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.
Freshwater gammarids infected with the acanthocephalan parasite Polymorphus minutus show behavioural alterations but also differ from uninfected individuals in their appearance because of the carotenoid-based colouration of the parasite visible through the cuticle. However, it's not clear whether this phenotypic alteration is an adaptation favouring parasite transmission to the definitive host. To test this hypothesis, we investigated the selective preference of mallard towards two prey types: uninfected gammarids on which we applied a dot of inconspicuous brown paint, and uninfected gammarids on which we applied a dot of bright orange paint to mimic the change in appearance due to P. minutus without changes in host behaviour. Mallards showed a significant preference for orange-painted gammarids regardless of how gammarids were distributed (isolated or aggregated). This suggests that parasite's colouration may play a role in enhanced transmission to definitive avian hosts. The role of P. minutus' colouration in the conspicuousness of gammarids has however to be balanced by the extent to which mallards use visual cues to forage in the field. From the perspective of a multidimensional manipulation, this study suggests that the change in appearance may act synergistically with the changes in behaviour to promote transmission to waterbirds.
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