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.
    International Journal for Parasitology: Parasites and Wildlife 08/2015; DOI:10.1016/j.ijppaw.2015.08.001
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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.
    Ethology 11/2011; 117(11):1019-1026. DOI:10.1111/j.1439-0310.2011.01951.x · 1.79 Impact Factor
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    • "A well-described example for parasite-induced changes in host behaviour is the acanthocephalanamphipod system (e.g. Bakker et al., 1997; Maynard et al., 1998; Médoc et al., 2006; Kaldonski et al., 2008; Benesh et al., 2009), where the amphipods serve as intermediate hosts that have to be ingested by birds or fishes, the parasite's final hosts (Crompton & Nickol, 1985). Fish parasites of the genus Pomphorhynchus are known to manipulate the photophobic behaviour (Bethel & Holmes, 1973; Kennedy et al., 1978; Bakker et al., 1997), the response to predator fish cues (Baldauf et al., 2007; Perrot-Minnot et al., 2007) as well as the activity (Dezfuli et al., 2003) of their amphipod intermediate hosts, and make them more conspicuous as the yellow–orange cystacanths are clearly visible through their cuticle (Bakker et al., 1997). "
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    ABSTRACT: Parasites with a complex life cycle are supposed to influence the behaviour of their intermediate host in such a way that the transmission to the final host is enhanced, but reduced to non-hosts. Here, we examined whether the trophically transmitted bird parasite Polymorphus minutus increases the antipredator response of its intermediate host, the freshwater amphipod Gammarus pulex to fish cues, i.e. non-host cues (‘increased host abilities hypothesis’). Aggregation behaviour and reduced activity are assumed to decrease the predation risk of gammarids by fishes. Uninfected G. pulex are known to aggregate in the presence of a fish predator. In the present study, gammarids were allowed to choose either to join a group of conspecifics or to stay solitary (experiment 1) or between two groups differing in infection status (experiment 2), both in the presence or absence of fish odour. The perception of the groups was limited to mainly olfactory cues. Contrary to the ‘increased host abilities hypothesis’, in infected gammarids of experiment 1, fish cues induced similar aggregation behaviour as in their uninfected conspecifics. In experiment 2, uninfected as well as infected gammarids did not significantly discriminate between infected and uninfected groups. Although only uninfected gammarids reduced their activity in the presence of predator cues, infected G. pulex were generally less active than uninfected conspecifics. This might suggest that P. minutus manipulates rather the general anti-predator behaviour than the plastic response to predation risk. KeywordsShoaling-Host-parasite interaction-Invertebrate-Crustacean-Gammarid-Group-Stickleback-Parasitic manipulation-Acanthocephala
    Hydrobiologia 10/2010; 654(1):137-145. DOI:10.1007/s10750-010-0377-6 · 2.28 Impact Factor
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