Heteroxenous Species Research Articles

How agricultural land use affects the abundance and prevalence of monoxenous and heteroxenous helminths in the generalist lizard Tropidurus hispidus.

Among the forms of anthropogenic disturbance, agricultural land use is one of the main threats to biodiversity. Understanding how interactions between parasites and hosts are affected by agricultural land use allows predictions of how these anthropogenic impacts affect parasites. Although parasitism patterns are affected by agricultural land use, it is noteworthy that different groups of parasites can respond differently to these environmental alterations. While heteroxenous species need more than one host to complete their life cycle and tend to be more harmed by anthropization, monoxenous species, which need only one host to complete their life cycle, tend to be less harmed. In this work, we evaluate how agricultural land use affects the abundance and prevalence of parasitism for monoxenous and heteroxenous helminths in the generalist lizard Tropidurus hispidus in Caatinga Domain, Brazil. We recorded differences in abundance and prevalence of heteroxeneous (higher in conserved areas) and monoxenous helminths (higher in agricultural areas). Heteroxenous helminths that have lizards as definitive hosts are mainly obtained through diet. Tropidurus hispidus predominantly consumes insects, so it is possible that the lower abundance and prevalence of heteroxenous parasites in agricultural areas, beyond habitat simplification, is related to the decrease in the insect population. As monoxenous species do not need an intermediate host, it is possible that this aspect has influenced their greater success in anthropogenic environments than heteroxenous species. This contrasting result reinforces the need for a separate assessment between these groups when evaluating effects of land use.

Conspecific migration and environmental setting determine parasite infracommunities of non-migratory individual fish.

Parasite infracommunities tend to be stochastic in nature, although environmental characteristics such as the type of water source in streams and host traits can have an effect on the biotic assemblages and by extension the parasite fauna. We examined the effect of water source and the rate of adult fish migration on the metazoan parasite infracommunities of conspecific juvenile brown trout, Salmo trutta L. among streams flowing into Lake Lucerne (Switzerland). Juvenile (1 to 2-year old) fish harboured higher parasite species richness in groundwater-fed than in surface water-fed streams, whereas the rate of fish migration did not affect infracommunity richness. Heteroxenous species were more common in groundwater-fed streams with high and medium rates of trout migration, whereas infracommunities in surface water-fed streams and streams with low rates of fish migration were dominated by one monoxenous parasite or lacked infections. Similarity in the parasite infracommunity composition of juvenile trout across streams was explained by the interaction between type of water source and adult migration rates. Our conclusions support that similarity in the parasite composition of resident freshwater conspecifics can be predicted by the local environmental settings and host migratory behaviour, whereas parasite richness is mainly influenced by the environmental characteristics.

Parasite communities in two sparid fishes from the western Mediterranean: a comparative analysis based on samples from three localities off the Algerian coast

Summary We provide the first known comparative assessment of metazoan parasite communities in two taxonomically and ecologically related sparids, Boops boops and Spicara maena, that are common in the coastal infralittoral habitats in the Mediterranean. Using abundant data for infracommunities in three localities off the Algerian coasts of the Mediterranean, we tested the general prediction that the phylogenetic proximity of the two hosts, their overlapping geographical distribution and habitat occupation, as well as the similar feeding habits and diet would contribute to a homogenization of their parasite community composition and structure. The regional fauna of parasites of B. boops and S. maena along the Algerian coasts of the western Mediterranean was species-rich (36 species) and dominated by heteroxenous species (27 spp; of these 20 digenean spp.). The phylogenetic relatedness between the two hosts resulted in a large number of shared parasites (56 %, 20 spp.). However, the significant overlap in the parasite faunas of the two sparid hosts and their similar feeding habits and diet did not translate into homogeneous parasite community pattern; a significant differentiation in terms of both, composition and structure, was observed.

Do captive conditions favor shedding of parasites in the reared Atlantic bluefin tuna (Thunnus thynnus)?

Tuna (Thunnus spp.) has been characterized by long distance migrations, highly predatory behavior and longevity, all of which in turn, enable infections with a wide spectrum of different parasitic groups, reflecting in a remarkable diversity of tuna parasite communities. Since 2003, we have been monitoring parasite communities of Atlantic bluefin tuna (Thunnus thynnus) that are caught from the wild and transferred into cages during spring–summer months, as well as assemblages in fish that exit rearing cycle during the winter harvest period after 1.5years. Interestingly in reared tuna, parasitic populations exhibit a significant decreasing trend at the end of the rearing cycle, rarely observed in other intensive productions that represent a suitable environment for the emergence, establishment and transmission of pathogens. In order to assess epizootiological behavior of tuna parasites assemblages at the beginning (B group) and at the end (A group) of 1.5year rearing cycle, we examined data on parasite prevalence and abundance over 4years. The aim was to evaluate parasite diversity indices and emerging differences between newly caught and harvested fish, as well as community compositions and their nestedness in respect to the event in the rearing cycle (capture or harvest time). In order to be able to predict classification of tuna in two categories (newly caught or heavily infected and harvested or less infected fish), based on empirical didymozoids abundances and year of sampling, we built a decision tree model. Results suggest that specificities of parasite assemblages and their dynamics in tuna before and after farming have no similar precedents in aquaculture. A trend of parasitic pauperization repeating in each rearing cycle over four-years time, in once diverse and species rich parasite communities is observed, however, structures of both B and A group rearing assemblages remain nested, with the same species being core parasites (Didymosulcus katsuwonicola and Koellikerioides intestinalis). The B group exhibited significantly higher total parasite richness and mean parasites abundance, as well as the heteroxenous species richness and abundance in comparison to A group, where monoxenous species were not recorded at all. Eleven parasite species out of 26 taxa were selected as important in discriminating between B and A groups' parasites assemblages, while significantly the most abundant in B group were D. katsuwonicola, Platocystis alalongae, K. intestinalis, Koellikerioides internogastricus, Didymocystis abdominalis and Anisakis sp. It is hard to postulate the combination of factors affecting these parasite populations, but environmental, anthropogenic or host intrinsic influence has to be taken into account for further investigation.

Parasites of the endangered Cantabrian capercaillie (Tetrao urogallus cantabricus): correlates with host abundance and lek site characteristics

In April 2000, we collected and analyzed for parasites 174 feces belonging to 48 different and identified Cantabrian capercaillies (Tetrao urogallus cantabricus) from 39 lek sites in the Cantabrian Mountains (North Spain) and determined the factors related with prevalence and abundance of propagule excretion: (1) interrelations with other parasite species, (2) characteristics of the capercaillie population (number of capercaillies in the lek site, number of occupied lek sites in a 2-km area, and abundance trend), and (3) characteristics of the lek site (orientation and altitude). The higher prevalence was observed for Eimeria sp. oocysts (29% of feces). Capillaria-like eggs were the most frequently detected among nematodes (9%). Excretion of Heterakis sp., Ascaridia sp., and Trichostrongylus sp. eggs was low. The presence of Capillaria propagules in feces was negatively related with those of Eimeria and Heterakis. This could be explained by differences in parasite transmission and capercaillie exposure because Eimeria and Heterakis have direct life cycle, whereas subfamily Capillariinae includes many heteroxenous species. Capillaria eggs were more prevalent in lek sites at lower altitude, which could be explained by altitude-related factors such as humidity, temperature, or soil characteristics that may affect intermediate host abundance. Although no relation was found with host abundance, the low parasite species diversity, prevalence, and abundance may indirectly reflect the decline of the Cantabrian capercaillie populations.

The helminth fauna of the barbary partridge Alectoris barbara in Tenerife, Canary Islands

The helminth fauna of the barbary partridge (Alectoris barbara) in Tenerife Island (Canary Archipelago) was studied from 2001 to 2002, as there were no records of helminths from this host in the Canary Islands. Seven helminth species were identified: two cestodes Choanotaenia infundibulum and Lyruterina nigropunctata, and five nematodes Aonchotheca caudinflata, Baruscapillaria obsignata, Eucoleus annulatus, Ascaridia galli and Heterakis gallinarum. Lyruterina nigropunctata, A. galli and E. annulatus are recorded for first time in A. barbara. An analysis of available data on Alectoris spp. reveals the importance of intermediate hosts such as arthropods and earthworms in the diet of partridges. Terrestrial helminths are dominant species, with monoxenous and heteroxenous species being present in similar numbers in different Alectoris species along their geographical distribution. Helminth species found in Tenerife from A. barbara are poor indicators of the host colonization from North Africa because these helminths are species that are commonly found in fowl with a cosmopolitan distribution.

Parasites of flounder (Platichthys flesus L.) from the German Bight, North Sea, and their potential use in biological effects monitoring

In the frame of an integrated biological effect monitoring programme, the parasite community of flounder (Platichthys flesus) was investigated at different locations in the German Bight from 1995 to 2000. In order to assess the impact of environmental contamination caused by anthropogenic activities on the parasite community, selected parasitological parameters that displayed significant differences between the sampling sites were subjected to correlation analyses with site-specific contamination and individual pollution loads of their fish hosts. In addition, correlation analyses were conducted with the responses of selected genetic, biochemical, histopathological, physiological and immunological parameters of fish, used as potential biomarkers. In total, 802 flounder were analysed for these parameters. Information on the chemical background at the sampling sites was derived from sediment samples and from 120 samples of blue mussel (Mytilus edulis) tissue, collected at each of the sampling sites. Based on chemical data available from the sediment and blue mussel samples, a pollution gradient could be established between the sampling sites for individual contaminants. The relative abundance of Acanthochondria cornuta, Cucullanus heterochrous and Zoogonoides viviparus, and the community measures species richness and number of heteroxenous species decreased with increasing concentrations of individual heavy metals or hydrocarbons in sediment and blue mussel samples. Most of the parasitological parameters significantly reflected the established site-specific contamination gradient, when data were pooled over all sampling campaigns. Significant correlations were also found with the contamination level of individual flounder. The parasitological parameters included the parasite species Lepeophtheirus pectoralis and Lernaeocera branchialis, which were not correlated to site-specific contamination. Several biomarkers were significantly correlated to the abundance of parasitic copepods A. cornuta, Lernaeocera branchialis and Lepeophtheirus pectoralis and to parasite community parameters. The results showed that the abundance of several metazoan parasite species, species richness and parasite diversity were reduced in contaminated habitats, and that differences between sites were not only related to natural factors, such as salinity, but also to pollution-induced stress. Thus, it can be concluded that the parasite community of fish responds to the level of pollution at a specific site as well as to residues of xenobiotics in individual fish. These findings give indications that the parasite community of fish is a valuable parameter for the assessment of ecological consequences of chemical contamination in aquatic habitats.

The use of fish metabolic, pathological and parasitological indices in pollution monitoring

The complex interactions between parasites, hosts and the environment are influenced by the stability of the ecosystem. Heteroxenous parasites, with complex, multiple-host life cycles, can persist only in habitats where the full range of their required hosts are present. Conversely, in impoverished environments such as those impacted by environmental stress, monoxenous species that have simple, single-host life cycles are likely to predominate. In the present study, we analyzed the ratio between heteroxenous and monoxenous (H/M) parasites as well as parasite species richness (SH/SM) and species diversity in rabbitfish (Siganus rivulatus) collected from several sites in the Red Sea. The rabbitfish is a Suez Canal immigrant, well established in the eastern Mediterranean, and fish were also collected from a site on the Mediterranean coast of Israel. Separate treatment of the micro- and macroparasite components of the rabbitfish parasite communities in the Red Sea suggested that macroparasites only – monogenea and gut parasites – were better indicators than the parasite community as a whole. Quantification of macroparasites is accurate, saves time and effort, produces more accurate data and better differentiates between sites. Higher H/M ratios and SH/SM ratios were found in the rabbitfish collected at the ecologically stable habitat of the coral reef compared to rabbitfish from sandy habitat or mariculture-impacted sandy habitat. The results of the study emphasized the negative impacts of cage mariculture on the environment. The rabbitfish collected near the mariculture farms supported the poorest and least diverse parasite communities of all sampled sites, with virtual depletion of heteroxenous species, and even reduction of gill monogenean infections on the hosts. When results from the Mediterranean sites were compared with those of the Red Sea, the data showed full representation of monoxenous parasites (all but one of Red Sea origin), while heteroxenous species were completely absent. We may therefore regard the Mediterranean as a simulation model for a severely environmentally deteriorated, impoverished habitat, in which all or part of the intermediate host species have been depleted, enabling survival of the monoxenous parasite species only. Parasitological investigations were supplemented by testing the activity of cytochrome P 450- dependent mono-oxygenase EROD as a measure of exposure, and lysosomal stability as a measure of toxic effect in the liver of rabbitfish. The results underline the parasitological findings, showing that fish caught at the impacted sandy beach location in the Red Sea have significantly higher EROD activity and a decreased membrane stability compared with animals from the coral reef. In comparison, EROD activity values in rabbitfish from the Mediterranean Sea were double, while lysosomal membrane stability was half that measured at the most impacted Red Sea location.

The use of fish metabolic, pathological and parasitological indices in pollution monitoring

An integrated biological effect monitoring concept has been tested in flounder (Platichthys flesus L.) from four locations with different anthropogenic impact in the German Bight. During 3 years of sampling, biomarkers at all levels of biological organisation from the molecular to the ecosystem level were applied and tested on 742 individual fish of body lengths between 18 and 25 cm. At the ecosystem level, the fish were taken as a habitat for the parasite assemblage. The hypothesis was that changes in the environment might lead to changes in the species diversity of parasites and in the infection intensity of single species, as well as between heteroxenic and monoxenic parasite species (H/M ratio). At the molecular level, activity of the CYP1A-dependent monooxygenase ethoxyresorufin O-deethylase (EROD) was used as a biomarker of exposure. At the subcellular level, the integrity of lysosomal membranes in hepatocytes was taken as an indicator of non-specific acute and chronic toxic effects. Both biomarkers are recommended by the ICES Advisory Committee on the Marine Environment for the application in biological effects monitoring programmes. In addition, neutral lipid content in the liver was used as a marker for pathologically induced fat accumulation. In the same individual fish, a new method for the measurement of macrophage aggregate activity in the liver was tested for its application and reliability in reflecting immunosuppression. Tests were accompanied by chemical analysis of standard organochlorine and heavy metal residues in flounder tissue. A total of 33 parasite species were found. As an indicator species, the mean abundance of Trichodina sp. reflected best the pollution gradient observed with highest infection intensity at the most polluted location. Species diversity was significantly higher in fish caught near the reference site and significantly lower in fish from the polluted Elbe estuary. The use of the heteroxenous/monoxenous species ratio as a marker was not useful at the locations investigated because of the dominance of heteroxenous species at all habitats. Since EROD activity and macrophage aggregate activity were dependent on sex and maturity of female flounder, only male fish were taken into consideration for the integrated evaluation of data. All biochemical and histochemical tests were able to reflect accurately the site-specific differences, as well as an observed pollution event at the end of 1995 as determined by chemical analyses. The correlation analysis revealed a connection not only between the single parasitological and biochemical parameters but also within these groups. The non-specific immune response and Trichodina infection intensity were correlated with all other parameters, leading to the assumption that these may serve as links between the lowest and the highest levels of biological organisation. The simultaneous use of metabolic and parasitological results facilitated the interpretation of the observed variations of the data and the distinction between natural variation and pollution-mediated effects.