Does the acanthocephalan parasite Polymorphus minutus modify the energy reserves and antitoxic defences of its intermediate host Gammarus roeseli?

Abstract

S U M M A R YIn disturbed environments, infected organisms have to face both parasitic and chemical stresses. Although this situation is common, few studies have been devoted to the effects of infection on hosts' energy reserves and antitoxic defence capacities, while parasite survival depends on host survival. In this study, we tested the consequences of an infection by Polymorphus minutus on the energy reserves (protein, lipid and glycogen) and antioxidant defence capacities (reduced glutathione, γ-glutamylcysteine ligase activity) of Gammarus roeseli males and females, in the absence of chemical stress. Moreover, malondialdehyde concentration was used as a toxicity biomarker. The results revealed that in infected G. roeseli, whatever their gender and the sampling month, protein and lipid contents were lower, but glycogen contents were higher. This could be explained by the fact that the parasite diverts part of the host's energy for its own development. Moreover, glutathione concentrations and γ-glutamylcysteine ligase activity were both lower, which could lead to lower antitoxic defence in the host. These results suggest negative effects on individuals in the case of additional stress (e.g. pollutant exposure). In the absence of chemical stress, the lower malondialdehyde level in infected gammarids could imply a probable protective effect of the parasite.

Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology’

“…Markers of energy metabolism such as total lipid and glycogen content were also shown to be differentially modulated by parasitism. Although no effect on glycogen levels due to Cd exposure were detected in uninfected gammarids, infection with microsporidians led to higher glycogen concentrations [ 62 , 63 ]. Levels of heat-shock proteins (HSP) as indication of a general stress response in organisms are usually increased due to pollutants but may be significantly reduced when exposed gammarids are infected with acanthocephalans [ 58 , 64 ].…”

“…Under polluted conditions the need for detoxification of pollutants can cause increased metabolic activity. Gismondi et al [ 62 ] described an increase of several host antitoxic defence capacities in P. minutus -infected G. roeseli females following cadmium toxicity although infection increases cadmium toxicity in G. roeseli females.…”

Effects of the acanthocephalanPolymorphus minutusand the microsporidianDictyocoela duebenumon energy reserves and stress response of cadmium exposedGammarus fossarum

“…Parasites are natural and ubiquitous parts of ecosystems and their role for ecosystem function and stability has been recognized in recent years ( Marcogliese, 2005 ; Hudson, Dobson & Lafferty, 2006 ; Kuris et al, 2008 ). Nevertheless, parasites are often neglected in ecotoxicological research, although results of recent studies showed that they may influence the host response to pollution ( Sures, 2004 ; Sures, 2008a ; Sures, 2008b ; Marcogliese & Giamberini, 2013 ) and can impact the stress response of their host, especially on the biochemical level ( Sures, Lutz & Kloas, 2006 ; Sures & Radszuweit, 2007 ; Frank et al, 2011 ; Frank et al, 2013 ; Gismondi, Cossu-Leguille & Beisel, 2012a ; Gismondi et al, 2012a ; Gismondi et al, 2012b ; Filipović Marijić, Vardić Smrzlić & Raspor, 2013 ; Grabner, Schertzinger & Sures, 2014 ). Such impacts are particularly relevant when using stress responses on the biochemical level as biomarkers in environmental monitoring programs to indicate the presence of contaminants and to unravel their effects on organisms.…”

“…For example, they can influence the activity of the host and its predator avoidance behavior ( Bauer et al, 2000 ; MacNeil et al, 2003a ; MacNeil et al, 2003b ; Benesh et al, 2008 ) or affect its reproduction rates ( Ward, 1986 ; Zohar & Holmes, 1998 ; Bollache, Gambade & Cézilly, 2001 ). Furthermore, acanthocephalans can influence the energy metabolism of the host and its vulnerability to metals ( Gismondi, Cossu-Leguille & Beisel, 2012a ; Gismondi, Cossu-Leguille & Beisel, 2012b ; Gismondi, Beisel & Cossu-Leguille, 2012b ).…”

Correlations between estrogen and testosterone concentrations, pairing status and acanthocephalan infection in an amphipod

“…In amphipods, acanthocephalan infection is correlated with modified phototaxis, geotaxis, clinging, drift and response to environmental stressors (e.g. Kaldonski, Perrot‐Minnot & Cézilly, ; Sures & Radszuweit, ; Gismondi, Cossu‐Leguille & Beisel, ,b; Lafferty & Shaw, ). Moreover, infection by some acanthocephalans is correlated with reduced reproductive success of male or female amphipods (e.g.…”