When trophically‐transmitted parasites combine predation enhancement with predation suppression to optimize their transmission

Médoc, Vincent; Beisel, Jean‐Nicolas

doi:10.1111/j.1600-0706.2011.19585.x

Cited by 28 publications

(28 citation statements)

References 56 publications

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“…Whether or not an individual experiences autoimmune or allergic diseases in a hygienic environment is likely to depend on factors that include host genotype, the severity of infection (e.g. how many parasites an individual is infected with), interactions between the host microbiome and helminth parasites, interactions between multiple helminth species infecting the same host, and whether or not infection happens early or late in life (Maizels & Nussey, 2013;Maizels, McSorley, & Smyth, 2014;McKay, 2009;Zaiss et al, 2015). These complexities make studying the importance of evolved dependence of host behaviour on parasites a potentially daunting task, but unravelling this complexity will yield a more ecologically relevant understanding of host behaviour.…”

Section: Introductionmentioning

confidence: 99%

Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Weinersmith

Earley

2016

Animal Behaviour

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Interest in how parasites shape host behaviour has increased dramatically in recent years. The main focus of behavioural ecologists has been on the negative effects of parasites on host behaviour. However, there are instances in which infected hosts express more adaptive behavioural phenotypes and have higher fitness relative to uninfected hosts, suggesting that it is sometimes beneficial to be parasitized. For example, hosts can exhibit evolved dependence, wherein the host coevolves with and comes to depend on parasites for the expression of adaptive host behaviours. Additionally, 'conditionally helpful parasites' modify the host phenotype in ways that benefit the host under particular conditions. These scenarios have been explored in the context of bacterial or fungal symbionts, but have been relatively unstudied with regard to metazoan parasites (e.g. trematodes, acanthocephalans, nematodes and cestodes). We explore how these scenarios apply to hosts infected by metazoan parasites, and consider implications for research in behavioural ecology. We examine conditions under which infection should result in more adaptive host behavioural phenotypes, and the implications for host fitness and evolution. We then discuss the implications of conditionally helpful parasites and parasites for which hosts have evolved dependence for laboratory studies of host behaviour and for conservation and reintroduction programmes.

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Section: Introductionmentioning

confidence: 99%

Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Weinersmith

Earley

2016

Animal Behaviour

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“…This might be achieved by increasing the vulnerability of intermediate hosts to predation by final hosts, decreasing their vulnerability to predation by non hosts, or both [15]. In the third case, the manipulation shows a high degree of specificity through the combination of predation enhancement and predation suppression [16]. Under the assumption of a highly specific manipulation, it is expected that manipulated intermediate hosts behave differently depending on whether the predator is a definitive host or a non host.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2014

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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.

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“…They can be infected by several parasites such as nematodes, trematodes [14], [15], microsporidia [5], [16]–[18] or acanthocephalans [19]–[22].…”

Section: Introductionmentioning

confidence: 99%

Polymorphus Minutus Affects Antitoxic Responses of Gammarus Roeseli Exposed to Cadmium

2012

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The acanthocephalan parasite Polymorphus minutus is a manipulator of its intermediate host Gammarus roeseli, which favours its transmission to the final host, a water bird. In contaminated environments, G. roeseli have to cope with two stresses, i.e. P. minutus infection and pollutants. As P. minutus survival relies on its host's survival, we investigated the influence of P. minutus on the antitoxic defence capacities and the energy reserves of G. roeseli females after cadmium exposure. In parallel, malondialdehyde, a toxic effect biomarker, was measured in G. roeseli females and in P. minutus. The results revealed that infected females displayed higher cell damage than uninfected ones, despite an apparent increase in reduced glutathione and metallothionein production. In fact, the increase of these antitoxic systems could be counterbalanced by carotenoid intake by the parasite, so that the overall defence system seemed less efficient in infected females than in uninfected ones. In addition, we demonstrated that cadmium induced cell damage in P. minutus, probably linked with cadmium accumulation in the parasite. Altogether, we observed a paradoxical pattern of responses suggesting that P. minutus increases cadmium toxicity in G. roeseli females although (i) it tends to increase several host antitoxic defence capacities and (ii) it bears part of the pollutant, as reflected by cell damage in the parasite.

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When trophically‐transmitted parasites combine predation enhancement with predation suppression to optimize their transmission

Cited by 28 publications

References 56 publications

Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

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

Polymorphus Minutus Affects Antitoxic Responses of Gammarus Roeseli Exposed to Cadmium

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