The increased occurrence of pollutants in ecosystems is a continuing area of concern. It is known that numerous diseases of wild aquatic animals can occur with decreased or increased prevalences in areas associated with high or chronic levels of pollution. This may have serious implications for environmental health. There has consequently been an increasing number of laboratory and field studies on disease transmission under polluted conditions, especially focusing on digeneans of medical or economic importance. The effect of pollutants to the transmission of larval digeneans (miracidia, cercariae, metacercariae) and snail-digenean interactions is therefore considered. An overview and interpretation of the published literature on laboratory and field studies is provided. It is apparent from these studies that the influence of pollutants on digenean transmission is highly complex with much of the observed effects in the laboratory often masked by a complexity of other factors in the field. Future studies would benefit from a standardisation of experimental procedures, increasing the number of combined laboratory and field studies, and increasing the complexity of the experiments undertaken.

Eight major reviews are cited to indicate a recent knowledge explosion on the use of marine parasites as potential indicators of pollution. A literature update is given for the period 1995–2001. An analysis of the publications cited is used to provide 10 refined criteria for selecting parasites as indicator/monitor species. Previously unpublished data on Diclidophora merlangi and Dictyocotyle coeliaca confirm their value as potential indicators of hydrocarbon pollution in the North Sea. An extensive knowledge of D. merlangi is summarised to emphasize its potential value as an indicator species and also to encourage studies on the health status and immune responses of its host when subjected to pollutant stressors and infection with this monogenean. A discussion focuses on publications which have reported significant recent advances in this area of research and also on accompanying issues, problems and controversies. These selected publications are used to suggest species, stages in the development of species and assemblages of species worthy of further more detailed investigations into their value as indicators/monitors of pollution. It is predicted that further good progress will be made when contaminants can be accurately identified, their precise effects on both host and parasite can be measured by histochemical and biological methods and the roles of contaminants and parasites in causing disease can be assessed separately. About 100 references are cited.

We compared parasite communities in fish taken from a polluted lake (L. Vatia) and two control lakes before (1986) and after (1995) nine years of markedly reduced chemical and nutrient loading from a pulpmill in central Finland. Discriminant analyses of the 1995 data, using a function based on the 1986 data, showed that the parasite communities in the fish from the two control lakes had changed relatively little, whereas those from L. Vatia had converged on those from the mesotrophic control lake, indicating substantial recovery from the effects of pollution. Only a few species of parasites provided evidence for recovery. These were anodontid glochidia, which had increased markedly in perch, Rhipidocotyle fennica in roach and R. campanula in both fish species. This suggests that the recovery of the polluted lake involved increased populations of anadontid clams in shallow waters. On the other side decrease of Dermocystidium percae on perch fins and Ichthyophthirius multifiliis on roach indicate increased immune responses in the fish, reflecting better water quality. Other parts of the system have apparently not yet recovered.

Intestinal helminths of fish are of increasing interest as potential bioindicators for heavy metal contamination in aquatic habitats. Among these parasites cestodes and acanthocephalans in particular have an enormous heavy metal accumulation capacity exceeding that of established free living sentinels. Metal concentrations several thousand times higher in acanthocephalans than in host tissues were described from field and laboratory studies. Whereas larval stages inside their intermediate hosts are not able to take up high quantities of metals, young worms begin to take up metals immediately after infection of the final host. After four to five weeks of exposure, the parasites reach a steady-state concentration orders of magnitude higher than the ambient water level. Thus, acanthocephalans are not only very effective in taking up metals, but they can also respond very rapidly to changes in environmental exposure. The mechanism which enable acanthocephalans to take up metals from the intestinal lumen of the host appears to be based on the presence of bile acids, which form organo-metallic complexes that are easily absorbed by the worms due to their lipophilicity. Investigations of the environmental conditions affecting metal uptake have shown that the parasites are more consistent and reliable indicators for metal pollution than the host tissues as metal levels of the latter are much more dependent on the water chemistry. Thus, after some years of research on the uptake of metals by acanthocephalans and on the factors affecting metal accumulation in intestinal parasites it should be asked if acanthocephalans meet the criteria commonly accepted for sentinels. If parasites can be considered as promising sentinels, we need reasons for the establishment of ‘new’ indicators. Therefore, this review summarises the present knowledge about parasites as bioindicators and compares the accumulation properties of parasites and established free living indicators. Finally, this review presents possible answers to the question why it could be advantageous to have new and even more sensitive indicators for environmental monitoring purposes.

This paper describes two approaches to evaluate the use of fish macroparasites as bioindicators of heavy metal pollution at selected river stretches in Austria. Firstly changes in the diversity and richness of endoparasites of the cyprinid barbel, Barbus barbus (L.), were tested in relation to heavy metal contents in the aquatic system. Secondly, the bioaccumulation potential of cadmium, lead and zinc was assessed in the acanthocephalan, Pomphorhynchus laevis (Müller, 1776), and compared with that in the muscle, liver and intestine of its barbel host. The present results indicated that in order to validate the role of parasite community patterns related to heavy metal pollution, more investigations on food web dynamics, interelationships between parasites and the presence/absence of intermediate hosts will be essential. Heavy metal concentrations differed significantly between the organs of barbel and P. laevis (P=0·001) with levels up to 2860 fold in the parasite. The high level of heavy metal accumulation in P. laevis compared with that in its barbel host, suggests that despite variability in the parasite infrapopulation, host mobility and feeding behaviour, P. laevis is a most sensitive indicator of heavy metals in aquatic ecosystems.

Although previous studies have highlighted the inflammatory responses of fish infected with parasites and exposed to pollutants, very little is known about how these two stressors interact within the fish. In this review, which also contains original data, the effect of these two parameters on the fish inflammatory response is assessed and, in particular, the role of apoptosis and the acute phase protein, C reactive protein, is evaluated. In Cyprinus carpio exposed to 0·5 mg NH4+ l−1 or 0·1 mg Cd2+ l−1 and experimentally infected with the blood fluke, Sanguinicola inermis, the pollutant type and the order in which the fish experiences the parasite and toxicant, significantly affects the ultrastructural appearance and cellular content of the pronephros and thymus. This is reflected in the intensity of infection where the pollutant appears to have less effect on an established infection. Both stressors, pollutant and infection, may mediate their effects via the endocrine system. Studies have revealed that cortisol at 100 ng ml−1 is able to induce apoptosis in pronephric cells of carp and that an increase in apoptosis is associated with an increase in phagocytosis in this immune organ. In addition, C reactive protein, which is used as a biomarker of the inflammatory response in humans and other mammals, is evaluated as a possible indicator of physiological states in fish exposed to pathogens and pollutants.

We are developing Tetrahymena thermophila as a delivery system for recombinant vaccines against parasitic protozoa, including the common fish parasite, Ichthyophthirius multifiliis. T. thermophila cell lines expressing I. multifiliis genes under the control of a cadmium-inducible metallothionein gene promoter conferred strong protection against a lethal parasite challenge when administered parenterally to naïve fish. Nevertheless, given that heavy metals can be toxic to parasites, a question arose as to whether protection resulted from Cd residues carried over with the vaccine, rather than acquired immunity per se. To address this issue, we examined the sensitivity of I. multifiliis to Cd in vitro and determined Cd concentrations in different host tissues following i.p. injection of juvenile channel catfish with the recombinant vaccine. We found that CdCl2 at concentrations [ges ]50 ppb were lethal to I. multifiliis theronts in vitro. Furthermore, Cd concentrations were clearly elevated in fish tissues and reached levels equivalent to 74 ng/g wet weight (74 ppb) in the skin within 14 days of injection with recombinant T. thermophila. Nevertheless, fish injected with non-transformed Tetrahymena grown in the presence or absence of CdCl2 showed no significant difference in either relative survival or parasite load following direct challenge with I. multifiliis.

Proliferative kidney disease (PKD) is a parasitic infection of salmonid fish characterized by an apparently abnormal immune response to the presence of the myxozoan parasite, Tetracapsuloides bryosalmonae. In order to examine the nature of the immune response at the molecular level, the expression of a range of immune regulatory genes, including cytokines and cyclooxygenase (COX)-2 was examined in naive unexposed fish and in naive fish exposed to parasite-infected water at three points during the course of a natural outbreak of PKD. Since fish with advanced PKD pathology generally exhibit increased susceptibility to secondary infections which is typical of stress/cortisol-mediated immune suppression, a further aim of this work was to examine in vitro the influence of the glucocorticoid cortisol on the bacterial lipopolysaccharide (LPS)-induced expression of the trout cytokine genes studied. Two weeks after the initial sampling, naive exposed fish showed a specific profile of up-regulated tumor necrosis factor (TNF)-α2, COX-2 and, to a lesser extent, transforming growth factor (TGF)-β1 expression. As the disease pathology increased, TNF-α2 and COX-2 expression returned to normal levels. Stress levels of cortisol suppressed the LPS inducibility of pro-inflammatory cytokine genes, although TGF-β1 and TNF-α2 appeared to be refractory. These data demonstrate that specific immune responses at the molecular level are affected during PKD infection, with the cortisol suppression of cytokine expression in vitro providing a possible link to PKD-mediated cytokine down-regulation and immune suppression.

Disruption of the endocrine system has been shown to occur in wild freshwater fish populations across the globe. Effects range from subtle changes in the physiology and sexual behaviour of fish to permanently altered sexual differentiation, impairment of gonad development and/or altered fertility. A wide variety of adverse environmental conditions may induce endocrine disruption, including sub-optimal temperatures, restricted food supply, low pH, environmental pollutants, and/or parasites. Furthermore, it is conceivable that any/all of these factors could act simultaneously to cause a range of disparate or inter-related effects. Some of the strongest evidence for a link between an adverse health effect, as a consequence of endocrine disruption, and a causative agent(s) is between the condition of intersex in wild roach (Rutlius rutilus) in UK rivers and exposure to effluents from sewage treatment works. The evidence to indicate that intersex in roach (and other cyprinid fish living in these rivers) is caused by chemicals that mimic and/or disrupt hormone function/balance in treated sewage effluent is substantial. There are a few parasites that affect the endocrine system directly in fish, including the tape worm Ligula intestinalis and a few parasites from the micropsora phylum. L. intestinalis acts at the level of the hypothalamus restricting GnRH secretion (resulting in poorly developed gonads) and is one of the very few examples where an endocrine disrupting event has been shown to result in a population-level effect (reducing it). It is well established that many parasites affect the immune system and thus the most common effect of parasites on the endocrine system in fish is likely to be an indirect one.