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

Abstract

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.

Infection with cerebral metacercariae of microphallid trematode parasites reduces reproductive output in the gammarid amphipodGammarus insensibilis(Stock 1966) in UK saline lagoons

“…Aberrant escape behaviour occurs in response to disturbance (Ottaviani & Franceschi, 1996). Arnal et al (2015) reported greatest activity by infected G. insensibilis in the presence of fish slime and bird faeces, both associated with potential definitive hosts. In the current study disturbance was minimal in the laboratory assay so activity may be reduced in the infected animals.…”

“…Therefore the effects of trematode infection on reproduction were probably initiated prior to the release of eggs into the marsupium, perhaps because of reduced energy to allocate to reproduction. Increased activity by hosts generated by manipulative parasites (Arnal et al ., 2015), melanization and encapsulation responses induced following infection (Kostadinova & Mavrodieva, 2005b) and wounding and haemolymph loss through penetration of the abdomen by cercariae (Fredensborg et al ., 2004) are probably energetically costly, reducing resources available for reproduction.…”

“…The cercariae enter through the abdomen of the amphipod and encyst in the head, as cerebral metacercariae. Microphallus papillorobustus manipulates the behaviour of G. insensibilis , inducing positive phototaxis, negative geotaxis and aberrant evasive behaviour when disturbed, thereby increasing vulnerability to predation by the charadriiform avian definitive host (Helluy, 1984; Thomas et al ., 1996b; Brown et al ., 2003; Arnal et al ., 2015). Behavioural modification only occurs when animals are infected by cerebral metacercariae, not when metacercariae are only located in the abdomen.…”

Few studies of wild animal performance account for parasite infections: A systematic review

“…The effects of parasites on host behaviour are similarly difficult to generalize. Parasite infection is related to both increased and decreased grouping behaviours (Arnal et al, 2015; Barber & Huntingford, 1995; Krause & Godin, 1994; Spagnoli et al, 2015), foraging (Barber et al, 2000; Meadows & Meadows, 2003), movement (reviewed in Binning et al, 2017) and activity (Arnal et al, 2015; Binning et al, 2017). As a result, ignoring parasite infection in studies of host performance can lead to biases, misinterpretations and erroneous conclusions that can be impossible to account for post‐hoc (Timi & Poulin, 2020).…”

Few studies of wild animal performance account for parasite infections: a systematic review

“…The effects of parasites on host behaviour are similarly difficult to generalize. Parasite infection is related to both increased and decreased grouping behaviours (Arnal et al, 2015;Barber & Huntingford, 1995;Krause & Godin, 1994;Spagnoli et al, 2015), foraging (Barber et al, 2000;Meadows & Meadows, 2003), movement (reviewed in Binning et al, 2017), and activity (Arnal et al, 2015;Binning et al, 2017). As a result, ignoring parasite infection in studies of host performance can lead to biases, misinterpretations and erroneous conclusions that can be impossible to account for post-hoc (Timi & Poulin, 2020).…”