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The link between climate changes and disease risks from various pathogens has been increasingly recognized. The effect of climatic factors on host–parasite population dynamics is particularly evident in northern latitudes where the occurrence and transmission of parasites are strongly regulated by seasonality-driven changes in environmental temperatures. Shortened winter periods would increase growth potential of many parasite populations. The ways in which climate warming could affect life history dynamics of the directly transmitted crustacean ectoparasite Argulus coregoni and complex life cycle trematode Diplostomum spathaceum, which frequently cause problems in northern fish farming, are discussed. Increased problems for fish farming are predicted in terms of increased infection pressure from these parasites in future. This would increase problems associated with infections and increase the use of expensive management protocols with high environmental impact.
Over the past decades, various free-living animals (hosts) and their parasites have invaded recipient areas in which they had not previously occurred, thus gaining the status of aliens or exotics. In general this happened to a low extent for hundreds of years. With variable frequency, invasions have been followed by the dispersal and establishment of non-indigenous species, whether host or parasite. In the literature thus far, colonizations by both hosts and parasites have not been treated and reviewed together, although both are usually interwoven in various ways. As to those factors permitting invasive success and colonization strength, various hypotheses have been put forward depending on the scientific background of respective authors and on the conspicuousness of certain invasions. Researchers who have tried to analyse characteristic developmental patterns, the speed of dispersal or the degree of genetic divergence in populations of alien species have come to different conclusions. Among parasitologists, the applied aspects of parasite invasions, such as the negative effects on economically important hosts, have long been at the centre of interest. In this contribution, invasions by hosts as well as parasites are considered comparatively, revealing many similarities and a few differences. Two helminths, the liver fluke, Fasciola hepatica, of cattle and sheep and the swimbladder nematode, Anguillicola crassus, of eels are shown to be useful as model parasites for the study of animal invasions and environmental global change. Introductions of F. hepatica have been associated with imports of cattle or other grazing animals. In various target areas, susceptible lymnaeid snails serving as intermediate hosts were either naturally present and/or were introduced from the donor continent of the parasite (Europe) and/or from other regions which were not within the original range of the parasite, partly reflecting progressive stages of a global biota change. In several introduced areas, F. hepatica co-occurs with native or exotic populations of the congeneric F. gigantica, with thus far unknown implications. Over the fluke's extended range, in addition to domestic stock animals, wild native or naturalized mammals can also serve as final hosts. Indigenous and displaced populations of F. hepatica, however, have not yet been studied comparatively from an evolutionary perspective. A. crassus, from the Far East, has invaded three continents, without the previous naturalization of its natural host Anguilla japonica, by switching to the respective indigenous eel species. Local entomostrac crustaceans serve as susceptible intermediate hosts. The novel final hosts turned out to be naive in respect to the introduced nematode with far reaching consequences for the parasite's morphology (size), abundance and pathogenicity. Comparative infection experiments with Japanese and European eels yielded many differences in the hosts' immune defence, mirroring coevolution versus an abrupt host switch associated with the introduction of the helminth. In other associations of native hosts and invasive parasites, the elevated pathogenicity of the parasite seems to result from other deficiencies such as a lack of anti-parasitic behaviour of the naïve host compared to the donor host which displays distinct behavioural patterns, keeping the abundance of the parasite low. From the small amount of available literature, it can be concluded that the adaptation of certain populations of the novel host to the alien parasite takes several decades to a century or more. Summarizing all we know about hosts and parasites as aliens, tentative patterns and principles can be figured out, but individual case studies teach us that generalizations should be avoided.
The swimbladder nematode Anguillicola crassus originates from Asia where it is a parasite of the Japanese eel Anguilla japonica. After its introduction to Europe about 25 years ago, the parasite spread rapidly within the indigenous populations of the European eel Anguilla anguilla and subsequently the prevalence and mean intensity appeared to stabilize. Under experimental and aquaculture conditions the naïve new host appears to be more susceptible to A. crassus compared to the original host. Both eel species develop a immune response against A. crassus. The antibody response is well characterized for the European eel, but poorly characterized for the Japanese eel. It remains unclear if antibodies have any protective function against A. crassus. Encapsulation of larvae of A. crassus can be observed in naturally infected European eels. However, encapsulation of larvae following experimental infection has not been detected in European eels, but only in Japanese eels. Reinfection experiments and intraperitoneal injection of A. crassus homogenates failed to demonstrate the development of acquired immunity in European eels. Immunization with irradiated third stage larvae provided preliminary evidence for acquired immunity against A. crassus in the Japanese eel, but not in the European eel.
Under conditions of pollution both host and parasite are susceptible to the pathogenic effects of toxicants, which in turn may result in detrimental changes to their immunological and physiological processes. Digenetic trematodes, which encompass species of both medical and economic importance, possess complex life cycles and are common parasites of both vertebrates and molluscs. The combined stress induced by pollution and parasitism influences the physiology of the host which can have implications not only on host survival but also on the functional biology of resident parasite populations. The present paper reviews the effects of pollutants on the immunology and physiology in both vertebrate and molluscan host–trematode systems and the implications for parasite transmission.
Parasitism poses a serious threat to hosts under certain circumstances, while the well-being of organisms is also negatively affected by environmental pollution. Little information is available on the simultaneous effects of parasites and pollutants on the physiological homeostasis of organisms. The present paper demonstrates that parasites: (i) may influence the metabolism of pollutants in infected hosts, (ii) interact with pollution in synergistic or antagonistic ways, and (iii) may induce physiological reactions in hosts which were thought to be pollutant-induced. Experimental studies on the uptake and accumulation of metals by fish reveal that fish infected with acanthocephalans have lower metal levels than uninfected hosts; e.g. Pomphorhynchus laevis reduces lead levels in fish bile, thereby diminishing or impeding the hepatic intestinal cycling of lead, which may reduce the quantity of metals available for fish. Alterations in pollutant uptake and accumulation in different intermediate and final hosts due to parasites are thus very important in the field of ecotoxicology. In addition to such alterations, there is a close interaction between the effects of pollutants and parasites which seems to be mediated at least partly by the endocrine system, which itself is closely related to the immune system in fish. Laboratory studies on eels experimentally infected with the swimbladder nematode Anguillicola crassus reveal that toxic chemicals such as polychlorinated biphenyls produce immunosuppressive effects which facilitate parasite infection. Similarly, an increase in serum cortisol concentration in eels due to chemical exposure and infection is correlated with decreasing levels of anti-A. crassus antibodies. Furthermore, parasites are able to elicit physiological changes which are attributed to chemicals with endocrine disrupting activity, e.g. the cestode Ligula intestinalis is known to suppress gonad development in roach. The most thoroughly documented examples of endocrine disruption in wild fish are in roach, and it is conceivable that this disruption is not only due to chemical activity but also to parasites such as L. intestinalis or species of the phylum Microspora.
The pink shrimp Farfantepenaeus duorarum may acquire pollutants, helminths and symbionts from their environment. Statistical associations were studied between the symbionts and helminths of F. duorarum and pollutants in sediments, water and shrimps in Campeche Sound, Mexico. The study area spatially overlapped between offshore oil platforms and natural shrimp mating grounds. Spatial autocorrelation of data was controlled with spatial analysis using distance indices (SADIE) which identifies parasite or pollutant patches (high levels) and gaps (low levels), expressing them as clustering indices compared at each point to produce a measure of spatial association. Symbionts included the peritrich ciliates Epistylis sp. and Zoothamnium penaei and all symbionts were pooled. Helminths included Hysterothylacium sp., Opecoeloides fimbriatus, Prochristianella penaei and an unidentified cestode. Thirty-five pollutants were identified, including polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), pesticides and heavy metals. The PAHs (2–3 ring) in water, unresolved complex mixture (UCM), Ni and V in sediments, and Zn, Cr and heptachlor in shrimps were significantly clustered. The remaining pollutants were randomly distributed in the study area. Juvenile shrimps acquired pesticides, PAHs (2–3 rings) and Zn, while adults acquired PAHs (4–5 rings), Cu and V. Results suggest natural PAH spillovers, and continental runoff of dichlorodiphenyltrichloroethane (DDT), PCBs and PAHs (2–3 ring). There were no significant associations between pollutants and helminths. However, there were significant negative associations of pesticides, UCM and PCBs with symbiont numbers after controlling shrimp size and spatial autocorrelation. Shrimps and their symbionts appear to be promising bioindicators of organic chemical pollution in Campeche Sound.
Levels of parasitism and the dynamics of helminth systems is subject to the impact of environmental conditions such that we may expect long term increases in temperature will increase the force of infection and the parasite's basic reproduction number, R0. We postulate that an increase in the force of infection will only lead to an increase in mean intensity of adults when adult parasite mortality is not determined by acquired immunity. Preliminary examination of long term trends of parasites of rabbits and grouse confirm these predictions. Parasite development rate increases with temperature and while laboratory studies indicate this is linear some recent studies indicate that this may be non-linear and would have an important impact on R0. Warming would also reduce the selective pressure for the development of arrestment and this would increase R0 so that in systems like the grouse and Trichostrongylus tenuis this would increase the instability and lead to larger disease outbreaks. Extreme climatic events that act across populations appear important in synchronizing transmission and disease outbreaks, so it is speculated that climate disruption will lead to increased frequency and intensity of disease outbreaks in parasite populations not regulated by acquired immunity.
Evidence is accumulating rapidly showing that temperature and other climatic variables are driving many ecological processes. At the same time, recent research has highlighted the role of parasitism in the dynamics of animal populations and the structure of animal communities. Here, the likely interactions between climate change and parasitism are discussed in the context of intertidal ecosystems. Firstly, using the soft-sediment intertidal communities of Otago Harbour, New Zealand, as a case study, parasites are shown to be ubiquitous components of intertidal communities, found in practically all major animal species in the system. With the help of specific examples from Otago Harbour, it is demonstrated that parasites can regulate host population density, influence the diversity of the entire benthic community, and affect the structure of the intertidal food web. Secondly, we document the extreme sensitivity of cercarial production in parasitic trematodes to increases in temperature, and discuss how global warming could lead to enhanced trematode infections. Thirdly, the results of a simulation model are used to argue that parasite-mediated local extinctions of intertidal animals are a likely outcome of global warming. Specifically, the model predicts that following a temperature increase of less than 4°C, populations of the amphipod Corophium volutator, a hugely abundant tube-building amphipod on the mudflats of the Danish Wadden Sea, are likely to crash repeatedly due to mortality induced by microphallid trematodes. The available evidence indicates that climate-mediated changes in local parasite abundance will have significant repercussions for intertidal ecosystems. On the bright side, the marked effects of even slight increases in temperature on cercarial production in trematodes could form the basis for monitoring programmes, with these sensitive parasites providing early warning signals of the environmental impacts of global warming.
A study was conducted in 2000 and 2003, following the collapse of the commercial fishery in 1990, to compare metazoan parasites of Atlantic cod Gadus morhua, captured off coastal Labrador, with samples taken in 1980 and 1986. Fish were captured by otter trawl offshore in the North Atlantic Fish Organisation subarea 2J. Parasites were removed from the digestive tract, stained, identified and compared between the different groups. Both the prevalence and mean abundance of trematodes, larval nematodes and E. gadi were significantly lower in fish taken in 2000 and 2003 than in 1980. While mean values of trematodes and nematodes declined in 1986, those of Echinorhynchus gadi remained unchanged in 1986 and 1990. Four-year-old cod sampled in 1990 harboured significantly fewer E. gadi than older age groups. The most commonly occurring trematodes included Podocotylereflexa, Lepidapedon elongatum, Derogenes varicus and Hemiurus levinseni while the larval nematode, Anisakis sp. was predominant. Comparison of offshore samples taken in 2000 and 2003 with others taken in previous years suggests an overall decline of parasites coincident with a change in climatic conditions, the absence of a major food source, namely capelin Mallotus villosus, of cod and ultimately the decline of the Labrador population.
Parasite heterogeneity is thought to be an important factor influencing the likelihood and the dynamics of infection. Previous studies have demonstrated that simultaneous exposure of hosts to a heterogeneous mixture of parasites might increase infection success. Here this view is extended towards the effect of parasite heterogeneity on subsequent infections. Using a system of the tapeworm Schistocephalus solidus and its copepod intermediate host, heterogeneity of the tapeworm surface carbohydrates is investigated, i.e. structures that are potentially recognized by the invertebrate host's immune system. With lectin labelling, a significant proportion of variation in surface carbohydrates is related to differences in worm sibships (i.e. families). Tapeworm sibships were used for experimental exposure of copepods to either homogeneous combinations of tapeworm larvae, i.e. worms derived from the same sibship or heterogeneous mixtures of larvae, and copepods were subsequently challenged with an unrelated larva to study re-infection. Contrary to expectation, neither an effect of parasite heterogeneity on the current infection, nor on re-infection were found. The effect of parasitic heterogeneity on host immunity is therefore complex, potentially involving increased cross-protection on the one hand, with higher costs of raising a more heterogeneous immune response on the other.
Transmission of the fox tapeworm Echinococcus multilocularis, the causative agent of human alveolar echinococcosis, is known to depend on various environmental factors which are subject to human influence. Epidemiological data suggest that in most endemic regions anthropogenic landscape changes (e.g. deforestation and agricultural practices) have led to more favourable conditions for the parasite's animal hosts, especially arvicolid rodents, thereby increasing the risk for parasite transmission and human disease. Examples are the conversion of forests or crop fields into meadows and pastures in Europe, China and North America, and overgrazing of natural grassland in central Asia. Other anthropogenic factors include interference with host population densities by wildlife disease control, changing hunting pressure and provision of new habitats, e.g. in urban areas. Domestic dogs may, under certain conditions, get involved in the otherwise largely wildlife-based transmission, and thereby greatly increase the infection pressure to humans. The introduction of neozootic host species may increase transmission, or even initiate the parasite's life-cycle in previously non-endemic regions. Lastly, the parasite itself may be accidentally introduced into non-endemic areas, if suitable host populations are present (e.g. in northern Japan).