The impact of low concentrations of cadmium on host-monogenean interactions

Abstract

Interpreting data gathered from field studies that investigate the effect of pollution on fish parasites is complicated by the presence of multiple parasite species and mixed pollutant loads. The aim of this study was, therefore, to use controlled experimental studies to assess the impact of a single heavy metal, cadmium, on selected species of the monogenean genera, Dactylogyrus Diesing, 1850 and Gyrodactylus von Nordmann, 1832 and on their hosts, Cyprinus carpio L. and Poecilia reticulata (Peters). The first host-monogenean system investigated was the gill fluke Dactylogyrus extensus Mueller & Van Cleave, 1932 and its host C. carpio; the second system, Gyrodactylus - P. reticulata, involved individual investigations on Gyrodactylus turnbulli Harris, 1986 and G. bullatarudis Turnbull, 1956. Independent investigations of parasite biology and host responses were undertaken in order to elucidate host-parasite interactions in the presence of cadmium. The maximum permitted level of cadmium in controlled freshwater sources is set at 5μg/l by EEC Directive 76/464/EEC and experiments were carried out using this concentration and the higher, but environmentally realistic, levels of 20-50μg/l. For the first time it has been demonstrated that Dactylogyrus extensus exposed to 5μg/l cadmium show a subtle enhancement in the in vitro rate of oviposition and a statistically significant enhancement in their in vivo rate of oviposition after 9-10 days exposure. The effect of cadmium on egg production by D. extensus and on selected aspects of the innate immune response of C. carpio were investigated in separate experiments. Although run independently of each other, the sample times of both experiments were the same. It was found that the treatment in which the rate of oviposition by the parasite was greatest, was the treatment, where at the same sample point, the phagocytic activity of C. carpio was greatest. Exposure of D. extensus to the higher level of 30μg/l cadmium, also enhanced egg production after 9 days, but, 14-30 days exposure resulted in a lower rate of oviposition than that recorded in control parasites, suggesting that cadmium may directly, as well as indirectly, influence the reproductive biology of this parasite species. The hatching of D. extensus eggs was similarly affected by cadmium exposure, with those produced and incubated in 5μg/l cadmium demonstrating a statistically significant more rapid hatch rate than the controls, while those produced and incubated at the higher concentration (30μg/l) showed a statistically significant slower rate of hatch than the controls. Exposure of adult D. extensus to cadmium concentrations ranging from 5 to 3,400μg/l in vitro resulted in an enhancement of survival above the controls. Only at 13,100μg/l cadmium was there a statistically significant reduction in survival and in vitro egg production. Atomic adsorption spectrometry demonstrated that D. extensus is a net accumulator of cadmium, with the concentration of cadmium accumulated by the parasite, increasing with increasing exposure concentrations. The degree of cadmium accumulation in C. carpio organs was in the order of gills > kidney > liver > muscle=spleen. Even at 5μg/l, the level of cadmium detected in the muscle (ca. 0.2μg/g) exceeded the permitted level in food fish (0.05 mg/kg (μg/g), after only 9 days exposure. The haematological and immunological responses of C. carpio exposed to 5μg/l cadmium showed only subtle differences from the control fish, with these differences being most marked in the early stages of the trial (days 9-14). By the end of the trial there was little difference in the responses of these fish from the controls, suggesting that carp can adapt to low-level cadmium exposure. Cadmium at 50μg/l resulted in exaggerated alterations to the immune responses of carp, with statistically higher cortisol levels, phagocytic activity of kidney phagocytes, granulocyte number and significant lymphopenia, at days 6 to 14 of the trial. Several of these changes are indicative of a typical stress response. The respiratory burst and phagocytosis of kidney phagocytes in C. carpio appear to be linked to the level of cortisol, with both factors increasing as cortisol levels fall, suggesting that the effects of cadmium on the immune system may be mediated to some extent via the production of corticosteroids. Cadmium at concentrations below the permitted maximum caused statistically significant increases in the population size of both Gyrodactylus bullatarudis Turnbull, 1956 and G. turnbulli Harris, 1986 on P. reticulata. Statistically significant differences in the population size of G. turnbulli were also recorded between male and female P. reticulata. Exposing P. reticulata to 5μg/l cadmium resulted in little difference in the respiratory burst of kidney phagocytes and the production of myeloperoxidase when compared to the same parameters in control fish. The phagocytic activity of these fish was, however, consistently elevated above the controls. Exposure to 20μg/l cadmium resulted in a further enhancement of both phagocytosis and respiratory burst in P. reticulata. Unlike, C. carpio, no adaptation to cadmium exposure was observed in P. reticulata within a 30-day period. During the trial, subtle differences in the innate immune parameters of male and female guppies also emerged. None of the three innate immune parameters investigated, i. e. phagocytic activity, respiratory burst and myeloperoxidase production, appeared to correlate to the observed differences in the population growth of G. turnbulli. The finding that cadmium at levels below its permitted maximum can significantly increase numbers of Gyrodactylus spp. to the detriment of P. reticulata, suggests that the water quality guidelines, with regard to the permitted concentration of this metal, should be reviewed. This study has provided the first information on the effects of low concentrations of cadmium on selected monogenean parasites and their hosts and has been the first to attempt to elucidate host-parasite interactions in the presence of this metal. The study has provided a range of interesting findings and has offered several avenues for further investigations into a complex field of research that is still in its infancy.