Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host

University of Burgundy, Dijon, Bourgogne, France
Animal Behaviour (Impact Factor: 3.14). 11/2007; 74(5):1311-1317. DOI: 10.1016/j.anbehav.2007.02.027


Fish acanthocephalans can modify the antipredator behaviour of their intermediate hosts in response to cues from fish predators. However, it is still unclear whether such behavioural changes are adaptive, or are just the consequence of infection. We addressed this question through studying two acanthocephalans, Pomphorhynchus laevis and Polymorphus minutus, and their intermediate host, the amphipod Gammarus pulex. Pomphorhynchus laevis completes its cycle in a freshwater fish, whereas P. minutus exploits waterbirds as final hosts. We first assessed vulnerability of infected and uninfected gammarids to predation by bullheads, Cottus gobio. Pomphorhynchus laevis-infected gammarids were more susceptible to predation than uninfected ones when a refuge was available, whereas no selective predation on P. minutus-infected individuals was recorded, independently of refuge availability. We then quantified refuge use when a bullhead was present in an enclosure or when the enclosure was empty. Individuals of each group significantly increased refuge use in the presence of a bullhead. However, a larger proportion of P. laevis-infected gammarids remained out of the refuge in the presence of a predator, compared with uninfected controls, whereas no such effect was observed in P. minutus-infected ones. Finally, we assessed reaction to bullhead olfactory cues, using a Y-maze apparatus. Pomphorhynchus laevis-infected gammarids spent significantly more time in the predator-scented arm, whereas the reverse was observed in uninfected ones. Polymorphus minutus-infected individuals, however, did not differ from uninfected controls. We discuss our results in relation with the adaptiveness of host manipulation by parasites.

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Available from: Frank Cézilly, Feb 18, 2014
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    • "Apart from effects on hosts' communities, the configuration of hosts' habitats, especially in rivers, can directly impact parasite manipulation or its outcome. For instance, G. pulex individuals manipulated by the acanthocephalan P. laevis were found to be significantly more predated than uninfected individuals only when S. Labaude et al. / International Journal for Parasitology: Parasites and Wildlife xxx (2015) 1e10 6 Please cite this article in press as: Labaude, S., et al., Host manipulation in the face of environmental changes: Ecological consequences, International Journal for Parasitology: Parasites and Wildlife (2015), refuges were available (Kaldonski et al., 2007). One of the consequences of environmental changes could be a modification in the availability of refuges, notably due to modifications of water levels due to global warming. "
    International Journal for Parasitology: Parasites and Wildlife 08/2015; DOI:10.1016/j.ijppaw.2015.08.001
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    • "For solitary fish, reducing visual oddity by associating with conspecifics is unlikely given their solitary social affiliation. Alternatively, infected fish can reduce predation risk by decreasing movement and remaining closer to shelter (Grant 1997; Mikheev and Pasternak 2006; Kaldonski et al. 2007). "
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    ABSTRACT: Risk of infection by parasites may be an important contributing cause or consequence of animal movement patterns. The diel movement patterns of French grunt, a common Caribbean coral reef fish, are well documented and known to connect reef and seagrass habitat. In the northeastern Caribbean, French grunts are known to be infected by Anilocra haemuli, one of the largest and most conspicuous ectoparasitic isopods. Studies on Anilocra infection have demonstrated that infection reduces host swimming performance and condition and may alter host behavior. We tested predictions of the hypothesis that A. haemuli infection influences the movement patterns of host French grunt, specifically whether short-distance daytime movements and/or reef–seagrass migration at dusk was associated with infection. We conducted focal observations on infected and uninfected fish during both daytime resting and dusk migration periods. We also conducted daytime and nocturnal surveys in reef habitat, documenting changes in the proportion of infected individuals. We found that infected fish move significantly less than uninfected conspecifics during the day and observed 100 % of uninfected focal fish and 37.5 % of infected focal fish departing the reef during dusk. In reef habitat, the proportion of fish infected with Anilocra was also significantly greater at night compared to daytime. We suggest that A. haemuli infection alters host movement patterns and that parasitism may therefore indirectly influence trophic connectivity between reef and seagrass ecosystems.
    Behavioral Ecology and Sociobiology 06/2015; · 2.35 Impact Factor
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    • "We recorded the proportion of time spent in the scented arm and its activity corrected by time, as the total number of zones crossed in the whole olfactometer or within one arm divided by the time spent within the corresponding arm. Two infected individuals spent more than two minutes motionless and were not considered in the analysis because they did not spend enough time in any arm to provide reliable estimation of relative odour preference [25], [26]. Water was changed and the tanks rinsed with ethanol and tap water after each test to remove the olfactory cues. "
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    ABSTRACT: Trophically-transmitted parasites often change the phenotype of their intermediate hosts in ways that increase their vulnerability to definitive hosts, hence favouring transmission. As a "collateral damage", manipulated hosts can also become easy prey for non-host predators that are dead ends for the parasite, and which are supposed to play no role in transmission strategies. Interestingly, infection with the acanthocephalan parasite Polymorphus minutus has been shown to reduce the vulnerability of its gammarid intermediate hosts to non-host predators, whose presence triggered the behavioural alterations expected to favour trophic transmission to bird definitive hosts. Whilst the behavioural response of infected gammarids to the presence of definitive hosts remains to be investigated, this suggests that trophic transmission might be promoted by non-host predation risk. We conducted microcosm experiments to test whether the behaviour of P. minutus-infected gammarids was specific to the type of predator (i.e. mallard as definitive host and fish as non-host), and mesocosm experiments to test whether trophic transmission to bird hosts was influenced by non-host predation risk. Based on the behaviours we investigated (predator avoidance, activity, geotaxis, conspecific attraction), we found no evidence for a specific fine-tuned response in infected gammarids, which behaved similarly whatever the type of predator (mallard or fish). During predation tests, fish predation risk did not influence the differential predation of mallards that over-consumed infected gammarids compared to uninfected individuals. Overall, our results bring support for a less sophisticated scenario of manipulation than previously expected, combining chronic behavioural alterations with phasic behavioural alterations triggered by the chemical and physical cues coming from any type of predator. Given the wide dispersal range of waterbirds (the definitive hosts of P. minutus), such a manipulation whose efficiency does not depend on the biotic context is likely to facilitate its trophic transmission in a wide range of aquatic environments.
    PLoS ONE 07/2014; 9(7):e101684. DOI:10.1371/journal.pone.0101684 · 3.23 Impact Factor
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