Is vision deterioration responsible for changes in the host's behavior caused by eye flukes?

Trematodes localizing in the lenses of fish change the behavior of their hosts. These behavioral changes are widely suggested to be parasitic manipulations of host behavior aimed at increasing the possibility of eye flukes completing their life cycle. It is often assumed that fish change their behavior due to the vision deterioration caused by trematode larvae. We checked this assumption by testing Salvelinus malma infected with eye flukes (Diplostomum pseudospathaceum) under different lighting conditions. We suggested that if the parasite alters the host's behavior through vision impairment, then in the dark (when fish do not rely on vision to navigate), the difference in the behavior of infected and uninfected fish would disappear. Eye flukes, indeed, changed fish behavior, making their hosts less vigilant. We believe this is the first evidence of possible parasitic manipulation in this study system. However, contrary to expectations, the difference in the behavior of infected and control fish was independent of the lighting conditions. Our results suggest that mechanisms of behavioral change other than vision impairment should be taken into account in this fish-eye fluke study system.

Contrasting temperature responses in seasonal timing of cercariae shedding by Rhipidocotyle trematodes.

Global warming is likely to lengthen the seasonal duration of larval release by parasites. We exposed freshwater mussel hosts, Anodonta anatina, from 2 high-latitude populations to high, intermediate and low temperatures throughout the annual cercarial shedding period of the sympatric trematodes Rhipidocotyle fennica and R. campanula, sharing the same transmission pathway. At the individual host level, under warmer conditions, the timing of the cercarial release in both parasite species shifted towards seasonally earlier period while its duration did not change. At the host population level, evidence for the lengthening of larvae shedding period with warming was found for R. fennica. R. campanula started the cercarial release seasonally clearly earlier, and at a lower temperature, than R. fennica. Furthermore, the proportion of mussels shedding cercariae increased, while day-degrees required to start the cercariae shedding decreased in high-temperature treatment in R. fennica. In R. campanula these effects were not found, suggesting that warming can benefit more R. fennica. These results do not completely support the view that climate warming would invariably increase the seasonal duration of larval shedding by parasites, but emphasizes species-specific differences in temperature-dependence and in seasonality of cercarial release.

Allee effect in a manipulative parasite within poikilothermic host under temperature change.

Temperature and intraspecific competition are important factors influencing the growth of all organisms, including parasites. The temperature increase is suggested to stimulate the development of parasites within poikilothermic hosts. However, at high parasite densities, this effect could be diminished, due to stronger intraspecific competition. Our study, for the first time, addressed the joint effects of warming and parasite abundances on parasite growth in poikilothermic hosts. The growth of the common fish parasite larvae (trematode Diplostomum pseudospathaceum) within the rainbow trout at different infection intensities and temperatures (15°C and 18°C) was experimentally investigated. The results showed that temperature was positively correlated with both parasite infection success and growth rates. The growth rates increased much more compared to those in many free-living poikilothermic animals. Atypically for a majority of parasites, D. pseudospathaceum larvae grow faster when abundant (Allee effect). The possible causes for this phenomenon (manipulation cost sharing, etc.) are discussed in this study. Importantly, limited evidence of the interaction between temperature and population density was found. It is likely that temperature did not change the magnitude of the Allee effect but affected its timing. The impact of these effects is supposed to become more pronounced in freshwater ecosystems under current climate changes.

Trematode cercariae as prey for zooplankton: effect on fitness traits of predators.

Removal of parasite free-living stages by predators has previously been suggested an important factor controlling parasite transmission in aquatic habitats. Experimental studies of zooplankton predation on macroparasite larvae are, however, scarce. We tested whether trematode cercariae, which are often numerous in shallow waters, are suitable prey for syntopic zooplankters. Feeding rates and survival of freshwater cyclopoids (Megacyclops viridis, Macrocyclops distinctus), calanoids (Arctodiaptomus paulseni), cladocerans (Sida crystallina) and rotifers Asplanchna spp., fed with cercariae of Diplostomum pseudospathaceum, a common fish trematode, were studied. In additional long-term experiments, we studied reproduction of cyclopoids fed with cercariae. All tested zooplankton species consumed cercariae. The highest feeding rates were observed for cyclopoids (33 ± 12 cercariae ind-1 h-1), which actively reproduced (up to one egg clutch day-1) when fed ad libitum with cercariae. Their reproductive characteristics did not change significantly with time, indicating that cercariae supported cyclopoids' dietary needs. Mortality of rotifers and cladocerans was high (25-28% individuals) when exposed to cercariae in contrast to cyclopoids and calanoids (<2%). Cercariae clogged the filtration apparatus of cladocerans and caused internal injuries in predatory rotifers, which ingested cercariae. Observed trophic links between common freshwater zooplankters and cercariae may significantly influence food webs and parasite transmission in lentic ecosystems.

Interactions between two parasites of brown trout (Salmo trutta): Consequences of preinfection.

Preinfection by one parasitic species may facilitate or by contrast hamper the subsequent penetration and/or establishment of other parasites in a host. The biology of interacting species, timing of preinfection, and dosage of subsequent parasite exposure are likely important variables in this multiparasite dynamic infection process. The increased vulnerability to subsequent infection can be an important and often overlooked factor influencing parasite virulence. We investigated how the preinfection by freshwater pearl mussel Margaritifera margaritifera glochidia could influence the success of subsequent infection by the common trematode Diplostomum pseudospathaceum in brown trout Salmo trutta and vice versa whether preinfection by the trematode made fish more susceptible to glochidia infection. The first experiment was repeated twice with different (low and high) exposure doses to initiate the subsequent trematode infection, while in the second experiment we varied the timing of the preinfection with trematodes. The preinfection with glochidia made fish more vulnerable to subsequent infection with trematodes. Since the trematodes penetrate through the gills, we suggest that increased host vulnerability was most likely the result of increased respiration caused by the freshwater pearl mussel glochidia encysted on gills. In turn, brown trout preinfected with trematodes were more vulnerable to the subsequent glochidial infection, but only if they were preinfected shortly before the subsequent infection (20 hr). Fish preinfected with trematodes earlier (2 weeks before the subsequent infection) did not differ in their vulnerability to glochidia. These effects were observed at moderate intensities of infections similar to those that occur in nature. Our study demonstrates how the timing and sequence of exposure to parasitic species can influence infection success in a host-multiparasite system. It indicates that the negative influence of glochidia on host fitness is likely to be underestimated and that this should be taken into consideration when organizing freshwater pearl mussel restoration procedures.

Positive density-dependent growth supports costs sharing hypothesis and population density sensing in a manipulative parasite.

Parasites manipulate their hosts' phenotype to increase their own fitness. Like any evolutionary adaptation, parasitic manipulations should be costly. Though it is difficult to measure costs of the manipulation directly, they can be evaluated using an indirect approach. For instance, theory suggests that as the parasite infrapopulation grows, the investment of individual parasites in host manipulation decreases, because of cost sharing. Another assumption is that in environments where manipulation does not pay off for the parasite, it can decrease its investment in the manipulation to save resources. We experimentally infected rainbow trout Oncorhynchus mykiss with the immature larvae of the trematode Diplostomum pseudospathaceum, to test these assumptions. Immature D. pseudospathaceum metacercariae are known for their ability to manipulate the behaviour of their host enhancing its anti-predator defenses to avoid concomitant predation. We found that the growth rate of individual parasites in rainbow trout increased with the infrapopulation size (positive density-dependence) suggesting cost sharing. Moreover, parasites adjusted their growth to the intensity of infection within the eye lens where they were localized suggesting population density sensing. Results of this study support the hypothesis that macroparasites can adjust their growth rate and manipulation investment according to cost sharing level and infrapopulation size.