How much energy should manipulative parasites leave to their hosts to ensure altered behaviours?

Maure, Fanny; Brodeur, Jacques; Hughes, David; Thomas, Frédéric

doi:10.1242/jeb.073163

Cited by 20 publications

(22 citation statements)

References 25 publications

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“…This type of mechanism could explain the intensity-related effect on behavior modification identified in the current study if both host sharing and host manipulation are costly to the A. dirus parasites. Consistent with this type of hypothesis, costs of both host sharing and manipulation have been identified (e.g., Dezfuli et al 2001;Maure et al 2013). We are currently examining the potential importance of this type of mechanism in the A. dirus-C. intermedius relationship.…”

Section: Discussionmentioning

confidence: 66%

Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition?

2014

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The acanthocephalan parasite Acanthocephalus dirus infects the freshwater isopod Caecidotea intermedius as an intermediate host before completing its life cycle in a fish. Male C. intermedius infected by A. dirus parasites are less likely to engage in mating behavior than uninfected males but there is a significant intra-population variation in the occurrence of this behavioral change. Previous studies on uninfected isopods have shown that glycogen content is a predictor of male mating behavior and we examined whether the intra-population variation in the mating behavior of infected male C. intermedius could be explained by this relationship. A field-based behavioral experiment was used to quantify intra-population variation in male mating behavior, which showed that 50% of infected males were responsive to females and 50% were not responsive. Biochemical analysis of responsive and non-responsive males revealed that glycogen content was a predictor of the mating behavior for uninfected males but was not a predictor of mating behavior for infected males. For infected males, parasite intensity was a predictor of mating behavior. Males that contained more A. dirus parasites were less likely to undergo modification of mating behavior. We propose that the intra-population variation in the mating behavior of infected C. intermedius identified in nature was not mediated by host condition.

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Section: Discussionmentioning

confidence: 66%

Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition?

2014

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“…One possible explanation for this finding is that the energy required by the host to accomplish a parasite-induced behavior such as the maintenance of aberrant surfacing behaviors represents a key energetic constraint (Maure et al, 2013). Manipulative parasites therefore have to "budget" for such costs when optimizing the exploitation of host resources as they develop Lefèvre et al, 2008;Poulin, 2010).…”

Section: Resultsmentioning

confidence: 99%

Activity level and aggregation behavior in the crustacean gammarid Gammarus insensibilis parasitized by the manipulative trematode Microphallus papillorobustus

et al. 2015

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Hosts manipulated by parasites are profoundly altered organisms exhibiting a broad range of potential modifications. Exploring this multidimensionality is an emerging field. Previous studies have shown that the bird trematode Microphallus papillorobustus induces several behavioral changes in the gammarid Gammarus insensibilis. Knowing that aggregation behavior and reduced activity levels are strategies that limit predation in other species of amphipods, we explored in this study these behavioral responses for infected and uninfected G. insensibilis in the presence of host and non-host predator olfactory cues (bird feces and fish mucus). While uninfected individuals reduced their activity level in the presence of predator cues, infected individuals did not change their activity level in presence of aquatic bird feces. We also studied the gammarid aggregation behavior. Uninfected gammarids in clean water spent significantly more time in aggregates than did infected individuals. Among the uninfected individuals, the aggregation level tended to increase when bird feces and fish mucus were added, but the difference was not significant. Among infected individuals, the level of aggregation was significantly increased only with the bird feces. We discussed our results in the context of the literature on multidimensional manipulations, acknowledging that subtle differences between unparasitized and parasitized gammarids can also be by-products of manipulation on other traits.

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“…Numerous studies have shown that host sharing can impact parasite development, growth, body size, and energy content, and that each of these factors has the potential to influence trait modification (Read and Phifer, 1959;Roberts, 2000;Dezfuli et al, 2001;Sparkes et al, 2004Sparkes et al, , 2006Benesh and Valtonen, 2007a;Franceschi et al, 2008Franceschi et al, , 2010Benesh et al, 2009a;Dianne et al, 2010Dianne et al, , 2012Caddigan et al, 2014Caddigan et al, , 2017. If competitive interactions among parasites influence the patterns of development, growth, and energy allocation, and if manipulation is costly, then parasites may benefit by adopting strategies that balance the conflicting demands associated with their own growth, and development with those that are associated with host manipulation (e.g., Poulin, 1994a;Parker et al, 2003;Thomas et al, 2005Thomas et al, , 2011Michaud et al, 2006;Ball et al, 2008;Franceschi et al, 2010;Maure et al, 2013). Consistent with this type of mechanism, infection of an aquatic isopod by an acanthocephalan parasite is associated with decreases in both parasite energy content, and modification of host behavior (mating) at higher intensities of infection (Caddigan et al, 2014(Caddigan et al, , 2017.…”

Section: Introductionmentioning

confidence: 99%

Multidimensionality of Modification in an Isopod-Acanthocephalan System

Park

Sparkes

2017

Front. Ecol. Evol.

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The acanthocephalan parasite Acanthocephalus dirus infects the freshwater isopod Caecidotea intermedius as an intermediate host before completing its life cycle in a fish. Transmission to the definitive host occurs after the parasite has reached the cystacanth stage and development into this stage is associated with changes in several behavioral and physiological traits of the host. Despite the numerous examples of trait modification in this system, little is known about the multidimensional nature of this modification. Here, we examined the relationships between cystacanth infection, and expression of multiple traits (body color, refuge use, activity, and body size) of both male and female C. intermedius. The pattern of multidimensional modification was determined for males and females and then measures of behavioral plasticity, individual consistency, and trait correlations were obtained for the modified traits. The results revealed that the overall pattern of host modification differed between males and females. Infected males and females showed similar decreases in body color but differed in changes to the other traits. Infected females were larger and less active than uninfected females, whereas infected males spent less time in refuge than uninfected males. A comparison between two situations revealed that refuge use exhibited high levels of plasticity and activity exhibited high levels of consistency and that these patterns differed based on both host sex and infection status. Analysis of the relationships among modified traits showed that traits appeared to be modified independently of each other and that correlations between traits that existed in one situation were absent in another. We suggest that the pattern of multidimensional modification is sex-specific and that the traits are modified independently. We also show that the patterns of multidimensional modification were not associated with variation in either parasite intensity of parasite size indicting that competitive interactions among parasites did not appear to act as a constraint on host modification.

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How much energy should manipulative parasites leave to their hosts to ensure altered behaviours?

Cited by 20 publications

References 25 publications

Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition?

Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition?

Activity level and aggregation behavior in the crustacean gammarid Gammarus insensibilis parasitized by the manipulative trematode Microphallus papillorobustus

Multidimensionality of Modification in an Isopod-Acanthocephalan System

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