Learned parasite avoidance is driven by host personality and resistance to infection in a fish–trematode interaction

Klemme, Ines; Karvonen, Anssi

doi:10.1098/rspb.2016.1148

Cited by 28 publications

(32 citation statements)

References 62 publications

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“…Therefore, when parasite threat arises, 424 activity reduction to some optimal level may become a more beneficial strategy. This Our 425 observation is in conformity with a previous study, which showed that more bold individuals can 426 compensate risky lifestyles with a quicker and more pronounced behavioral response to the parasitic 427 threat (Klemme & Karvonen, 2016) . Therefore, we suggest that the fish personality affects fish 428 vulnerability to parasites immediately after the host encounter with the parasitic threat.…”

Section: Infection Intensity 253supporting

confidence: 88%

Parasite transmission in aquatic ecosystems under climate change: joint effects of temperature, host behavior and elimination of parasite larvae by predators

Gopko

Mironova

Pasternak

et al. 2019

Preprint

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A moderate raise in temperature was suggested to enhance the impact of parasites on aquatic ecosystems. Under higher temperatures, poikilothermic animals (e.g. fish), increase their activity, which can result in a more frequent encounter with parasites. However, temperature increase may also trigger processes counteracting an increased risk of parasitic infections. For instance, removal of free-living stages of parasites by filter-feeding organisms can increase with temperature and potentially mitigate disease risk in ecosystems under climate change.In our study, we aimed to find out whether an increased infection transmission under higher temperatures can be, at least, partly compensated by the increased removal of parasitic larvae be aquatic predators. In addition, we planned to reveal the behavioral mechanism underlying the more successful transmission of the parasite at higher temperatures.We experimentally studied how temperature, the behavior of fish host (rainbow trout) and the presence of filter-feeding mussels in the environment influence transmission success of trematode larvae (Diplostomum pseudospathaceum cercariae) to fish host.We found that temperature raise increased, while presence of filter-feeding mussels in the environment decreased infection intensities in fish. However, the effect of mussel’s presence was constant within the tested range of water temperatures (15-23ºC), which suggests that it cannot compensate for the observed increased transmission of parasites under temperature raise. The difference in fish individual behavior (swimming activity) before the exposure to parasites was a substantial factor the affecting host’s vulnerability to infection. However, fish motor activity only weakly correlated with temperature, therefore, it is unlikely to be responsible for the increased infection success under warmer conditions. After exposure to parasites, fish strongly decreased their activity. This decrease was temperature-dependent and more pronounced in bolder (more active) fish, which leads to lower variability in activity of fish exposed to parasites compared with the safe environment. Post-exposure activity did not influence the infection intensity.In general, we showed that the elimination of trematode larvae by filter-feeders is unlikely to deter the potential effects of global warming on host-parasite interactions in temperate freshwater ecosystems.

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Section: Infection Intensity 253supporting

confidence: 88%

Parasite transmission in aquatic ecosystems under climate change: joint effects of temperature, host behavior and elimination of parasite larvae by predators

Gopko

Mironova

Pasternak

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…Cercariae used in our experiments were no older than 5 hr. The exposure time was 30 min which is similar to previous studies (e.g., Gopko et al., , ; Klemme & Karvonen, , ; Mikheev, Pasternak, Taskinen, & Valtonen, ; Mikheev et al., ; Seppälä et al., ). During the exposure water levels in each tank were decreased to 70 L and water flow was turned off.…”

Section: Methodssupporting

confidence: 81%

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

Gopko

Chowdhury

Taskinen

2018

Ecology and Evolution

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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.

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“…We found no evidence that males avoided food patches that contained infectious conidiospores or sporulating cadavers, though females appeared to avoid food patches that contained infectious corpses. Males may activate immune defenses in the presence of infectious corpses, thus reducing the need for avoidance behaviors (see Klemme & Karvonen, for evidence in sea trout), though this remains to be tested in our system and others. We also observed three cases where males were courting and attempting to copulate with female corpses, one of which was with an infectious corpse.…”

Section: Discussionmentioning

confidence: 99%

Sex differences in disease avoidance behavior vary across modes of pathogen exposure

et al. 2019

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Sex differences in disease susceptibility are widespread, and these disparities are often compounded in cases where sexual dimorphism increases exposure risk to parasites for one sex more than the other. Studies rarely link sex differences in disease susceptibility to sex differences in infection avoidance behavior. Yet, understanding the intersection of hosts’ susceptibility to infection and infection avoidance behavior is essential to predicting infection risk variation. Here, we use the fruit fly Drosophila melanogaster and a generalist entomopathogenic fungus, Metarhizium robertsii, which can be transmitted directly, indirectly, and post‐mortem as a model host–pathogen system. We test whether the relationship between susceptibility to infection and pathogen avoidance behavior covaries with host sex. We first measured differences in resistance between male and female flies after three different types of exposure—direct, sexual, and environmental—to infectious fungal conidiospores. Then, we tested whether male and female flies differed in the likelihood of mating with infected partners and their avoidance of food patches with increased infection risk. Females were more susceptible to infection under all three exposure techniques. When confronted with an infectious partner, females mated sooner than males. However, when given a choice between an exposed partner and an unexposed partner, females take longer to begin copulating compared with males, though neither sex was more likely to choose the unexposed partner than expected by chance. Neither male nor females flies avoided food patches containing infectious conidiospores, though only females show an aversion to food sites containing an infectious fly corpse. These experiments suggest that sex differences in disease susceptibility may be counteracted via differential pathogen avoidance behavior, though the strength of avoidance behavior appears to vary across different contexts of infection risk.

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Learned parasite avoidance is driven by host personality and resistance to infection in a fish–trematode interaction

Cited by 28 publications

References 62 publications

Parasite transmission in aquatic ecosystems under climate change: joint effects of temperature, host behavior and elimination of parasite larvae by predators

Parasite transmission in aquatic ecosystems under climate change: joint effects of temperature, host behavior and elimination of parasite larvae by predators

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

Sex differences in disease avoidance behavior vary across modes of pathogen exposure

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