Detection of the parasitic dinoflagellate Hematodinium in the Norway lobster Nephrops norvegicus by ELISA

Norway lobsters Nephrops norvegicus from the coastal waters of Scotland are seasonally infected by a parasitic dinoflagellate of the genus Hematodinium. An enzyme-linked immunosorbent assay (ELISA) has been developed for the detection of the parasite in the haemolymph of N. norvegicus. The ELISA is simple to perform with a detection limit of 5 x 10(4) parasites ml(-1) haemolymph. The ELISA is currently being used to study the prevalence and seasonality of Hematodinium infection in N. norvegicus and other crustacean hosts.     

Effect of different concentrations of heavy metal ions on the normal physical and chemical characteristics of the hemolymph of Palanorbarius purpura (Mollusca: Bulinidae) in the norm and during a trematode infection

Short-term simultaneous effect of high concentrations (LC25, LC50, LC75) of heavy metal ions. (Cu2+, Zn2+, Cd2+ and Pb2+) and infection with trematode partenites Echinoparyphium aconiatum onto haemolymph of mollusk has been investigated. It was noted that low doses of toxicant (2.5 and 10 maximum admitted concentrations) have variable effect. In infected molluscs the concentration of haemoglobin decreases, while in intact ones it increases. In relation to this index, it was found, that the ion Cu2+ is highly toxic, Zn2+ and Cd(2+)--toxic, Pb(2+)--moderately toxic.     

Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea, Amphipoda) to non-host invertebrate predators

Phenotypic alterations induced by parasites in their intermediate hosts often result in enhanced trophic transmission to appropriate final hosts. However, such alterations may also increase the vulnerability of intermediate hosts to predation by non-host species. We studied the influence of both infection with 3 different acanthocephalan parasites (Pomphorhynchus laevis, P. tereticollis, and Polymorphus minutus) and the availability of refuges on the susceptibility of the amphipod Gammarus pulex to predation by 2 non-host predators in microcosms. Only infection with P. laevis increased the vulnerability of amphipods to predation by crayfish, Orconectes limosus. In contrast, in the absence of refuges, the selectivity of water scorpions, Nepa cinerea, for infected prey was significant and did not differ according to parasite species. When a refuge was available for infected prey, however, water scorpion selectivity for infected prey differed between parasite species. Both P. tereticollis- and P. laevis-infected gammarids were more vulnerable than uninfected ones, whereas the reverse was true of P. minutus-infected gammarids. These results suggest that the true consequences of phenotypic changes associated with parasitic infection in terms of increased trophic transmission of parasites deserve further assessment.     

Rainfall induces time-lagged changes in the proportion of tropical aquatic hosts infected with metazoan parasites

Rainfall serves as a powerful driving force, shifting temporal abundance and prevalence patterns in parasites and free-living aquatic organisms in tropical environments. However, there is a lack of sound evidence showing the temporal scales at which rainfall influences infection parameters of parasites in the tropics either directly by affecting the parasite life cycle or indirectly by modifying host population abundance. In the present study, we demonstrate that changes in rainfall patterns lead to changes in the proportion of infected hosts with several parasite species, causing immediate or lagged favourable conditions for an increase in levels of infection. However, the temporal scale of the influence of rainfall varied depending on the ecological characteristics of aquatic ecosystems. Despite the environmental heterogeneity and stochastic events (storms and hurricanes) which affect the study sites, the proportion of infected hosts shows frequency cycles on a yearly scale, suggesting that environmental changes are within the range of variability that naturally occur at the study sites. We propose that the incorporation of stochastic events into long-term predictive models is crucial for understanding the potential effects of global climate change on infection parameters of tropical parasites.     

How parasitism and pollution affect the physiological homeostasis of aquatic hosts

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.     

Variation in stickleback head morphology associated with parasite infection

Parasites can affect host phenotypes, influencing their ecology and evolution. Host morphological changes occurring post-infection might result from pathological by-products of infection, or represent adaptations of hosts or parasites. We investigated the morphology of three-spined sticklebacks, Gasterosteus aculeatus , from a population naturally infected with Schistocephalus solidus , which grows to large sizes in their body cavity. We examined local effects of infection on trunk shape, which are imposed directly by the bulk of the growing parasite, and distant effects on head morphology. We show that trunk shape differed between infection classes, and was affected more severely in fish with heavier total parasite mass. We further show unexpected differences in head morphology. The heads of infected fish were reduced in size and differently shaped to those of non-infected fish, with infected fish having deeper heads. Importantly, both head size and shape were also affected more severely in fish with heavier total parasite mass. This latter result suggests that differences in morphology are caused by post-infection changes. Such changes may be incidental, evolutionarily neutral 'side effects' of infection. However, because head morphology affects foraging ecology, such changes are likely to have fitness consequences for hosts, and may constitute adaptations, either of hosts or of parasites. We discuss our finding in the context of the evolution of phenotypic plasticity, and suggest testable hypotheses examining the proximate mechanisms underlying these morphological effects and their potential evolutionary basis.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 759–768.     

An empirical model of the optimal timing of reproduction for female amphipods infected by trematodes

Life-history theory predicts that hosts should reproduce when first infected by parasites if hosts are capable and if parasites have a lower cost on current than on future reproduction of hosts. We constructed an empirical model to explore fitness of females of the intertidal amphipod Corophium volutator that reproduced soon versus long after infection by the trematode Gynaecotyla adunca. For uninfected females, the optimal time to reproduce was at their maximum body length. However, for females infected by low or high intensities of trematode metacercariae, reproductive potential (realized fecundity) was highest for females that mated immediately after becoming infected. Even after removing a high cost of delaying reproduction for infected amphipods (high likelihood of depredation by sandpipers, which are final hosts of G. adunca), realized fecundity remained highest if reproduction occurred immediately following infection by trematodes. Results from our model support the view that early reproduction of female amphipods following infection by G. adunca is an adaptive life-history response to parasitism.     

Parasite-mediated selection in experimental metapopulations of Daphnia magna

In metapopulations, only a fraction of all local host populations may be infected with a given parasite species, and limited dispersal of parasites suggests that colonization of host populations by parasites may involve only a small number of parasite strains. Using hosts and parasites obtained from a natural metapopulation, we studied the evolutionary consequences of invasion by single strains of parasites in experimental populations of the cyclical parthenogen Daphnia magna. In two experiments, each spanning approximately one season, we monitored clone frequency changes in outdoor container populations consisting of 13 and 19 D. magna clones, respectively. The populations were either infected with single strains of the microsporidian parasites Octosporea bayeri or Ordospora colligata or left unparasitized. In both experiments, infection changed the representation of clones over time significantly, indicating parasite-mediated evolution in the experimental populations. Furthermore, the two parasite species changed clone frequencies differently, suggesting that the interaction between infection and competitive ability of the hosts was specific to the parasite species. Taken together, our results suggest that parasite strains that invade local host populations can lead to evolutionary changes in the genetic composition of the host population and that this change is parasite-species specific.     

A standardizable protocol for infection of Rhodnius prolixus with Trypanosoma rangeli, which mimics natural infections and reveals physiological effects of infection upon the insect

Trypanosoma rangeli is a protozoan parasite that shares hosts - mammals and triatomines - with Trypanosoma cruzi, the etiological agent of Chagas disease. Although T. rangeli is customarily considered to be non-pathogenic to human hosts, it is able to produce pathologies in its invertebrate hosts. However, advances are hindered by a lack of standardization of infection procedures and these pathologies need documentation. To establish a suitable, and standardizable, infection protocol, the duration of the fourth instar was evaluated in nymphs infected by injection into the thorax with different concentrations of parasites, and compared with nymphs infected naturally (i.e. orally). We demonstrate that delays in moult were attributable to the presence of the parasite in the haemolymph (vs. the gut) and propose that the protocol presented here simulates closely natural infections. This methodology was then used for the evaluation of physiological parameters and several hitherto unreported effects of T. rangeli infection on Rhodnius prolixus were revealed. Haemolymph volume was greater in infected than uninfected nymphs but this alteration could not be attributed to water retention, since infected insects lost the same amount of water as controls. However, we found that lipid content and fat body weight were both increased in insects infected by T. rangeli. We propose that this is due to the parasite’s sequestration of host blood lipids and carrier proteins. With these findings, we have taken a few first steps to unravelling physiological details of the host-parasite interaction. We suggest future directions towards a fuller understanding of mechanistic and adaptive aspects of triatomine-trypanosomatid interactions.     

The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice

The presence of Trichinella spiralis infection in groups of male mice caused behavioural changes in both infected and uninfected mice. Also, for some behaviours, the extent of behavioural change in infected mice appeared to be determined by the number of muscle larvae they harboured. Infected mice showed a reduced frequency of exploratory and social behaviours compared with uninfected mice while uninfected mice performed more social investigatory activities towards those that were infected. Social interactions between infected and uninfected mice were also affected by familiarity. Behavioural differences shown to result from infection in mice familiar with each other were similar but more pronounced when the mice were unfamiliar. These results suggest that other factors may influence the behavioural effects of parasites on their hosts. For some behaviours, the greatest alterations in behaviour apparently caused by infection coincided with the period of infectivity to another host. The significance of this in relation to parasite transmission is considered.     

Effect of nitroammofoska on the aldolase activity of the normal hemolymph in the mollusk Planorbarius banaticus and in trematode invasion

The infection of Planorbarius banaticus with sporocysts of Cotylurus cornutus is accompanied by an increase in aldolase activity of molluscs' haemolymph of 1.2 fold. In solutions of nitroammofoska (0.1, 1 and 10 mg/1) the activity of this ferment in infected individuals increases much higher than in non-infected ones. This results in fast carbohydrate expenditures by molluscs, intermediate hosts of trematodes, and their death from exhaustion.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Positive phototropism is accelerated in Biomphalaria glabrata snails by infection with Schistosoma mansoni

Parasite-induced behavioral changes in their hosts favor to complete the lifecycle of parasites. Schistosome infection is also known to cause physiological changes in infected freshwater snail intermediate hosts. Here, we report, a novel phenomenon in which Schistosoma mansoni, a highly debilitating worm affecting millions of people worldwide, alters the phototropic behavior of Biomphalaria glabrata, the vector snail. S. mansoni-infection enhanced positive phototropism of vector snails and infected snails spent significantly more time in light. Possibly, these behavioral changes help the parasite to be released efficiently from the infected intermediate hosts, and to infect mammalian hosts.     

Bayesian inference supports the host selection hypothesis in explaining adaptive host specificity by European bitterling

Generalist parasites have the capacity to infect multiple hosts. The temporal pattern of host specificity by generalist parasites is rarely studied, but is critical to understanding what variables underpin infection and thereby the impact of parasites on host species and the way they impose selection on hosts. Here, the temporal dynamics of infection of four species of freshwater mussel by European bitterling fish (Rhodeus amarus) was investigated over three spawning seasons. Bitterling lay their eggs in the gills of freshwater mussels, which suffer reduced growth, oxygen stress, gill damage and elevated mortality as a result of parasitism. The temporal pattern of infection of mussels by European bitterling in multiple populations was examined. Using a Bernoulli Generalized Additive Mixed Model with Bayesian inference it was demonstrated that one mussel species, Unio pictorum, was exploited over the entire bitterling spawning season. As the season progressed, bitterling showed a preference for other mussel species, which were inferior hosts. Temporal changes in host use reflected elevated density-dependent mortality in preferred hosts that were already infected. Plasticity in host specificity by bitterling conformed with the predictions of the host selection hypothesis. The relationship between bitterling and their host mussels differs qualitatively from that of avian brood parasites.     

Manipulation of host-resource dynamics impacts transmission of trophic parasites

Many complex life cycle parasites rely on predator–prey interactions for transmission, whereby definitive hosts become infected via the consumption of an infected intermediate host. As such, these trophic parasites are embedded in the larger community food web. We postulated that exposure to infection and, hence, parasite transmission are inherently linked to host foraging ecology, and that perturbation of the host-resource dynamic will impact parasite transmission dynamics. We employed a field manipulation experiment in which natural populations of the eastern chipmunk (Tamias striatus) were provisioned with a readily available food resource in clumped or uniform spatial distributions. Using replicated longitudinal capture-mark-recapture techniques, replicated supplemented and unsupplemented control sites were monitored before and after treatment for changes in infection levels with three gastro-intestinal helminth parasites. We predicted that definitive hosts subject to food supplementation would experience lower rates of exposure to infective intermediate hosts, presumably because they shifted their diet away from the intermediate host towards the more readily available resource (sunflower seeds). As predicted, prevalence of infection by the trophically transmitted parasite decreased in response to supplemental food treatment, but no such change in infection prevalence was detected for the two directly transmitted parasites in the system. The fact that food supplementation only had an impact on the transmission of the trophically transmitted parasite, and not the directly transmitted parasites, supports our hypothesis that host foraging ecology directly affects exposure to parasites that rely on the ingestion of intermediate hosts for transmission. We concluded that the relative availability of different food resources has important consequences for the transmission of parasites and, more specifically, parasites that are embedded in the food web. The broader implications of these findings for food web dynamics and disease ecology are discussed.     

Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod

According to the 'parasitic manipulation hypothesis', phenotypic changes induced by parasites in their intermediate hosts are effective means of increasing trophic transmission to final hosts. One obvious prediction, although seldom tested, is that increased vulnerability of infected prey to an appropriate predator should be achieved by the parasite altering the anti-predator behaviour of its intermediate host. In this study, we tested this prediction using the fish acanthocephalan Pomphorhynchus tereticollis and the freshwater amphipod Gammarus pulex. Firstly, we estimated the relative vulnerability of infected and uninfected gammarids to predation by the bullhead Cottus gobio in the field. Second, we investigated under experimental conditions how two common anti-predator behaviours of aquatic invertebrates, refuge use and short-distance reaction to predator chemical cues, were affected by infection status. We found that the prevalence of infection in the field was 10 times higher among gammarids collected from the stomach contents of bullheads compared with free-ranging individuals collected in the same river. In a microcosm uninfected gammarids, but not infected ones, increased the use of refuge in the presence of a bullhead. Finally, a behavioural experiment using an Y-maze olfactometer showed opposite reactions to predator odour. Whereas uninfected gammarids were significantly repulsed by the chemical cues originating from bullheads, infected ones were significantly attracted to the odour of the predator. Taken together, our results suggest that the alteration of anti-predator behaviour in infected G. pulex might enhance predation by bullheads in the field. Reversing anti-predator behaviour might thus be an efficient device by which parasites with complex life-cycles increase their trophic transmission to final hosts. Further studies should pay more attention to both the increased vulnerability of infected prey to an appropriate predator in the field and the influence of parasitic infection on the anti-predator behaviour of intermediate hosts.     

Infection dynamics of Cichlidogyrus tilapiae and C. sclerosus (Monogenea, Ancyrocephalinae) in Nile tilapia (Oreochromis niloticus L.) from Uganda

The infection dynamics of the gill monogeneans Cichlidogyrus tilapiae and C. sclerosus on Oreochromis niloticus with respect to habitat type (reservoir, stream, ponds and cages), host sex, size and seasons was determined between January and November 2008. During the study period, 45.2% of the 650 fish examined were infected with Cichlidogyrus spp. The infected hosts harboured an average of 8.6 ± 3.4 parasites/fish. Across habitat types, the proportion of infected fish was not statistically different. In contrast, the number of parasites recorded on infected fish from different habitat types differed significantly. The highest parasite number was recorded in reservoir-dwelling fish and lowest in stream-dwelling hosts. Concerning sex, more female O. niloticus were infected and harboured a high number of parasites than male and sexually undifferentiated fish. A weak negative relationship was found between rainfall and monthly parasite infections. However, a higher number of parasites and proportion of infected hosts were found during dry than in wet seasons, except in ponds. Results of this study show that differential exposure due to changes in fish behaviour associated with habitat modification and sex may account for the infection difference across the sampled sites. Meanwhile, rainfall and the associated hydrological events are important factors regulating monogenean infections in tropical aquatic environments. The continuous presence of Cichlidogyrus spp. in fish provides evidence of possible parasite outbreaks, indicating the application of biosecurity measures as crucial for the success of intensive fish farming.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

Parasite effects on host’s trophic and isotopic niches

Wild animals are usually infected with parasites that can alter their hosts’ trophic niches in food webs as can be seen from stable isotope analyses of infected versus uninfected individuals. The mechanisms influencing these effects of parasites on host isotopic values are not fully understood. Here, we develop a conceptual model to describe how the alteration of the resource intake or the internal resource use of hosts by parasites can lead to differences of trophic and isotopic niches of infected versus uninfected individuals and ultimately alter resource flows through food webs. We therefore highlight that stable isotope studies inferring trophic positions of wild organisms in food webs would benefit from routine identification of their infection status.     

Signs of a vector's adaptive choice: on the evasion of infectious hosts and parasite‐induced mortality

Laboratory and field experiments have demonstrated in many cases that malaria vectors do not feed randomly, but show important preferences either for infected or non‐infected hosts. These preferences are likely in part shaped by the costs imposed by the parasites on both their vertebrate and dipteran hosts. However, the effect of changes in vector behaviour on actual parasite transmission remains a debated issue. We used the natural associations between a malaria‐like parasite Polychromophilus murinus, the bat fly Nycteribia kolenatii and a vertebrate host the Daubenton's bat Myotis daubentonii to test the vector's feeding preference based on the host's infection status using two different approaches: 1) controlled behavioural assays in the laboratory where bat flies could choose between a pair of hosts; 2) natural bat fly abundance data from wild‐caught bats, serving as an approximation of realised feeding preference of the bat flies. Hosts with the fewest infectious stages of the parasite were most attractive to the bat flies that did switch in the behavioural assay. In line with the hypothesis of costs imposed by parasites on their vectors, bat flies carrying parasites had higher mortality. However, in wild populations, bat flies were found feeding more based on the bat's body condition, rather than its infection level. Though the absolute frequency of host switches performed by the bat flies during the assays was low, in the context of potential parasite transmission they were extremely high. The decreased survival of infected bat flies suggests that the preference for less infected hosts is an adaptive trait. Nonetheless, other ecological processes ultimately determine the vector's biting rate and thus transmission. Inherent vector preferences therefore play only a marginal role in parasite transmission in the field. The ecological processes rather than preferences per se need to be identified for successful epidemiological predictions.