Seasonal changes in host phenotype manipulation by an acanthocephalan: time to be transmitted?

Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, Plön, Germany.
Parasitology (Impact Factor: 2.56). 02/2009; 136(2):219-30. DOI: 10.1017/S0031182008005271
Source: PubMed


Many complex life cycle parasites exhibit seasonal transmission between hosts. Expression of parasite traits related to transmission, such as the manipulation of host phenotype, may peak in seasons when transmission is optimal. The acanthocephalan Acanthocephalus lucii is primarily transmitted to its fish definitive host in spring. We assessed whether the parasitic alteration of 2 traits (hiding behaviour and coloration) in the isopod intermediate host was more pronounced at this time of year. Refuge use by infected isopods was lower, relative to uninfected isopods, in spring than in summer or fall. Infected isopods had darker abdomens than uninfected isopods, but this difference did not vary between seasons. The level of host alteration was unaffected by exposing isopods to different light and temperature regimes. In a group of infected isopods kept at 4 degrees C, refuge use decreased from November to May, indicating that reduced hiding in spring develops during winter. Keeping isopods at 16 degrees C instead of 4 degrees C resulted in higher mortality but not accelerated changes in host behaviour. Our results suggest that changes in host and/or parasite age, not environmental conditions, underlie the seasonal alteration of host behaviour, but further work is necessary to determine if this is an adaptive parasite strategy to be transmitted in a particular season.

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    • "For instance, some acanthocephalan parasites induce a stronger change in refuge use by their isopod hosts during spring, compared to summer or fall (Benesh et al., 2009a). Benesh et al. (2009a) suggested that seasonal variations in isopod behavioral alterations could result from a manipulation strategy adjusted to seasonal variation in the diet of definitive hosts. Regardless of whether seasonal modifications in manipulation are adaptive or not, temperature changes are very likely to alter such seasonality through their influence on both host and parasite ecology. "
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    ABSTRACT: Several parasite species, particularly those having complex life-cycles, are known to induce phenotypic alterations in their hosts. Most often, such alterations appear to increase the fitness of the parasites at the expense of that of their hosts, a phenomenon known as “host manipulation”. Host manipulation can have important consequences, ranging from host population dynamics to ecosystem engineering. So far, the importance of environmental changes for host manipulation has received little attention. However, because manipulative parasites are embedded in complex systems, with many interacting components, changes in the environment are likely to affect those systems in various ways. Here, after reviewing the ecological importance of manipulative parasites, we consider potential causes and consequences of changes in host manipulation by parasites driven by environmental modifications. We show that such consequences can extend to trophic networks and population dynamics within communities, and alter the ecological role of manipulative parasites such as their ecosystem engineering. We suggest that taking them into account could improve the accuracy of predictions regarding the effects of global change. We also propose several directions for future studies.
    Full-text · Article · Aug 2015 · International Journal for Parasitology: Parasites and Wildlife
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    • "In isopods infected by an acanthocephalan parasite, host manipulation changes between seasons, but this does not seem to be caused by either temperature or lighting conditions but might rather be related to host or parasite age (Benesh et al. 2009). Resource availability, too, could affect host manipulation . "
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    ABSTRACT: Host manipulation is a common strategy of parasites employed to increase their fitness by changing the phenotype of their hosts. Whether host manipulation might be affected by environmental factors such as resource availability, has received little attention. We experimentally infected laboratory-bred copepods with the cestode Schistocephalus solidus , submitted infected and uninfected copepods to either a high or a low food treatment, and measured their behaviour. Infection reduced host activity and speed in both feeding treatments. However, the difference between the infected and uninfected copepods was smaller under low food conditions, because uninfected, but not infected, copepods moved slower under these conditions. We suggest that these differences are mediated by the physical condition of copepods rather than changes in how strongly the parasite manipulated host behaviour. Additionally, we measured three fitness-relevant traits (growth, development and infection rate in the next host) of the parasite to identify potential trade-offs with host manipulation. The largest parasites in copepods appeared the least manipulative, i.e. their hosts showed the smallest behavioural alterations, but this may again reflect variation in copepod condition, rather than life history trade-offs between parasite growth and host manipulation. Our results point to the possibility that parasite transmission depends on environmental conditions.
    Full-text · Article · Jan 2015
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    • "One possible reason why we did not detect a difference was a lack of natural predator cues in the refuge use experiment and may therefore serve as a better measure for 'boldness' than actual time to seek cover from predation. In a number of studies involving acanthocephalan parasites and the behavior of their amphipod intermediate host, refuge use was lower among infected amphipods compared with uninfected amphipods in the presence of a predator or predatory olfactory cues (Benesh et al. 2009, 2008; Hechtel et al. 1983; Kaldonski et al. 2007; Perrot-Minnot et al. 2007). Hence, future studies should incorporate the presence of a predator and ⁄ or chemical cues specific to the definitive host, the white-footed mouse. "
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    ABSTRACT: Many parasites with complex life cycles are known to modify their host phenotype to enhance transmission from the intermediate host to the definitive host. Several earlier studies explored these effects in acanthocephalan and trematode parasites, especially in aquatic ecosystems; however, much less is known about parasite‐mediated alterations of host behavior in terrestrial systems involving nematodes. Here, we address this gap by investigating a trophically transmitted nematode (Pterygodermatites peromysci) that uses a camel cricket (Ceuthophilus pallidipes) as the intermediate host before transmission to the final host, the white‐footed mouse (Peromyscus leucopus). In a laboratory experiment, we quantified the anti‐predatory responses of the cricket intermediate host using simulated predator cues. Results showed a decrease in jumping performance among infected crickets as compared with uninfected crickets, specifically in terms of frequency of jumps and jumping distance. Additionally, the relationship between parasite load and frequency of jumps is negatively correlated with the intensity of infection. These behavioral modifications are likely to increase vulnerability to predation by the definitive host. An analysis of the age‐intensity pattern of infection in natural cricket populations appears to support this hypothesis: parasites accumulate with age, peak at an intermediate age class before the intensity of infection decreases in older age groups. We suggest that older, heavily infected crickets are preferentially removed from the population by predators because of increased vulnerability. These results show that cricket intermediate hosts infected with P. peromysci have diminished jumping performance, which is likely to impair their anti‐predatory behavior and potentially facilitate parasite transmission.
    Full-text · Article · Nov 2011 · Ethology
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