DISCUSSION

Fish parasites are useful biological indicators to monitor environmental change (Vidal-Martínez et al. Reference Vidal-Martínez, Pech, Sures, Purucker and Poulin2010). They have been used to indicate e.g. bacterial biomass (Palm and Dobberstein, Reference Palm and Dobberstein1999; Palm and Rückert, Reference Palm and Rückert2009), heavy metals (Sures and Siddall, Reference Sures and Siddall2003) or environmental stress (Landsberg et al. Reference Landsberg, Blakesley, Reese, McRae and Forstchen1998) (for reviews on parasitological bioindicators see Lafferty, Reference Lafferty1997; Marcogliese and Cone, Reference Marcogliese and Cone1997; Overstreet, Reference Overstreet1997; Williams and MacKenzie, Reference Williams and MacKenzie2003; Marcogliese, Reference Marcogliese2005). Sasal et al. (Reference Sasal, Mouillot, Fichez, Chifflet and Kulbicki2007) utilized fish parasites to detect anthropogenic influences (urban and industrial pollution), and Lafferty et al. (Reference Lafferty, Shaw and Kuris2008b) proposed them being a convenient method for assessing spatial variation in their final host distribution. Because their occurrence is dependent on the composition of the food web, a low biodiversity could impair parasite transmission by reducing the availability of hosts required by parasites with complex life cycles (Lafferty et al. Reference Lafferty, Shaw and Kuris2008b). Consequently, heteroxenous fish parasites with complex life cycles are generally useful tools to indicate food web relationships in unaffected marine habitats (e.g. Palm, Reference Palm1999; Palm et al. Reference Palm, Klimpel and Walter2007; Klimpel et al. Reference Klimpel, Rückert, Piatkowski, Palm and Hanel2006), and thus reflect the status of the marine food web that might be affected through environmental change.

The present study analysed the fish parasite fauna of groupers from a mariculture facility in a marine national park in Indonesia. The samples were carried out in 6 consecutive years, using fish of a similar size range and from the same net cages. By using the methodology of Bell and Morse (Reference Bell and Morse2003) and Palm and Rückert (Reference Palm and Rückert2009), we applied (1) the prevalence of trichodinid ciliates to indicate bacterial load (Palm and Dobberstein, Reference Palm and Dobberstein1999; Ogut and Palm, Reference Ogut and Palm2005; Palm and Rückert, Reference Palm and Rückert2009); (2) the ratio of ecto- versus endoparasites to indicate the natural parasite composition of free living E. fuscoguttatus in Indonesia (where the endoparasite richness is higher than the ectoparasite richness (Vidal-Martínez et al. Reference Vidal-Martínez, Aguirre-Macedo, Vivas-Rodríguez and Moravec1998; Jakob and Palm, Reference Jakob and Palm2006; Rückert et al. Reference Rückert, Hagen, Yuniar and Palm2009a)); (3) the endohelminth parasite diversity to indicate parasite transfer into the open water netcage mariculture (Rückert et al. Reference Rückert, Hagen, Yuniar and Palm2009a); (4) the prevalence of tetraphyllidean cestodes as common parasites of elasmobranch final hosts (Lafferty et al. Reference Lafferty, Shaw and Kuris2008b), and the prevalence of the nematodes Terranova sp. (5) and Raphidascaris sp. 1 (6). Four of the chosen bioindicators demonstrated significant change over the years, where the metazoan prevalence of infection decreased significantly together with a significant trend towards reduced endoparasite diversity. The Ec/En ratio remained relatively stable in the first four sampling periods, but increased in the last two years. The ectoparasitic trichodinid ciliates were only recorded in 2003/04 and 2007/08 and 2008/09 at a low prevalence of 2·9%.

According to our data, the holding conditions of the cultured Epinephelus fuscoguttatus must have changed significantly since the beginning of our sampling in 2004 until 2009. Since the holding conditions in terms of cage usage, food enrichment, freshwater bath or sorting did not change since the testing phase of the farm in 2001–2002 until today and no major disease outbreak occurred, other factors must have impacted the parasite infracommunity of the sampled fish. According to Rückert et al. (Reference Rückert, Klimpel, Al-Quraishy, Mehlhorn and Palm2009b, Reference Rückert, Klimpel and Palm2009c), trash fishes are responsible for the transmission of endohelminths into E. coioides and E. fuscoguttatus mariculture in Lampung Bay, Indonesia, depending on the trash fish species and the use of different body parts. The infestation of pellet-fed fish with endohelminths demonstrated that infestation could also occur via organisms that naturally live in, on, and in the surroundings of the net cages (Rückert et al. Reference Rückert, Klimpel, Al-Quraishy, Mehlhorn and Palm2009b). Five of the bioindicators utilized here describe the occurrence of endohelminths that are transmitted to the groupers through the intermediate hosts. The E. fuscoguttatus studied were fed with trash fishes that originated mainly from local fishermen between 2001 and 2006 and in part also from Jakarta fish market since 2006 until 2009. The trash fishes, especially those bought in larger quantities in Jakarta, were kept deep frozen and given in daily portions directly into the grouper cages. Consequently, some of the parasites recorded might have been introduced through the regular feed, though the use of frozen trash fish in larger quantities since 2006 could have minimized this effect.

Another explanation of the observed parasite transmission is mainly through the intermediate hosts that live on the net cages and in their surroundings (Rückert et al. Reference Rückert, Klimpel, Al-Quraishy, Mehlhorn and Palm2009b). The infestation of the sampled groupers may therefore reflect the parasite infestation of natural host organisms surrounding the mariculture farm. As mesh sizes and treatments did not change over the years of our samplings, a significant decrease in the grouper parasitisation might have been caused by an overall reduced number of fish parasites within the natural intermediate hosts. Palm and Rückert (Reference Palm and Rückert2009) explained the high diversity of fish parasites in the sampled groupers in 2004/05 by the novelty of the mariculture site (founded in 2001) and the use of a low number of open-water floating net cages with low stocking densities. High parasite biodiversity in the surroundings of the net cages, combined with the use of local (possibly fresh?) trash fishes must have been responsible for the observed high biodiversity of endohelminth parasites in the beginning of our sampling, between 2003/04 and 2004/05. The Thousand Islands, one of the marine national parks, can be seen as a relatively clean environment at the sampled site (Fig. 1). Under such a scenario, the fish parasites studied could be used as biological indicators for a significant ecosystem change. The low trichodinid prevalence in 2003/04 and 2007/08 and 2008/09 still indicates low bacterial load and presumably little eutrophication in the system (see Palm and Rückert, Reference Palm and Rückert2009, Rückert et al. Reference Rückert, Hagen, Yuniar and Palm2009a). The disappearance of the elasmobranch-parasitic Scolex pleuronectis and Terranova sp., however, might be connected with a transition of a relatively undisturbed marine environment at the beginning of the mariculture activity into a more affected tropical habitat, lacking important biota such as elasmobranchs as the most common top predators (Lafferty et al. Reference Lafferty, Shaw and Kuris2008b). This can be either caused by the mariculture activity itself or through a possible increased fishing pressure from the surrounding islands.

Under exclusion of a direct parasite transfer through the net cage, our data would indicate a significant change in management methods. A change in fish treatment would affect the presence of ectoparasites, thus having a greater effect on the Ec/En ratio and the presence of trichodinid ciliates. During our sampling, the ectoparasite numbers were relatively stable, and also the presence of some ectohelminths within all samples and the low number of trichodinids indicates no major shift. This can be either related to a similar and possibly ‘optimal’ treatment of the fish or to a relatively stable water quality (see above). Consequently, a major change in fish treatment during the 6 years of sampling is unlikely and cannot explain the observed result. The only other possibility is a change in feed use, from fresh local trash fishes at the beginning of the sampling in 2004 to the addition of deep frozen trash fishes from Jakarta fish markets that might have killed the endohelminth larvae before feeding them to the groupers. In summer 2009, it was also observed that cultured milkfish was used as additional grouper feed, practically preventing parasite transmission (only a single adult digenean, Isorchis parvus, was found in 35 milkfish from the netcages, with a prevalence of 83·3% in the intestine and pyloric caecae). However, some endohelminth species such as Lecithochirium sp., Prosorhynchus sp., Raphidascaris sp. and Scolex pleuronectis occurred in the groupers throughout the sampling period, suggesting that at least a portion of the feed use must not have changed, originated as fresh trash fishes from local fishermen, or directly from the surroundings of the net cage (see above).

According to Vidal-Martínez et al. (Reference Vidal-Martínez, Pech, Sures, Purucker and Poulin2010), the circumstances under which parasites can be used as biological indicators of environmental impact have not been demonstrated conclusively. This is on the one hand caused by different physiological and ecological adaptations of the different parasite species, leading to conflicting evidence if different indicator species are used. Changes in parasite abundance can be biased by sampling size, host collection and migration, or by spatial or seasonal variation. On the other hand, significant interactions have been demonstrated between different parasite taxa and environmental stressors, where it remains difficult to attribute a numerical change in parasite prevalence and intensities to a single stressor in the field. The present study demonstrates that regular systematic, parasitological studies of fish (methodology see Palm and Rückert, Reference Palm and Rückert2009) can supervise and monitor feed use and management practice within a commercially run mariculture farm. By routinely sampling a separate batch of cultured fish that is exclusively fed with trash fishes from the surroundings of the farm, groupers can be used as a model organism to monitor the mariculture environment. As such they can be introduced as a methodological standard to regulate and monitor grouper finfish mariculture, providing useful information to the fish farmers and decision makers. To protect the cultured fishes and private investment, better parasite and disease control while monitoring the health status of the environment is the prerequisite for a sustainable and environmentally friendly mariculture in Indonesia.

We have applied a method that can visualize long-term change by using parasite metrics together on a single star graph (Palm and Rückert, Reference Palm and Rückert2009). By using this approach we could demonstrate that the chosen fish parasite metrics successfully indicate a significant change in maricultured fish under holding conditions, either caused by a different culture management (especially feeding) or by environmental change. A high diversity of recorded grouper parasites, and the possibility to use the groupers and their parasites to monitor long-term changes, also suggests that this model might be useful to monitor environmental change in the wild. Though the present study is based on a series of taxonomic and systematic studies in Indonesian waters (Palm, Reference Palm2000, Reference Palm2004, 2008; Palm and Overstreet, 2000; Jakob and Palm, Reference Jakob and Palm2006; Yuniar et al. Reference Yuniar, Palm and Walter2007; Palm et al. Reference Palm, Damriyasa, Linda and Oka2008; Rückert et al. Reference Rückert, Palm and Klimpel2008; Bray and Palm, Reference Bray and Palm2009; Kuchta et al. Reference Kuchta, Scholz, Vlčková, Říha, Walter and Palm2009), several recorded parasites could not be identified to species level, and the taxonomic status of many of them is far from being resolved. This, however, is important for a broader application of fish parasites as bioindicators for environmental impact and change. Because such applications are especially useful under high biodiversity conditions – as in tropical and subtropical regions that underlie anthropogenic stressors caused by pollution, over-exploitation as well as shrimp or finfish mariculture – further taxonomic research on marine fish parasites in these regions is urgently needed.

The use of parasite diversity as an indicator of environmental change is very promising, considering the high species number of fish, their parasites and parasitic life cycle stages. Depending on the host and parasite systematics and ecology, specific model organisms are more useful than others. This necessitates taxonomic expertise, especially in tropical countries where high species diversity is common. This, however, often does not reflect reality, where most emphasis is given to short-term applied research, combined with a severe lack of taxonomic expertise in many public research institutions. We propose that fish parasites and the presented methodology should be included within regular environmental impact monitoring programmes (e.g. in Indonesia), providing further data on the parasite biodiversity in tropical countries. While gathering important information on regional environmental health aspects in tropical waters, this would also promote further interest in fish parasite systematics and taxonomy in so far underdeveloped regions.