Pomphorhynchus laevis manipulates Gammarus pulex behaviour despite salt pollution

Abstract

Salt pollution of freshwater ecosystems represents a major threat to biodiversity, and particularly to interactions between free‐living species and their associated parasites. Acanthocephalan parasites are able to alter their intermediate host's phenotype to reach final hosts, but this process could be affected by salt pollution, thereby compromising survival of the parasite. We experimentally assessed the impact of salt on the extended phenotype of the parasite Pomphorhynchus laevis in their intermediate host, the amphipod Gammarus pulex, based on three amphipod behaviours: distance covered in flowing water, phototaxis, and geotaxis. We hypothesised that: (1) salt pollution negatively affected the behaviour of uninfected gammarids, and (2) that P. laevis could maintain their capacity to manipulate their host despite this pollution. All three amphipod behaviours were altered by P. laevis: infected G. pulex covered a greater distance, were less photophobic and were more attracted to the water surface than uninfected amphipods, in control or salt‐polluted water. However, salinity reduced distance covered in flowing water and increased attraction to the water surface of uninfected and infected G. pulex. For the phototaxis behaviour, P. laevis enhanced this capacity of manipulation in salt‐polluted water compared to control water. Pomphorhynchus laevis can still manipulate the behaviour of their intermediate host in salt‐polluted water. Acanthocephalan parasites have not been known to be able to manipulate their intermediate host when under pollution stress. Trophic interactions, but not the chances of parasite transmission to their definitive host, appear to be affected by salt pollution. Our study indicates that behavioural modifications induced by complex lifecycle parasites should be more considered in the context of growing concentrations of chemical pollutants in some freshwater ecosystems. Interspecific interactions, and particularly host–parasite relationships, are a key component of ecosystem stability and their alteration could result in major changes in energy flow.

Effects of multiple stressors in fish: how parasites and contaminants interact

“…It is known that parasites are also successfully transferred to the next host in polluted environments through host manipulation (e.g. Fanton et al ., 2020 ). However, there is not much research studies on changes in host behaviour under pollution conditions and how this affects the transmission efficiency of parasites.…”

Acanthocephalan parasites reflect ecological status of freshwater ecosystem

“…Following the "increased host abilities" of Médoc and Beisel (2008), acanthocephalan parasite could improve its survival until transmission through increasing the ability of its intermediate host. Additionally, infection by acanthocephalan parasites could be temporarily beneficial to their hosts in a polluted environment (Fanton et al, 2020;Molbert et al, 2020).…”

“…For example, S. cephalus individuals infected by P. laevis were shown to exhibit lower oxidative damage compared to uninfected ones under polluted conditions (Molbert et al, 2020). Moreover, in a heavily polluted environment, P. laevis still manipulates the behaviour of its intermediate host (Fanton et al, 2020). During infection, acanthocephalans could slightly promote their definitive and, to a lesser extent their intermediate hosts" tolerance to polluted conditions.…”

“…There is growing interest in the effects of pollution on freshwater parasites (Lafferty 1997;Marcogliese 2005;Sures et al, 2017;Grabner and Sures 2020;Fanton et al, 2020;Duarte et al, 2020). Acanthocephalans could provide a clear picture of ecosystem composition by reflecting the presence and the viability of their intermediate, definitive and paratenic host populations (Marcogliese and Cone 1997).…”