers, they were attracted by a small molecular fraction of fish serum, D-glucose (at 1, 10, and 1000 μm), D-mannose, D-maltotriose and Cl-ions, whereas D-glucosamine repelled them (even at 1·0 nm). Amino acids were not attractive, but arginine in tetrapeptides attracted at concentrations as low as 1 μm and melatonin at 0·4–4·3 pm. We suggest a preliminary model for the behaviour of diplostomula in fish fins and attracting (+) or repelling (−) host cues: (1) migration towards deeper skin layers and avoidance of skin surface, cues: Cl-ions (+ and −), glucose (+), glucosamine (−), light radiation (−); (2) orientation in cranial direction, cue: Cl-ions (+); (3) localization of blood vessels, cues: glucose (+), arginine-residues (+); (4) localization of the retina, cue: melatonin (+). A comparison with the navigation mechanisms of tissue-migrating schistosomules and hookworm larvae reveals an enormous diversity of strategies.

Keywords

Diplostomum spathaceumcercariadiplostomulumchemotaxisorientation mechanismsparasite behavioursite-findingfish parasite
Type
Research Article
Information
Parasitology , Volume 134 , Issue 7 , July 2007 , pp. 1013 - 1023
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Betterton, C. (1974). Studies on the host specificity of the eyefluke, Diplostomum spathaceum, in brown and rainbow trout. Parasitology 69, 11–29.Google Scholar
Blasco, J., Marimon, I., Viaplana, I. and Fernandez-Borras, J. (2001). Fate of plasma glucose in tissues of brown trout in vivo: effects of fasting and glucose loading. Fish Physiology and Biochemistry 24, 247–258.Google Scholar
Davis, D. J. (1936). Pathological studies on the penetration of the cercariae of the strigeid trematode, Diplostomum flexicaudum. Journal of Parasitology 22, 329–337.Google Scholar
Erasmus, D. A. (1959). Studies on the morphology, biology and development of a strigeid cercaria (Cercaria X Baylis 1930). Parasitology 48, 312–335.Google Scholar
Evans, D. H., Piermarini, P. M. and Choe, K. P. (2005). The multifunctional fish gill: site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews 85, 97–177.Google Scholar
Falcon, J., Gothilf, Y., Coon, S. L., Boeuf, G. and Klein, D. C. (2003). Genetic, temporal and developmental differences between melatonin rhythm generating systems in the teleost fish pineal organ and retina. Journal of Neuroendocrinology 15, 378–382.Google Scholar
Ferguson, M. S. (1943). Migration and localization of an animal parasite within the host. Journal of Experimental Zoology 93, 375–401.Google Scholar
Forward, R. B. and Rittschof, D. (1999). Brine shrimp larval photoresponses involved in diel vertical migration: activation by fish mucus and modified amino sugars. Limnology and Oceanography 44, 1904–1916.Google Scholar
Forward, R. B. and Rittschof, D. (2000). Alteration of photoresponses involved in diel vertical migration of a crab larva by fish mucus and degradation products of mucopolysaccharides. Journal of Experimental Marine Biology and Ecology 254, 277–292.Google Scholar
Grabe, K. and Haas, W. (2004 a). Navigation within host tissues: Schistosoma mansoni and Trichobilharzia ocellata schistosomula respond to chemical gradients. International Journal for Parasitology 34, 927–934.Google Scholar
Grabe, K. and Haas, W. (2004 b). Navigation within host tissues: cercariae orientate towards dark after penetration. Parasitology Research 93, 111–113.Google Scholar
Groff, J. M. and Zinkl, J. G. (1999). Haematology and clinical chemistry of cyprinid fish. Common carp and goldfish. Veterinary Clinics of North America: Exotic Animal Practice 2, 741–776.Google Scholar
Haas, W. (1974 a). Analyse der Invasionsmechanismen der Cercarie von Diplostomum spathaceum. I. Fixation und Penetration. International Journal for Parasitology 4, 311–319.Google Scholar
Haas, W. (1974 b). Analyse der Invasionsmechanismen der Cercarie von Diplostomum spathaceum. II. Chemische Invasionsstimuli. International Journal for Parasitology 4, 321–330.Google Scholar
Haas, W. (1975). Einfluss von CO2 und pH auf das Fixationsverhalten der Cercarie von Diplostomum spathaceum (Trematoda). Zeitschrift für Parasitenkunde 46, 53–60.Google Scholar
Haas, W. (1994). Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109 (Suppl.), S15–S29.Google Scholar
Haas, W. (2003). Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349–364.Google Scholar
Haas, W. and Haberl, B. (1997). Host recognition by trematode miracidia and cercariae. In Advances in Trematode Biology (ed. Fried, B. and Graczyk, T. K.), pp. 197–227. CRC Press, Boca Raton, Florida, USA.Google Scholar
Haas, W., Granzer, M. and Brockelman, C. (1990). Opisthorchis viverrini: Finding and recognition of the fish host by the cercariae. Experimental Parasitology 71, 422–431.Google Scholar
Haas, W., Körner, M., Hutterer, E., Wegner, M. and Haberl, B. (1995). Finding and recognition of the snail intermediate host by 3 species of echinostome cercariae. Parasitology 110, 133–142.Google Scholar
Haas, W., Grabe, K., Geis, C., Päch, T., Stoll, K., Fuchs, M., Haberl, B. and Loy, C. (2002 a). Recognition and invasion of human skin by Schistosoma mansoni cercariae: the key-role of L-arginine. Parasitology 124, 153–167.Google Scholar
Haas, W., Stiegeler, P., Keating, A., Kullmann, B., Rabenau, H., Schönamsgruber, E. and Haberl, B. (2002 b). Diplostomum spathaceum cercariae respond to a unique profile of cues during recognition of their fish host. International Journal for Parasitology 32, 1145–1154.Google Scholar
Haas, W., Haberl, B., Syafruddin Idris, I., Kallert, D., Kersten, S. and Stiegeler, P. (2005). Behavioural strategies used by the hookworms Necator americanus and Ancylostoma duodenale to find, recognize and invade the human host. Parasitology Research 95, 30–39.Google Scholar
Hemre, G.-I., Mommsen, T. P. and Krogdahl, A. (2002). Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquaculture Nutrition 8, 175–194.Google Scholar
Iigo, M., Furukawa, K., Hattori, A., Ohtani-Kaneko, R., Hara, M., Suzuki, T., Tabata, M. and Aida, K. (1997). Ocular melatonin rhythms in the goldfish, Carassius auratus. Journal of Biological Rhythms 12, 182–192.Google Scholar
Karnaky, K. J. (1998). Osmotic and ionic regulation. In The Physiology of Fishes (ed. Evans, D. H.), pp. 157–176. CRC Press, Boca Raton, Florida, USA.Google Scholar
Kirschner, L. B. (2004). The mechanism of sodium chloride uptake in hyperregulating aquatic animals. Journal of Experimental Biology 207, 1439–1452.Google Scholar
Lumsden, J. S. and Ferguson, H. W. (1994). Isolation and partial characterization of rainbow trout (Oncorhynchus mykiss) gill mucin. Fish Physiology and Biochemistry 12, 387–398.Google Scholar
Marshall, W. S. (2002). Na+, Cl−, Ca2+ and Zn2+ transport by fish gills: retrospective review and prospective synthesis. Journal of Experimental Zoology 293, 264–283.Google Scholar
Moon, T. W. (2001). Glucose intolerance in teleost fish: fact or fiction? Comparative Biochemistry and Physiology 129B, 143–249.Google Scholar
Nakagawa, H., Asakawa, M. and Enomoto, N. (1988). Diversity in the carbohydrate moieties of mucus glycoproteins of various fishes. Nippon Suisan Gakkaisi 54, 1653–1658.CrossRefGoogle Scholar
Niewiadomska, K. (1984). Present status of Diplostomum spathaceum (Rudolphi, 1819) and differentiation of Diplostomum pseudospathaceum nom. nov. (Trematoda: Diplostomatidae). Systematic Parasitology 6, 81–86.Google Scholar
Niewiadomska, K. and Kiseliene, V. (1994). Diplostomum cercariae (Digenea) in snails from Lithuania. II. Survey of species. Acta Parasitologica 39, 179–186.Google Scholar
Perry, S. F., Shahsavarani, A., Georgalis, T., Bayaa, M., Furimsky, M. and Thomas, S. L. Y. (2003). Channels, pumps, and exchangers in the gill and kidney of freshwater fishes: their role in ionic and acid-base regulation. Journal of Experimental Zoology 300A, 53–62.Google Scholar
Rahman, Y. J., Forward, R. B. and Rittschof, D. (2000). Responses of mud snails and periwinkles to environmental odors and disaccharide mimics of fish odor. Journal of Chemical Ecology 26, 679–696.Google Scholar
Ratanarat-Brockelman, C. (1974). Migration of Diplostomum spathaceum (Trematoda) in the fish intermediate host. Zeitschrift für Parasitenkunde 43, 123–134.Google Scholar
Rittschof, D. (1993). Body odors and neutral-basic peptide mimics: a review of responses by marine organisms. American Zoologist 33, 487–493.Google Scholar
Rittschof, D. and Cohen, J. H. (2004). Crustacean peptide and peptide-like pheromones and kairomones. Peptides 25, 1503–1516.Google Scholar
Sukhdeo, M. V. K. and Sukhdeo, S. C. (1994). Optimal habitat selection by helminths within the host environment. Parasitology 109 (Suppl.) S41–S55.Google Scholar
Sukhdeo, M. V. K. and Sukhdeo, S. C. (2002). Fixed behaviours and migration in parasitic flatworms. International Journal for Parasitology 32, 329–342.Google Scholar
Sukhdeo, M. V. K. and Sukhdeo, S. C. (2004). Trematode behaviours and the perceptual worlds of parasites. Canadian Journal of Zoology 82, 292–315.Google Scholar
Tan, D.-X., Manchester, L. C., Hardeland, R., Lopez-Burillo, S., Mayo, J. C., Sainz, R. M. and Reiter, R. J. (2003). Melatonin: a hormone, a tissue factor, an autocoid, a paracoid, and an antioxidant vitamin. Journal of Pineal Research 34, 75–78.Google Scholar
White, S. K., Secombes, C. J. and Chappell, L. H. (1991). Studies on the infectivity of Diplostomum spathaceum in rainbow trout (Oncorhynchus mykiss). Journal of Helminthology 65, 169–178.Google Scholar
Whitehead, D. L. (1978). Application of a rapid method for determining glycosaminoglycans in mucus secreted by an aquatic pulmonate Biomphalaria glabrata. Comparative Biochemistry and Physiology 59A, 27–30.Google Scholar
Zaunreiter, M., Brandstätter, R. and Goldschmid, A. (1998). Evidence for an endogenous clock in the retina of rainbow trout: I. Retinomotor movements, dopamine and melatonin. NeuroReport 9, 1205–1209.Google Scholar