Non-Specific Manipulation of Gammarid Behaviour by P. minutus Parasite Enhances Their Predation by Definitive Bird Hosts

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.

Host Manipulation by Parasites: A Look Back Before Moving Forward

“…Nevertheless, the drop in the proportion of studies using experimentally infected hosts indicates a shift away from the rigorous approach to infer causality that was promoted and established earlier in the history of research on host manipulation by parasites. Predation tests used to demonstrate the effectiveness of host manipulation by trophically transmitted parasites range from trials conducted under controlled laboratory conditions [38,39] to tests performed in natural or semi-natural habitats [18,40,41]. These tests remain relatively few, however, especially those conducted in natural conditions.…”

Adaptive parasitic manipulation as exemplified by acanthocephalans

“…In the experimental study of Jacquin et al. (), however, target‐host and non‐host predatory cues triggered a similar alteration of the anti‐predator behaviour in P. minutus‐ infected gammarids.…”

“…There is ample convincing evidence for adaptive trait manipulation by acanthocephalan parasites (Table S1). While Bethel and Holmes (, ) showed already in the 1970s that Polymorphus minutus alters the geotaxis and clinging behaviour of its gammarid intermediate host, Jacquin, Mori, Pause, Steffen, and Médoc () provided clear experimental evidence that this behavioural change indeed leads to an increased predation by the final host, a water bird. Furthermore, behavioural manipulation by the acanthocephalans Pomphorhynchus laevis , Polymorphus paradoxus , Corynosoma constrictum , and Acanthocephalus tumescens has been shown in intermediate hosts carrying the infectious cystacanth stage, but not or less pronounced in hosts carrying the non‐infectious acanthella stage (e.g., Franceschi, Bauer, Bollache, & Rigaud, ; Dianne et al., , ; Dianne, Perrot‐Minnot, Bauer, Güvenatam, & Rigaud, ; reviewed in Table S1), indicating that the altered behaviour is actually a consequence of infection and not its cause.…”

Parasite‐induced inversion of geotaxis in a freshwater amphipod: a role for anaerobic metabolism?

“…; Jacquin et al . ), and on the reduced metabolic rate of P. minutus‐ infected G. roeseli (Lukacsovics 1959, in Jacquin et al . ).…”

“…; Jacquin et al . ). This suggests that the parasite may mimic anaerobic conditions in its amphipod host.…”