Effects ofMicrophallus papillorobustus(Platyhelminthes: Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain ofGammarus insensibilis(Crustacea: Amphipoda)

Abstract

The larval flatworm Microphallus papillorobustus encysts in the protocerebrum of its intermediate host, Gammarus insensibilis, and changes the gammarid's responses to mechanical and photic stimuli. The resulting aberrant escape behaviour renders infected gammarids more susceptible to predation by birds, the definitive hosts of the parasite. We used immunocytochemical methods to explore the mechanisms underlying these subtle behavioural modifications. Whole mounts of gammarid brains were labelled with fluorescent anti-serotonin and anti-synapsin antibodies and viewed using confocal microscopy. Two types of change were observed in infected brains: the intensity of the serotonergic label was altered in specific regions of the brain, and the architecture of some serotonergic tracts and neurons was affected. A morphometric analysis of the distribution of the label showed that serotonergic immunoreactivity was decreased significantly (by 62%) in the optic neuropils, but not in the olfactory lobes, in the presence of the parasite. In addition, the optic tracts and the tritocerebral giant neurons were stunted in parasitized individuals. Published evidence demonstrates changes in serotonin levels in hosts ranging from crustaceans to mammals infected by parasites as diverse as protozoans and helminths. The present study suggests that the degeneration of discrete sets of serotonergic neurons might underlie the serotonergic imbalance and thus contribute to host manipulation.

The effects of toxoplasma infection on rodent behavior are dependent on dose of the stimulus

“…If the flatworm manages to infect the cerebral region, it results in aberrant photic and mechanical response of the host (Helluy, 1983, Helluy andThomas, 2003). This makes the intermediate host more vulnerable to predation by birds, which are the definitive hosts for the parasite (Helluy, 1984, Helluy andThomas, 2003). Interestingly, parasites that enter the brain have higher mortality rates than those that remain in the abdomen and hence do not take active part in behavioral manipulation (Thomas et al, 2000).…”

“…For example, the flatworm Microphallus papillorobustus infects amphipod Gammarus spp. If the flatworm manages to infect the cerebral region, it results in aberrant photic and mechanical response of the host (Helluy, 1983, Helluy andThomas, 2003). This makes the intermediate host more vulnerable to predation by birds, which are the definitive hosts for the parasite (Helluy, 1984, Helluy andThomas, 2003).…”

Parasite manipulation of brain monoamines in California killifish ( Fundulus parvipinnis ) by the trematode Euhaplorchis californiensis

“…The manipulation of invertebrate hosts involves parasitesecreted molecules (Beckage 1993;de Jong-Brink et al 2001;Biron et al 2005), and neuroanatomical and monoaminergic disruption (Adamo & Shoemaker 2000;Helluy & Thomas 2003;Thomas et al 2003;Rojas & Ojeda 2005;Tain et al 2006), including reduced activity of monoaminergic neurons (Rosenberg et al 2006). There are fewer studies on vertebrates (see Klein (2003) for a review).…”

Impacts of a newly identified behaviour-altering trematode on its host amphipod: from the level of gene expression to population

“…Furthermore, a better understanding of the pathways from genes to phenotypes will increase our knowledge of the mechanistic basis of animal behaviour. Amphipods clearly represent one of the best animal groups for the study of parasiteinduced behavioural manipulation (Bethel and Holmes, 1973;Helluy, 1983aHelluy, , b, 2013Helluy and Holmes, 1990;Cezilly et al 2000;Helluy and Thomas, 2003;Damsgaard et al 2005;Kostadinova and Mavrodieva, 2005;Ponton et al 2005Ponton et al , 2006Leung and Poulin, 2006;Tain et al 2007). However, in comparison with well-established model arthropod species, investigations using amphipods have been hampered by a lack of genomic resources and an inability to apply transgenic technologies.…”

“…Furthermore, components of the serotonin pathway have been implicated by experiments demonstrating that injection of serotonin, a monoamine neurotransmitter, into gammarids causesbehaviours similar to that induced by manipulating parasites (Helluy and Holmes, 1990;Tain et al 2006;Perrot-Minnot et al 2014), while other neurotransmitters at similar concentrations, failed to induce a comparable response (Helluy and Holmes, 1990). In addition, it has been shown that once M. papillorobustus metacercariae encyst in the cerebral ganglia, specifically the protocerebrum responsible for all visual sensory input Helluy and Thomas, 2003;Kostadinova and Mavrodieva, 2005), serotonin levels become altered in specific regions, with a decrease of 62% observed in the optic neuropils (Ponton et al 2006), a decrease thought to be due to the degeneration of discrete sets of serotonergic neurons. Consistent with studies implicating serotonin related pathways, positive phototaxic and negative geotaxic behavioural changes have been observed in E. marinus exposed to serotonin and the selective serotonin reuptake inhibitor (SSRI) fluoxetine (Guler and Ford, 2010).…”