Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-10T12:35:22.900Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of infection with Anguillicola crassus and simultaneous exposure with Cd and 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) on the levels of cortisol and glucose in European eel (Anguilla anguilla)

Published online by Cambridge University Press:  06 October 2005

B. SURES ,
I. LUTZ  and
W. KLOAS
B. SURES
Affiliation:
Zoologisches Institut I - Ökologie/Parasitologie, Universität Karlsruhe, Geb. 07.01, Kornblumenstrasse 13, D76128, Karlsruhe, Germany
I. LUTZ
Affiliation:
Leibniz-Institut für Gewässerökologie und Binnenfischerei, Abt. Binnenfischerei, Müggelseedamm 310, D12587 Berlin, Germany
W. KLOAS
Affiliation:
Leibniz-Institut für Gewässerökologie und Binnenfischerei, Abt. Binnenfischerei, Müggelseedamm 310, D12587 Berlin, Germany Institut für Biologie, Abt. Endokrinologie, Humboldt Universität Berlin, Invalidenstrasse 43, D10115 Berlin, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

To investigate whether the stress response of European eels infected with Anguillicola crassus is influenced by environmental pollutants, experimentally infected eels were exposed to Cd and/or to 3,3′, 4,4′, 5-pentachlorobiphenyl (PCB 126). Serum cortisol and glucose concentrations of these eels were monitored over a period of 103 days and were compared with data from infected, unexposed eels as well as with data from uninfected eels. Additionally, the levels of cortisol were correlated with concentrations of Anguillicola-specific antibodies. All eels showed an initial increase of the cortisol levels until day 63. This general elevation of plasma cortisol is most likely due to handling stress, as all eels were repeatedly netted and afterwards inoculated with a feeding tube. At the end of the exposure period eels which were infected and those which were infected and simultaneously exposed to Cd and PCB showed significantly higher levels than the controls. The general course of serum glucose levels in eels resembled that of cortisol. Accordingly, Spearman correlation analysis revealed that an increase in serum cortisol concentrations is correlated with rising levels of glucose. With respect to immune-endocrine interactions a significant negative correlation between cortisol and anti-A. crassus antibodies was found. Our data show that A. crassus is the most potent stressor for European eels among the treatments tested within this study. This is important in terms of ecotoxicological studies as the main effects are caused by parasites rather than chemicals. Accordingly, effects of parasites on the physiological homeostasis of organisms must be considered in ecotoxicology. From the parasitological point of view our results suggest that probably as part of an unbalanced host-parasite interaction A. crassus evokes a strong cortisol response in A. anguilla, thereby suppressing the immune response which in turn enables the parasite to establish. The parasite-induced stress response in the newly adopted European eel might be one of the factors which contributes to the extremely effective colonizing strategy of A. crassus.

Keywords

stress responsecortisolglucoseAnguillicola crassusAnguilla anguillaparasites as stressorsPCBCd
Type
Research Article
Information
Parasitology , Volume 132 , Issue 2 , February 2006 , pp. 281 - 288
Copyright
2005 Cambridge University Press

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

Barton, B. A. and Iwama, G. K. ( 1991). Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annual Review of Fish Diseases 1, 3–26.CrossRefGoogle Scholar
Folmar, L. C. ( 1993). Effects of chemical contaminants on blood chemistry of teleost fish: a bibliography and synopsis of selected papers. Environmental Toxicology and Chemistry 12, 337–375.CrossRefGoogle Scholar
Gilham, I. D. and Baker, B. I. ( 1987). A black background facilitates the response to stress in teleosts. Journal of Endocrinology 105, 99–105.Google Scholar
Gill, T. S., Leitner, G., Porta, S. and Epple, A. ( 1993). Response of plasma cortisol to environmental cadmium in the eel, Anguilla rostrata Lesueur. Comparative Biochemistry and Physiology 104C, 489–495.CrossRefGoogle Scholar
Gollock, M. J., Kennedy, C. R. and Brown, J. A. ( 2005). Physiological responses to acute temperature increase in European eels (Anguilla anguilla (L.)) infected with Anguillicola crassus, compared to uninfected eels. Diseases of Aquatic Organisms 64, 223–228.Google Scholar
Gollock, M. J., Kennedy, C. R., Quabius, E. S. and Brown, J. A. ( 2004). The effect of parasitism of European eels with the nematode, Anguillicola crassus on the impact of netting and aerial exposure. Aquaculture 233, 45–54.CrossRefGoogle Scholar
Haenen, O. L. M., Van Wijngaarden, T. A. M. and Borgsteede, F. H. M. ( 1994). An improved method for the production of infective third-stage juveniles of Anguillicola crassus. Aquaculture 123, 163–165.CrossRefGoogle Scholar
Kelly, C. E., Kennedy, C. R. and Brown, J. A. ( 2000). Physiological status of wild European eels (Anguilla anguilla) infected with the parasitic nematode Anguillicola crassus. Parasitology 120, 195–202.CrossRefGoogle Scholar
Klar, B. and Sures, B. ( 2004). A nonlinear model of stress hormone levels in rats – the interaction between pollution and parasites. Eotoxicology and Environmental Safety 59, 23–30.CrossRefGoogle Scholar
Kloas, W. ( 1999). Stress physiology in fish. In Recent Developments in Comparative Endocrinology and Neurobiology ( ed. Roubos, E. W., Wendelaar Bonga, S. E., Vaudry, H. and De Loof, A.), pp. 157–160. Shaker Publishing B.V., Maastricht, The Netherlands.
Kloas, W., Reinecke, M. and Hanke, W. ( 1994). Role of the atrial natriuretic peptide for adrenal regulation in the teleost fish Cyprinus carpio. American Journal of Physiology 267, 1034–1042.CrossRefGoogle Scholar
Knopf, K. and Mahnke, M. ( 2004). Differences in susceptibility of the European eel (Anguilla anguilla) and the Japanese eel (Anguilla japonica) to the swimbladder nematode Anguillicola crassus. Parasitology 129, 491–496.CrossRefGoogle Scholar
Knopf, K., Würtz, J., Sures, B. and Taraschewski, H. ( 1998). Impact of low water temperature on the development of Anguillicola crassus in the final host Anguilla anguilla. Diseases of Aquatic Organisms 33, 143–149.CrossRefGoogle Scholar
Køie, M. ( 1991). Swimbladder nematodes (Anguillicola spp.) and gill monogeneans (Pseudodactylogyrus spp.) parasitic on the European eel (Anguilla anguilla). Journal du Conseil – Conseil Permanent International pour l'Eploration de la Mer 47, 391–398.Google Scholar
Molnár, K. ( 1994). Formation of parasitic nodules in the swimbladder and intestinal walls of the eel Anguilla anguilla due to infections with larval stages of Anguillicola crassus. Diseases of Aquatic Organisms 20, 163–170.Google Scholar
Molnár, K., Szakolczai, J. and Vetési, F. ( 1995). Histological changes in the swimbladder wall of eels due to abnormal location of adult and second stage larvae of Anguillicola crassus. Acta Veterinaria Hungarica 43, 125–137.Google Scholar
Molnár, K., Székely, C. and Baska, F. ( 1991). Mass mortality of eel in Lake Balaton due to Anguillicola crassus infection. Bulletin of the European Association of Fish Pathologists 11, 211–212.Google Scholar
Molnár, K., Baska, F., Csaba, G., Glávits, R. and Székely, C. ( 1993). Pathological and histopathological studies of the swimbladder of eels Anguilla anguilla infected with Anguillicola crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms 15, 41–50.CrossRefGoogle Scholar
Pratap, H. B. and Wendelaar Bonga, S. E. ( 1990). Effects of water-borne cadmium on plasma cortisol and glucose in the cichlid fish Oreochromis mossambicus. Comparative Biochemistry and Physiology 95C, 313–317.CrossRefGoogle Scholar
Quabius, E. S., Balm, P. H. M. and Wendelaar Bonga, S. E. ( 1997). Interrenal stress resonsiveness of tilapia (Oreochromis mossambicus) is impaired by dietary exposure to PCB 126. General and Comparative Endocrinology 108, 472–482.CrossRefGoogle Scholar
Stoeppler, M. ( 1984). Cadmium. In Metalle in der Umwelt: Verteilung, Analytik und biologische Relevanz ( ed. Merian, E.), pp. 375–408. Verlag Chemie, Weinheim, Germany.
Sures, B. ( 2004). Environmental parasitology: relevance of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170–177.CrossRefGoogle Scholar
Sures, B. and Knopf, K. ( 2004 a). Parasites as a threat to freshwater eels? Science 304, 208–209.Google Scholar
Sures, B. and Knopf, K. ( 2004 b). Individual and combined effects of Cd and 3,3′, 4,4′, 5-pentachlorobiphenyl (PCB 126) on the humoral immune response in European eel (Anguilla anguilla) experimentally infected with larvae of Anguillicola crassus (Nematoda). Parasitology 128, 445–454.Google Scholar
Sures, B., Knopf, K. and Kloas, W. ( 2001). Induction of stress by the swimbladder nematode Anguillicola crassus in European eels, Anguilla anguilla, after repeated experimental infection. Parasitology 123, 179–184.CrossRefGoogle Scholar
Sures, B., Knopf, K. and Taraschewski, H. ( 1999). Development of Anguillicola crassus (Dracunculoidea, Anguillicolidae) in experimentally infected Balearic congers (Ariosoma balearicum, Anguilloidea, Congridae). Diseases of Aquatic Organisms 39, 75–78.CrossRefGoogle Scholar
Sures, B., Scheef, G., Klar, B., Kloas, W. and Taraschewski, H. ( 2002). Interaction between cadmium exposure and infection with the intestinal parasite Moniliformis moniliformis (Acanthocephala) on the stress hormone levels in rats. Environmental Pollution 119, 333–340.CrossRefGoogle Scholar
Teles, M., Santos, M. A. and Pacheco, M. ( 2004). Responses of European eel (Anguilla anguilla L.) in two polluted environments: in situ experiments. Ecotoxicology and Environmental Safety 58, 373–378.Google Scholar
Tort, L., Kargacin, B., Torres, P., Giralt, M. and Hidalgo, J. ( 1996). The effect of cadmium exposure and stress on plasma cortisol, metallothionein levels and oxidative status in rainbow trout (Oncorhynchus mykiss) liver. Comparative Biochemistry and Physiology 114C, 29–34.CrossRefGoogle Scholar
Van Banning, P. and Haenen, O. L. M. ( 1990). Effect of the swimbladder nematode Anguillicola crassus in wild and farmed eel, Anguilla anguilla. In Pathology in Marine Science ( ed. Perkins, F. O. and Cheng, T. C.), pp. 317–330. Academic Press, New York.CrossRef
Wedemeyer, G. A., Barton, B. A. and McLeay, D. J. ( 1990). Stress and acclimation. In Methods for Fish Biology ( ed. Schreck, C. B. and Moyle, P. B.), pp. 451–489. American Fisheries Society, Bethesda, MD.
Wendelaar Bonga, S. E. ( 1997). The stress response in fish. Physiological Reviews 77, 591–625.CrossRefGoogle Scholar
Werner, W., Rey, H. G. and Wielinger, Z. ( 1970). Über die Eigenschaften eines neuen Chromogens für die Blutzuckerbestimmung nach der GOD/POD-Methode. Zeitschrift für Analytische Chemie 252, 224–228.CrossRefGoogle Scholar
Weyts, F. A. A., Cohen, N., Flik, G. and Verburg-van Kemenade, B. M. L. ( 1999). Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish and Shellfish Immunology 9, 1–20.CrossRefGoogle Scholar
Würtz, J. and Taraschewski, H. ( 2000). Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Diseases of Aquatic Organisms 39, 121–134.CrossRefGoogle Scholar