Helgol Mar Res (1999) 53:195–208 © Springer-Verlag and AWI 1999 ORIGINAL ARTICLE A. Diamant · A. Banet · I. Paperna H. v. Westernhagen · K. Broeg · G. Kruener W. Koerting · S. Zander The use of fish metabolic, pathological and parasitological indices in pollution monitoring II. The Red Sea and Mediterranean Received: 25 February 1999 / Received in revised form: 15 May 1999 / Accepted: 20 May 1999 Abstract The complex interactions between parasites, fish from sandy habitat or mariculture-impacted sandy hosts and the environment are influenced by the stability habitat. The results of the study emphasized the negative of the ecosystem. Heteroxenous parasites, with complex, impacts of cage mariculture on the environment. The multiple-host life cycles, can persist only in habitats rabbitfish collected near the mariculture farms supported where the full range of their required hosts are present. the poorest and least diverse parasite communities of all Conversely, in impoverished environments such as those sampled sites, with virtual depletion of heteroxenous impacted by environmental stress, monoxenous species species, and even reduction of gill monogenean infec- that have simple, single-host life cycles are likely to pre- tions on the hosts. When results from the Mediterranean dominate. In the present study, we analyzed the ratio be- sites were compared with those of the Red Sea, the data tween heteroxenous and monoxenous (H/M) parasites as showed full representation of monoxenous parasites (all well as parasite species richness (SH/SM) and species di- but one of Red Sea origin), while heteroxenous species versity in rabbitfish (Siganus rivulatus) collected from were completely absent. We may therefore regard the several sites in the Red Sea. The rabbitfish is a Suez Ca- Mediterranean as a simulation model for a severely envi- nal immigrant, well established in the eastern Mediterra- ronmentally deteriorated, impoverished habitat, in which nean, and fish were also collected from a site on the all or part of the intermediate host species have been de- Mediterranean coast of Israel. Separate treatment of the pleted, enabling survival of the monoxenous parasite micro- and macroparasite components of the rabbitfish species only. Parasitological investigations were supple- parasite communities in the Red Sea suggested that mac- mented by testing the activity of cytochrome P 450- roparasites only – monogenea and gut parasites – were dependent mono-oxygenase EROD as a measure of ex- better indicators than the parasite community as a whole. posure, and lysosomal stability as a measure of toxic ef- Quantification of macroparasites is accurate, saves time fect in the liver of rabbitfish. The results underline the and effort, produces more accurate data and better differ- parasitological findings, showing that fish caught at the entiates between sites. Higher H/M ratios and SH/SM ra- impacted sandy beach location in the Red Sea have sig- tios were found in the rabbitfish collected at the ecologi- nificantly higher EROD activity and a decreased mem- cally stable habitat of the coral reef compared to rabbit- brane stability compared with animals from the coral reef. In comparison, EROD activity values in rabbitfish A. Diamant (✉) · A. Banet from the Mediterranean Sea were double, while lysoso- National Center for Mariculture, mal membrane stability was half that measured at the Israel Oceanographic and Limnological Research Ltd; most impacted Red Sea location. P.O. Box 1212, Eilat, Israel 88112 e-mail: [email protected] Key words Pollution monitoring · Red Sea · I. Paperna Mediterranean · Heteroxenous and monoxenous parasites · The Hebrew University of Jerusalem, Faculty of Agriculture, Rabbitfish (Siganus rivulatus) · EROD · Lysosome stability P.O. Box 12, Rehovot, Israel 76100 H. v. Westernhagen · K. Broeg · G. Kruener Biologische Anstalt Helgoland, Introduction Alfred Wegener Institut für Polar- und Meeresforschung, Notkestrasse 31, D-22607 Hamburg, Germany The assessment of ecosystem health in terms of applied W. Koerting · S. Zander Tierärztliche Hochschule Hannover, ecological criteria is becoming increasingly important in Fachgebiet Fischkrankheiten und Fischhaltung, the attempt to define the human impact beyond the sim- Bunteweg 17, D-30559 Hannover, Germany ple measurement of anthropogenic pollutants in the envi- 196 ronment. The health of an ecological system can be mea- ity in sampling, detection, identification, data recording sured by the health of its individual components ex- and analysis. pressed as biochemical parameters, or by its resilience to To test whether the results obtained from the parasito- disturbance and its level of biodiversity, employing vari- logical data were due to the influence of environmental ous ecological parameters. Venturing from chemical to contamination, two biological effect monitoring parame- biological monitoring towards the application of bio- ters at the molecular and subcellular level of biological chemical parameters in biological effects monitoring has organization were measured in the same rabbitfish of the marked a milestone in the approach to environmental Mediterranean Sea and the Red Sea. The activity of the quality assessment. In addition, the consequent applica- CYP1A-dependent mono-oxygenase EROD in fish liver tion of a still more holistic approach will inevitably lead was used as a biomarker of exposure of specific lipophil- from the use of established biochemical and biological ic, planar compounds like polyaromatic hydrocarbons parameters (such as EROD activity) to a better under- (PAHs) and polychlorinated bi-phenyls (PCBs), while standing of human impact effects through the elucidation the stability of hepatocyte lysosomal membranes was of ecological processes. tested as a biomarker for nonspecific toxic response. The impact of human activities should be visible at all Both parameters are recommended by the ICES Adviso- ecological levels and concomitantly with the conserva- ry Committee on the Marine Environment (ACME) for tive biomarkers such as used in chemical and biological application in biological effect monitoring and have been monitoring, and even in biological effects monitoring at tested extensively in the North Sea for their utility the subcellular level, effects should be detectable on (Anonymous 1996). higher organizational levels to the extent that whole eco- systems, or changes therein, may be used as a biomarker for anthropogenic impact. In the present study, host-spe- Materials and methods cific parasite communities are considered as the ecosys- tem under question and their reactions are compared The model fish for our study was the rabbitfish (Siganus rivula- with conservative and histochemical biomarkers. tus). It is abundant in the Gulf of Eilat, the Red Sea, and has also Parasites, due to the great diversity of their life history migrated via the Suez Canal into the east Mediterranean Sea (Ben Tuvia 1953). Rabbitfish occupy a variety of coastal habitats and strategies, appear to be extremely sensitive bio-indicators their associated parasite community components are relatively in the ecosystem (Overstreet 1997; Paperna 1997). Heter- well known (Diamant 1985, 1989a,b, Diamant and Paperna 1986). oxenous parasites, with complex, multiple-host life cy- In the northern Gulf of Eilat, samples were regularly obtained dur- cles, can apparently persist only in habitats where the full ing 1995–1998 from five stations representing a diversity of habi- tats (Fig. 1): site 1, a coastal coral reef at the Underwater Observa- range of required hosts persist – the implication of this tory and Inter-University Institute (OBS-IUI); site 2, a sandy assumption is that transmission can be constrained in im- beach (north beach, NB); site 3, a mariculture site on the sandy poverished environments with low diversity (Bartoli and northern beach (AR); site 4, Eilat harbor (EH), site 5, a coral reef Boudouresque 1997). In such environments, monoxenous site at the oil terminal (DK). The latter two sites provided relative- ly small numbers of fish, and were considered in the analyses only species that have simple developmental strategies restrict- in some cases as additional groups for comparison, see map (Fig. ed to a single host will predominate (D’Amelio and 2) in the introductory paper to the MARS 1 project (this volume). Gerasi 1997). The basic hypothesis in this study is that In the Mediterranean most fish were obtained from Ashdod har- the ratio between the heteroxenous and monoxenous par- bor, near a mariculture cage fish farm, and a few additional fish asite community indices – or H/M (numerically or as were obtained from two other sites, at Atlit and in Haifa Bay (Kishon Harbor). population parameters) – is indicative of the biotic stabili- For the application of the biochemical and histochemical tests, ty of the ecosystem. In the present study, this evaluation parallel to parasitology on the same individual, fish were caught in was employed parallel to an analysis of the diversity pa- November 1995 in the Mediterranean Sea (Ashdod) and in the rameters of the parasite community as a whole. Red Sea (NB). The Red Sea location NB was also sampled in April and October 1997 to test whether seasonal differences occur In an impacted habitat, the analysis of parasitic infec- in a temperate sea. The Mediterranean Sea location Ashdod was tions in fishes is dependent on our ability to detect natu- sampled in April 1996 again for the same reason. Site-specific dif- ral variations