DISCUSSION

As indicated in our aims and objectives, research on marine parasites as pollution indicators is fraught with problems and issues. Amongst the main problems are (1.) difficulties in defining what constitutes pollution and its main causes, and (2.) understanding the relationship between a parasite species and its environment which is affected by almost 30 biotic and abiotic factors (Williams & Jones, 1994). There are however, clear indications in recent publications that some of these problems are being slowly resolved. A main issue is a division between a minority of fish parasitologists, for example Kennedy (1997) and Elston et al. (1997), who are sceptical about the use of fish parasites in this research, and a substantial majority who are in favour although many advocate caution in doing so. A comment on the minority view is appropriate before discussing how some of the main problems are being resolved. Kennedy (1997) was of the view that until we know the precise causal relationship between fish parasites and pollution their use has no clear advantages over free-living organisms as indicators of pollution. He listed 8 problems and difficulties in using them as indicators of environmental change. It is evident, however that six of these problems do not apply in our choice of D. merlangi as an indicator. Chubb (1997), anticipating publications by Yeomans, Chubb & Sweeting (1997) and Yeomans et al. (1999), questioned Kennedy's view that it is unlikely that parasites will provide easy options for monitoring environmental change. Chubb's work and that of his colleagues present convincing field and experimental results that indicate a clear link between water-borne bacterial numbers (in an organic pollution gradient) and increased intensity of trichodinid infestations. Elston et al. (1997), in discussing research results funded by the Exxon Corporation, found no trends in the health and condition of herring Clupea pallasi that could reasonably be attributed to the Exxon Valdez oil spill in 1989 in Prince William Sound, Alaska. They were sceptical about the use of condition factor, disease and indices of liver function as indicators of pollution exposure. They believed that such claims are invalid unless other factors unrelated to pollutant exposure are considered, for example age and reproductive stage of the herring, spawning behaviour and location and date of capture. The results of Moles & Wade (2001), however, do not support those of Elston et al. (1997). They stated that the link between hydrocarbon-induced immunosuppression and gill parasites, although often theorised, had never been tested. They maintained Pacific sand lance, Ammodytes hexapterus, for five weeks in a holding tank with a 3 cm layer of sand sediment before exposing them to crude oil at a level corresponding approximately to the concentrations of hydrocarbons in the shallow subtidal (10–30 m) following the Exxon Valdez oil spill. The effects of the oiled sediment on blood phagocytic function and parasite abundance were determined. This was the first laboratory study to note increases in a species of Gyrodactylus on the gills of a fish maintained on sediments at a low concentration of crude oil. They suggested that the fish were immunologically compromised due to the stress of exposure to oiled sediments. Higher levels of exposure not only resulted in lower non-specific immune responses but were also correlated to an increase in prevalence of gill monogeneans. Conversely when the immune response was elevated both prevalence and abundance of the parasite infections were reduced. Immune based biomarkers are useful measures of environmental quality. The stress associated with exposure to polycyclic aromatic hydrocarbons (PAH) can both stimulate and suppress phagocytic activity, depending on concentrations. The prevalence and abundance of gill parasites appears to be correlated with phagocytic activity and may provide a field estimate of animal health.

In returning to a discussion of the problems referred to above we can now claim to have a better understanding of the general nature of pollution and its causes. McIntyre (1995 a) pointed out that monitoring aimed at selected problems of marine pollution began around 1920 and from then until the 1940s focused mainly on problems arising from discharges of oil from ships. From the late 1940s to the 1950s fallout from radionuclides could be detected in all the world's oceans. Persistent residues from pesticides also affected fish-eating birds during this period on a global basis. The ‘Minimata’ disease in Japan in the 1950s was eventually traced to mercury-rich factory effluents and this drew attention to the dangers of heavy metals at sea. The Torrey Canyon disaster in 1967 diverted attention away from operational discharges of oil and focused on spills from large tankers. McIntyre (1995 a) lists contaminants to include metals, nutrients, radionuclides, oil, synthetic organic compounds, plastics, sediments, carbon dioxide and other radiatively active gases, and a great diversity of municipal and industrial wastes. Seventy-seven per cent of contaminants originate from land and reach the sea waterborne or airborne. Only 12% are derived from shipping.

In referring to the report of the North Sea Task Force (1993), McIntyre (1995 b) gives an excellent reason for supporting studies in the North Sea. This report was put together over several years by scientists from the eight countries surrounding the North Sea. Offshore the main polluting inputs, apart from atmospheric deposition, are from shipping and hydrocarbon extraction and there is little contamination in the northern and central parts. Shallow coastal zones, however, are very heavily polluted with many contaminants. McIntyre concluded that although in most situations pollution effects would be the results of multiple exposures to a variety of contaminants, the best measure of the integrated impact is through biological effect studies. The North Sea Task Force report firmly recommends fish disease surveys as one of four approaches in studying pollution effects although all carry difficulties in interpretation. Although the diseases referred to did not include metazoan parasites, we consider our decision to examine whiting and its specific Diclidophora parasite to be vindicated in the report.

We are also pleased that the suggestion in MacKenzie et al. (1995) and MacKenzie (1999) that the transmission stages of parasites, particularly helminths, could provide a good early warning system for marine pollution has received practical support from the results of Cross, Irwin & Fitzpatrick (2001). Their study clearly indicated that pollution-induced reductions in cercarial quality of the common inshore digenean Cryptocotyle lingua seemed capable of producing transmission failure. They also commented that cercariae in general could be excellent indicators. This study investigated the effects of heavy metal pollution, but again it is important to note that other types of pollution can have the opposite effect. Barker, Khan & Hooper (1994) found significantly higher levels of C. lingua infection in winter flounder from a site contaminated by pulp and paper mill effluent than in those from their reference site.

Lafferty (1997) gave an admirable review of the use of parasites to assess environmental quality and its complexity. He briefly discussed eight approaches to environmental assessment. A table summarised the nine main causes of change in aquatic environments: heavy metals, acid precipitation, sewage-sludge, industrial effluent, crude oil, pulp-mill effluent, thermal effluent, eutrophication and unspecified human ‘disturbance’. Their effects on parasites have been studied on Digenea, Acanthocephala, Cestoda, Monogenea, Nematoda, Ciliophora and ‘other groups’. Lafferty correctly drew attention to the need to fill many important gaps in our knowledge before conclusions can be drawn on the use of parasites as pollution indicators and advocated further research on the cercariae and miracidia of digeneans, ciliated protozoans and the presence or absence of digeneans in fish as promising areas for further research. A most important step towards further progress would be to adopt better study designs widely used in environmental impact assessment. With increased knowledge and improvements in methodology Lafferty believed environmental parasitology would contribute substantially to future impact assessment.

Lafferty & Kuris (1999) reiterated this view and drew attention to many examples of the interaction between parasites and other stressors in aquatic environments. They emphasized the importance of considering the full range of potentially interacting components of a system because the various direct and indirect effects that can impinge on a parasite's complex life cycle can make the effect of a stressor quite complex. Complexities aside, they believed that parasites can and do interact with other stressors. Recognizing these complexities fish parasitologists, as stated by McVicar (1997), appear to have pursued one or more types of study focusing on (1.) a known contaminant, (2.) a known source of pollution, and/or (3.) disease as the end point of pollution. Progress, often based only on field work, has been made on the effects of a single contaminant or a known source of pollution, as is evident from many examples given in our table updating recent literature on parasites and pollution. In assessing this progress careful consideration should be given to Hoole (1997) who stated that there is no definitive study correlating a pollutant with change in the immune status of fish and subsequent susceptibility to parasitic infection. There are, however, studies which have noted changes in several immune parameters. Hoole reviewed the variable effects of pollutants on innate immunity, antibody levels and leucocyte activity, migration and numbers and emphasized that pollutants affect the dynamics of parasite infections in fish in (1.) having toxic effects on the parasite and its free-living stages, (2.) reducing numbers of invertebrate hosts, and (3.) altering the susceptibility of fish to parasite infection. He concluded that there is evidence that pollution does affect several immune mechanisms which are stimulated by parasites. These immune parameters can be increased in fish exposed to chronic levels of some pollutants thereby possibly increasing host resistance to parasites. In contrast, the suppressive effects of pollutants on the fish immune system is also well documented and he cites his work on increase in apoptosis in pronephric cells of Cyprinus carpio exposed to cadmium. The interactions between pollutant, immune response and parasite are, therefore, very complex. More work is required on fish helminths to clarify: (1.) immune evasion strategies, for example inhibition of leucocyte adherence; (2.) evasion/tolerance of reactive oxygen intermediates; (3.) evasion of antibodies; (4.) proteinase inhibitor production; and (5.) masking host proteins.

Attempts are being made by a number of workers to consider one or more of the problems we have already discussed. Amongst those who have reported encouraging results are Khan (1998 a,b, 1999), Khan et al. (1994), Broeg et al. (1999), Diamant et al. (1999), George-Nascimento et al. (2000) and Overstreet (1999). These authors used data in addition to those from parasite studies, such as chemical analysis of the water together with biochemical and histochemical studies of host tissues. A recommendation of the ICES Advisory Committee on the Marine Environment was pursued by Broeg et al. (1999), i.e. tests on the activity of CYPIA-dependent monoxygenase ethoxyresoruffin O-decthylase (EROD) on the integrity of lysosomal membranes in hepatocytes as an indicator of non-specific acute and chronic toxic effects. The neutral lipid content in the liver was used as a marker for pathologically induced fat accumulation and lysosomal stability/macrophage aggregate activity was tested for measuring immunosuppression. Using flounder, Platichthys flesus, and its parasite assemblage of 33 species in four locations of the German Bight, Broeg et al. concluded that use of a combination of bioindicators for pollution monitoring, including EROD activity, lysosomal membrane stability and parasite diversity, facilitates the interpretation of results against a background of natural and seasonal variation and provides valuable information about the stress level of individual fish. Trichodina sp. best reflected the pollution gradient with highest infection intensity in the most polluted location, the Elbe estuary. A significant result from residue analysis of DDT and PCBs in flounder muscle was that the pollution pattern was different for every site and season sampled in the North Sea. No location was ‘unpolluted’.

A similar approach was adopted by Diamant et al. (1999) in a study of 22 species of heteroxenous and monoxenous parasites of Siganus rivulatus in the Red Sea and the Mediterranean. The Mediterranean data yielded a very low species richness value due to the absence of heteroxenous species. Mean values of EROD activity in Mediterranean fish were almost double those from the Red Sea and were therefore a good measure of exposure to contaminants. Lysosomal stability values were even more discernible for the two localities. Using acid phosphatase, the mean destabilisation time in fish from the Mediterranean was 8 minutes compared with 18 minutes for Red Sea fish. These results clearly indicated liver cell damage in the Mediterranean fish and was a good measure of the basic effects of the contaminants on the liver of S. rivulatus. This is a comparison of species richness in two localities showing high values in an ecologically stable habitat and low values for polluted areas near cage mariculture activities. These were validated by biochemical and histochemical results. It was concluded that changes in parasitological parameters are sensible tools for detecting environmental changes due to pollution.

Towards concluding this discussion of recent progress in marine pollution studies, we draw attention to difficulties in interpreting results in three areas of research, namely the effects of (1.) climate and temperature changes, (2.) pollutants on the community ecology of parasites, and (3.) a mixture of pollutants especially in areas where little basic work has been done on parasite taxonomy and much less on the ecology of host-parasite systems. A reminder of the complexity of the effects of temperature and climate changes was given by Attrill & Power (2002). They drew attention to the long-term influence of climate on our seas and thus on marine fish stocks. These authors found that nine of the 15 species of fish investigated demonstrated a significant variation between population abundance and the North Atlantic Oscillation Index (NAOI), but no significant relationship between gadoids, including whiting M. merlangus, and this index. Marcogliese (2001) drew attention to notable consequences of climate change for abiotic and biotic aspects of the environment and to the enormous literature on this subject. He then explored the potential response of parasites of aquatic animals to climate change. Kesting & Zander (2000) and Landsberg et al. (1998) are good examples of interesting results obtained from community ecology studies and of investigations of the different effects of various pollutants.

From 1992 to 1994 Kesting & Zander (2000) examined 1245 fish of five species, 2850 gammarids of four species, 18980 copepods of four species, and 1610 snails of three species in the Schlei Fjord of the Baltic Sea. Their main aims were to gain knowledge of the metazoan parasite communities of brackish water with varying degrees of salinity and to compare the results with other studies in the same area from 1977 to 1994, since it was known that a considerable increase in eutrophication had taken place during this 17 year period. They found that 21 host species were known in the study area in 1991 but only 14 were present in 1994. Similarly from 1991 to 1994 there was a reduction in the number of parasite species from 18 to 8. It is suggested that two stressors may be related to these changes: low and changing salinity and, more importantly, eutrophication with high oxygen deficiency following pollution with nitrogen and phosphate as a result of farming activities.

An important contribution was made by Landsberg et al. (1998). They evaluated the influence of parasite assemblages on the health of fish and also changes in parasite diversity, prevalence, richness and abundance in response to environmental stressors. Three categories of environmental parameters were considered: (1.) external abiotic (2.) external biotic and (3.) condition of individual fish using organosomatic indices of the spleen and liver. Their aim was to develop a cost-effective index for monitoring and assessing estuarine health. Twenty silver perch, Berdiella chrysura, were taken from each of the 19 sites off the coast of Florida and 18461 parasites representing 44 taxa were found. Nine of the taxa were present at every site and 22 of the most abundant taxa comprised 99·16% of the individuals found. The species diversity ranged from 1·48 to 3·36. Data on the prevalence of parasite groups by site and apparent response of these to environmental stressors were subjected to a rigorous statistical analysis using various methods. The results were used to construct a parasite index with a point score by site. This index was based on changes in the prevalence of parasitic groups and also in three ecological parasite measures (species diversity, parasite species richness and mean number of taxa per fish) in response to particular environmental stressors. Scores of 59 and 109 were recorded for the healthiest and unhealthiest site respectively. A relationship was found between particular stressors and parasites, namely (1.) temperature and monogeneans, (2.) contaminants and nematodes, (3.) low dissolved oxygen and protozoans and (4.) salinity together with a mixture of metal and organic contaminants and crustaceans. They concluded that parasites of fish are useful biomarkers and appear to be more sensitive to environmental stressors than are the fish themselves.

Finally in these complex areas of research, Marcogliese, Nagler & Cyr (1998) reported notable results. They exposed American plaice, Hippoglossoides platessoides, to high levels of polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) in contaminated sediments. The fish were infected with 18 helminth species, four myxozoans and one protozoan. Significant results were obtained from Trichodina sp., Gyrodactylus sp. and gastrointestinal digeneans. There was a greater abundance of Gyrodactylus and a decrease in Trichodina in exposed fish. An intriguing result was obtained with gastrointestinal digeneans in that, contrary to other studies, no change was observed.