Contrasting alterations in brain chemistry in a crustacean intermediate host of two acanthocephalan parasites

Abstract

The dynamic properties of neural systems throughout life can be hijacked by so-called manipulative parasites. This study investigated changes in the brain chemistry of the amphipod Gammarus fossarum in response to infection with two trophically-transmitted helminth parasites known to induce distinct behavioral alterations: the bird acanthocephalan Polymorphus minutus and the fish acanthocephalan Pomphorhynchus tereticollis. We quantified brain antioxidant capacity as a common marker of homeostasis and neuroprotection, and brain total protein, on 72 pools of six brains. We analyzed the concentration of serotonin (5HT), dopamine (DA) and tyramine in 52 pools of six brains, by using ultrafast high performance liquid chromatography with electrochemical detection (UHPLC-ECD). Brain total protein concentration scaled hypo-allometrically to dry body weight, and was increased in infected gammarids compared to uninfected ones. The brain of gammarids infected with P. minutus had significantly lower total antioxidant capacity relative to total proteins. Infection with P. tereticollis impacted DA level compared to uninfected ones, and in opposite direction between spring and summer. Brain 5HT level was higher in summer compared to spring independently of infection status, and was decreased by infection after correcting for brain total protein concentration estimated from dry whole-body weight. The potential implication of 5HT/DA balance in parasite manipulation, as a major modulator of the reward-punishment axis, is discussed. Taken together, these findings highlight the need to consider both brain homeostatic and/or structural changes (antioxidant and total protein content) together with neurotransmission balance and flexibility, in studies investigating the impact of parasites on brain and behavior.