Ecology of parasitically modified populations: a case study from a gammarid-trematode system

Abstract

Examples of behavioural manipulation by parasites are numerous but the consequences of these phenomena on the ecology of host populations remains unclear. Through its effect on Gammarus insensibilis behaviour, the salt marsh trematode Microphallus papillorobustus splits its host population into 2 discrete subunits, one living at the surface (infected individuals) and the other living near the bottom (uninfected individuals). Here, we compare several biological characteristics of gammarids from these 2 spatially segregated subunits. Infected females were smaller and thus less fecund than uninfected females. They also had a longer intermoult duration. The mean body size of infected and uninfected males was not significantly different. However, energy reserves were significantly different: infected males possessed higher glycogen and lipid contents and lower glucose content compared to uninfected males. Interestingly, uninfected males living at the surface (those paired with infected females) also displayed higher energy reserves compared to uninfected conspecifics living in the bottom subunit (those paired with uninfected females). In both of the 2 subunits, there was no significant relationship between male sexual performance (measured through the size of their partner) and their levels of energy reserves. The pattern of size-assortative pairing was not significantly different between pairs from the surface and from the bottom, but male sexual performances were on average smaller for males from the surface subunit. Our results also indicated that the benefits of preferring large more fecund females are however likely to be counterbalanced by the higher mortality rate of these females compared to smaller ones during the subsequent intermoult. Because such a phenomenon directly influences the number of juveniles produced, it reduces the inequalities between the true sexual performances (i.e. number of descendants) achieved by males from the surface and from the bottom. This study supports the idea that infected gammarids are not simply normal hosts with an aberrant behaviour, they are more deeply modified in ways that may substantially alter host population ecology.

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

“…It is increasingly recognized that manipulative parasites alter several phenotypic traits in their hosts, these alterations occurring simultaneously and/or successively (Thomas et al, 2010). For example, several bird helminths (trematodes, acanthocephalans and cestodes) parasitizing crustaceans from the genus Gammarus and Artemia, in addition to modifying the behaviour of their host, are able to increase the host's level of energetic resources (glycogen and especially lipids) (Amat et al, 1991;Plaistow et al, 2001;Ponton et al, 2005). Although experimental evidence is still lacking, these findings suggest that these parasites physiologically manipulate their hosts in a way that will compensate for the energetic expenditures associated with manipulated behaviours.…”

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.…”

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

“…Infected individuals were identified in the field through the aberrant surface behavior induced by M. papillorobustus (Helluy, 1981;Ponton et al, 2005). From our long field experience (20 years), we know that all gammarids collected at the surface with an aberrant behavior harbor at least one mature cyst of M. papillorobustus, while those collected at the bottom are either non-parasitized or infected by immature metacercariae.…”

“…M. papillorobustus metacercariae are always encysted in the brain (protocerebrum) of G. insensibilis and induce strong behavioral and physiological alterations in this host, i.e., positive phototaxis, negative geotaxis, aberrant evasive behavior, and higher lipid content (Helluy, 1981(Helluy, , 1984Ponton et al, 2005). Infected gammarids typically live at the surface of the water while uninfected ones inhabit the bottom (Helluy, 1981;Ponton et al, 2005). It is thought that these multiple behavioral changes increase the vulnerability of gammarids to predation by aquatic birds and therefore promote parasite transmission (Helluy, 1984).…”

“…This salt marsh trematode has a complex life cycle that includes snails from the genus Hydrobia as the first intermediate host, gammaridean amphipods as the second intermediate host, and various aquatic birds as definitive hosts (order Charadriiformes; Rebecq, 1964). M. papillorobustus metacercariae are always encysted in the brain (protocerebrum) of G. insensibilis and induce strong behavioral and physiological alterations in this host, i.e., positive phototaxis, negative geotaxis, aberrant evasive behavior, and higher lipid content (Helluy, 1981(Helluy, , 1984Ponton et al, 2005). Infected gammarids typically live at the surface of the water while uninfected ones inhabit the bottom (Helluy, 1981;Ponton et al, 2005).…”