Is the host or the parasite the most locally adapted in an amphipod-acanthocephalan relationship? A case study in a biological invasion context

Manipulative endoparasites with complex life cycles can alter their intermediate host immunity and behaviour in ways that increase survival probability within the host body cavity and enhance successful transmission to the definitive host. These parasitic manipulations are variable among and within parasite species and may result from co-evolutionary processes, in which the parasite is constrained for adaptation to the local intermediate host. Hence, arrival of a new host species in a local host population may promote local parasite maladaptation. This study tested the occurrence of local adaptation in two distantly located populations of the acanthocephalan parasite Pomphorhynchus laevis and its effect on the immunity and behaviour of its gammarid intermediate host Gammarus roeseli. This was done in France (an area for which G. roeseli is a recent invader) and Hungary (an area from which G. roeseli was believed to be native). As expected, we found no alteration in G. roeseli's immune defence and behaviour associated with infection by P. laevis in localities, where the gammarid is invasive. Unexpectedly, we found similar results in Hungarian populations, where the parasite was even more exposed to the host immune response. Whilst these results suggest maladaptation of the parasite to the gammarid in both countries, they also suggest that the gammarid host might be locally adapted to the parasite. Genetic analyses were performed on both the parasite and the host and the results suggest that the two subsets of populations we studied harbour rather isolated host-parasite systems, both probably deriving from a common ancestral population. We propose that G. roeseli is also of recent acquisition in Hungary, and that a recent co-evolutionary history between P. laevis and G. roeseli in association with a long generation time in the parasite has constrained parasite adaptations in Europe or even favoured host adaptation to the parasite.     

An acanthocephalan parasite boosts the escape performance of its intermediate host facing non-host predators

Among the potential effects of parasitism on host condition, the 'increased host abilities' hypothesis is a counterintuitive pattern which might be predicted in complex-life-cycle parasites. In the case of trophic transmission, a parasite increasing its intermediate host's performance facing non-host predators improves its probability of transmission to an adequate, definitive host. In the present study, we investigated the cost of infection with the acanthocephalan Polymorphus minutus on the locomotor/escape performance of its intermediate host, the crustacean Gammarus roeseli. This parasite alters the behaviour of its intermediate host making it more vulnerable to predation by avian definitive hosts. We assessed the swimming speeds of gammarids using a stressful treatment and their escape abilities under predation pressure. Despite the encystment of P. minutus in the abdomen of its intermediate host, infected amphipods had significantly higher swimming speeds than uninfected ones (increases of up to 35%). Furthermore, when interacting with the non-host crustacean predator Dikerogammarus villosus, the highest escape speeds and greatest distances covered by invertebrates were observed for parasitized animals. The altered behaviour observed among the manipulated invertebrates supported the 'increased host abilities' hypothesis, which has until now remained untested experimentally. The tactic of increasing the ability of infected intermediate hosts to evade potential predation attempts by non-host species is discussed.     

Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species

The physiological mechanisms by which parasites with complex life cycles manipulate the behaviour of their intermediate hosts are still poorly understood. In Burgundy, eastern France, the acanthocephalan parasite Pomphorhynchus laevis inverses reaction to light in its amphipod host Gammarus pulex, but not in Gammarus roeseli, a recent invasive species. Here, we show that this difference in manipulation actually reflects a difference in the ability of the parasite to alter brain serotonergic (5-HT) activity of the two host species. Injection of 5-HT in uninfected individuals of both host species was sufficient to inverse reaction to light. However, a difference in brain 5-HT immunocytochemical staining levels between infected and uninfected individuals was observed only in G. pulex. Local adaptation of the parasite to the local host species might explain its inability to manipulate the behaviour and nervous system of the invasive species.     

Polymorphus minutus affects antitoxic responses of gammarus roeseli exposed to cadmium

The acanthocephalan parasite Polymorphus minutus is a manipulator of its intermediate host Gammarus roeseli, which favours its transmission to the final host, a water bird. In contaminated environments, G. roeseli have to cope with two stresses, i.e. P. minutus infection and pollutants. As P. minutus survival relies on its host's survival, we investigated the influence of P. minutus on the antitoxic defence capacities and the energy reserves of G. roeseli females after cadmium exposure. In parallel, malondialdehyde, a toxic effect biomarker, was measured in G. roeseli females and in P. minutus. The results revealed that infected females displayed higher cell damage than uninfected ones, despite an apparent increase in reduced glutathione and metallothionein production. In fact, the increase of these antitoxic systems could be counterbalanced by carotenoid intake by the parasite, so that the overall defence system seemed less efficient in infected females than in uninfected ones. In addition, we demonstrated that cadmium induced cell damage in P. minutus, probably linked with cadmium accumulation in the parasite. Altogether, we observed a paradoxical pattern of responses suggesting that P. minutus increases cadmium toxicity in G. roeseli females although (i) it tends to increase several host antitoxic defence capacities and (ii) it bears part of the pollutant, as reflected by cell damage in the parasite.     

Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation

Manipulation by parasites is a catchy concept that has been applied to a large range of phenotypic alterations brought about by parasites in their hosts. It has, for instance, been suggested that the carotenoid-based colour of acanthocephalan cystacanths is adaptive through increasing the conspicuousness of infected intermediate hosts and, hence, their vulnerability to appropriate final hosts such as fish predators. We revisited the evidence in favour of adaptive coloration of acanthocephalan parasites in relation to increased trophic transmission using the crustacean amphipod Gammarus pulex and two species of acanthocephalans, Pomphorhynchus laevis and Polymorphus minutus. Both species show carotenoid-based colorations, but rely, respectively, on freshwater fish and aquatic bird species as final hosts. In addition, the two parasites differ in the type of behavioural alteration brought to their common intermediate host. Pomphorhynchus laevis reverses negative phototaxis in G. pulex, whereas P. minutus reverses positive geotaxis. In aquaria, trout showed selective predation for P. laevis-infected gammarids, whereas P. minutus-infected ones did not differ from uninfected controls in their vulnerability to predation. We tested for an effect of parasite coloration on increased trophic transmission by painting a yellow-orange spot on the cuticle of uninfected gammarids and by masking the yellow-orange spot of infected individuals with inconspicuous brown paint. To enhance realism, match of colour between painted mimics and true parasite was carefully checked using a spectrometer. We found no evidence for a role of parasite coloration in the increased vulnerability of gammarids to predation by trout. Painted mimics did not differ from control uninfected gammarids in their vulnerability to predation by trout. In addition, covering the place through which the parasite was visible did not reduce the vulnerability of infected gammarids to predation by trout. We discuss alternative evolutionary explanations for the origin and maintenance of carotenoid-based colorations in acanthocephalan parasites.     

Patterns of intermediate host use and levels of association between two conflicting manipulative parasites.

For many parasites with complex life cycles, manipulation of intermediate host phenotypes is often regarded as an adaptation to increase the probability of successful transmission. This phenomenon creates opportunities for either synergistic or conflicting interests between different parasite species sharing the same intermediate host. When more than one manipulative parasite infect the same intermediate host, but differ in their definitive host, selection should favour the establishment of a negative association between these manipulators. Both Polymorphus minutus and Pomphorhynchus laevis exploit the amphipod Gammarus pulex as intermediate host but differ markedly in their final host, a fish for P. laevis and a bird for P. minutus. The pattern of host use by these two conflicting manipulative parasites was studied. Their incidence and intensity of infection and their distribution among G. pulex were first examined by analysing three large samples of gammarids collected from the river Tille, Eastern France. Both parasites had low prevalence in the host population. However, temporal fluctuation in the level of parasitic infection was observed. Overall, prevalence of both parasite species was higher in male than in female G. pulex. We then assessed the degree of association between the two parasites among their intermediate hosts, using two different methods: a host-centred measure and a parasite-centred measure. Both measures gave similar results; showing random association between the two acanthocephalan species in their intermediate hosts. We discuss our results in relation to the selective forces and ecological constraints that may determine the pattern of association between conflicting manipulative parasites.     

Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission?

Trophically transmitted parasites often alter their intermediate host's phenotype, thereby predisposing the hosts to increased predation. This is generally considered a parasite strategy evolved to enhance transmission to the next hosts. However, the adaptive value of host manipulation is not clear as it may be associated with costs, such as increased susceptibility to predators that are unsuitable next hosts for the parasites. We examined the ratio between the benefits and costs of host manipulation for transmission success of Acanthocephalus lucii (Acanthocephala), a parasite that alters the hiding behaviour and pigmentation of its isopod hosts. We experimentally compared the susceptibility of infected and uninfected isopods to predation by perch (Perca fluvialis; definitive host of the parasite) and dragonfly larvae (dead end). We found that the parasite predisposed the isopods to predation by both predators. However, the increased predation vulnerability of the infected isopods was higher towards perch. This suggests that, despite the costs due to non-host predation, host manipulation may still be advantageous for the parasite.     

Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odours

Many parasites with complex life cycles increase the chances of reaching a final host by adapting strategies to manipulate their intermediate host's appearance, condition or behaviour. The acanthocephalan parasite Pomphorhynchus laevis uses freshwater amphipods as intermediate hosts before reaching sexual maturity in predatory fish. We performed a series of choice experiments with infected and uninfected Gammarus pulex in order to distinguish between the effects of visual and olfactory predator cues on parasite-induced changes in host behaviour. When both visual and olfactory cues, as well as only olfactory cues were offered, infected and uninfected G. pulex showed significantly different preferences for the predator or the non-predator side. Uninfected individuals significantly avoided predator odours while infected individuals significantly preferred the side with predator odours. When only visual contact with a predator was allowed, infected and uninfected gammarids behaved similarly and had no significant preference. Thus, we believe we show for the first time that P. laevis increases its chance to reach a final host by olfactory-triggered manipulation of the anti-predator behaviour of its intermediate host.     

Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda)

Because resistance to parasites usually has a cost for host species, it is theoretically expected that, in case of multi-infection, host immune responses should vary according to the levels of parasite pathogenicity. The crustacean gammarid Gammarus aequicauda is the second intermediate host of 4 trematode species. Three of these parasites always encyst in the abdomen of gammarids and have no particular effect on the host. However, 1 of these species is sometimes able to encyst in the cerebroid ganglia of the gammarid and strongly alter its behavior in a way that increases its predation risk by aquatic birds, the definitive hosts. In accordance with the hypothesis that the level of parasite pathogenicity influences the likelihood and the degree of host reaction, cases of melanization in our gammarid collection almost exclusively concern the cerebral metacercariae. Our results also indicate that this melanization is able to cancel the behavioral alterations induced by the parasite, suggesting that the cause of the manipulation is not the physical presence of metacercariae in the brain.     

Carotenoids of two freshwater amphipod species (Gammarus pulex and G. roeseli) and their common acanthocephalan parasite Polymorphus minutus

Carotenoid compositions of two freshwater Gammarus species (Crustacea: Amphipoda) and of their common acanthocephalan parasite Polymorphus minutus were characterized. The effect of carotenoid uptake by the parasite was addressed by comparing the carotenoid content of uninfected and infected female hosts. Using high-pressure liquid chromatography (HPLC), co-chromatography of reference pigments and electron ionization mass spectrometry of collected HPLC fractions (EI-MS), several xanthophylls and non-polar compounds were identified. Seven kinds of carotenoids, mainly xanthophylls, were identified in gammarids. Astaxanthin was predominant, amounting to 40 wt.% of total carotenoid in both uninfected G. pulex and G. roeseli. By contrast, we found only non-polar compounds with a predominance of esterified forms of astaxanthin in P. minutus larvae. No significant effect of infection on carotenoid content was evidenced in G. pulex and G. roeseli females. Our study highlights the use of a Matrix Solid Phase Dispersion as an efficient extraction method of both xanthophylls and non-polar pigments in small samples, including lipid-rich ones as P. minutus parasite. We discuss on the presumptive pathway leading to the formation of free astaxanthin in gammarids via hydroxy compounds, and on the accumulation of esters of astaxanthin in parasites.     

Identification of a host-associated species complex using molecular and morphometric analyses,with the description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae,Monogenea)

Gyrodactylus rugiensis was originally described as a parasite occurring on the marine gobies Pomatoschistus minutus and Pomatoschistus microps. In our preliminary survey this species was also frequently found on Pomatoschistus pictus and Pomatoschistus lozanoi. Subsequent molecular analysis of the internal transcribed spacers rDNA region revealed that this parasite actually represents a complex of two apparently cryptic species, one restricted to P. microps and the other shared by P. minutus, P. lozanoi and P. pictus. Morphometric analyses were conducted on 17 features of the opisthaptoral hard parts of specimens collected from all four host species. Standard discriminant analysis showed a clear separation of both genotypes by significant differences in marginal hook and ventral bar features. Statistical classifiers (linear discriminant analysis and nearest neighbours) resulted in an estimated misclassification rate of 4.7 and 3.1%, respectively. Based on molecular, morphological and statistical analyses a new species, Gyrodactylus rugiensoides is described. This species seems to display a lower host-specificity than generally observed for Gyrodactylus species as it infects three sympatric host species.However, seasonal and host-dependent morphometric variation is shown for G. rugiensoides collected on P. pictus. Host-switching and gene flow might be important factors preventing speciation on closely related and sympatric host species. The presence of host associated species complexes in this Gyrodactylus-Pomatoschistus system is also confirmed by the presence of two host-dependent genotypes within G. micropsi found on P. minutus and P. lozanoi, and P. microps, respectively. By comparing host and parasite phylogeny, phylogenetic and ecological factors influencing host-specificity are discussed.     

Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod

According to the 'parasitic manipulation hypothesis', phenotypic changes induced by parasites in their intermediate hosts are effective means of increasing trophic transmission to final hosts. One obvious prediction, although seldom tested, is that increased vulnerability of infected prey to an appropriate predator should be achieved by the parasite altering the anti-predator behaviour of its intermediate host. In this study, we tested this prediction using the fish acanthocephalan Pomphorhynchus tereticollis and the freshwater amphipod Gammarus pulex. Firstly, we estimated the relative vulnerability of infected and uninfected gammarids to predation by the bullhead Cottus gobio in the field. Second, we investigated under experimental conditions how two common anti-predator behaviours of aquatic invertebrates, refuge use and short-distance reaction to predator chemical cues, were affected by infection status. We found that the prevalence of infection in the field was 10 times higher among gammarids collected from the stomach contents of bullheads compared with free-ranging individuals collected in the same river. In a microcosm uninfected gammarids, but not infected ones, increased the use of refuge in the presence of a bullhead. Finally, a behavioural experiment using an Y-maze olfactometer showed opposite reactions to predator odour. Whereas uninfected gammarids were significantly repulsed by the chemical cues originating from bullheads, infected ones were significantly attracted to the odour of the predator. Taken together, our results suggest that the alteration of anti-predator behaviour in infected G. pulex might enhance predation by bullheads in the field. Reversing anti-predator behaviour might thus be an efficient device by which parasites with complex life-cycles increase their trophic transmission to final hosts. Further studies should pay more attention to both the increased vulnerability of infected prey to an appropriate predator in the field and the influence of parasitic infection on the anti-predator behaviour of intermediate hosts.     

Conflict between parasites with different transmission strategies infecting an amphipod host

Competition between parasites within a host can influence the evolution of parasite virulence and host resistance, but few studies examine the effects of unrelated parasites with conflicting transmission strategies infecting the same host. Vertically transmitted (VT) parasites, transmitted from mother to offspring, are in conflict with virulent, horizontally transmitted (HT) parasites, because healthy hosts are necessary to maximize VT parasite fitness. Resolution of the conflict between these parasites should lead to the evolution of one of two strategies: avoidance, or sabotage of HT parasite virulence by the VT parasite. We investigated two co-infecting parasites in the amphipod host, Gammarus roeseli: VT microsporidia have little effect on host fitness, but acanthocephala modify host behaviour, increasing the probability that the amphipod is predated by the acanthocephalan's definitive host. We found evidence for sabotage: the behavioural manipulation induced by the Acanthocephala Polymorphus minutus was weaker in hosts also infected by the microsporidia Dictyocoela sp. (roeselum) compared to hosts infected by P. minutus alone. Such conflicts may explain a significant portion of the variation generally observed in behavioural measures, and since VT parasites are ubiquitous in invertebrates, often passing undetected, conflict via transmission may be of great importance in the study of host-parasite relationships.     

Effects of Microphallus papillorobustus (Platyhelminthes: Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda)

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.     

Transmission and burden and the impact of temperature on two species of vertically transmitted microsporidia

Microsporidia are unusual amongst eukaryotic parasites in that they utilize both vertical and horizontal transmission and vertically transmitted species can cause sex ratio distortion in their host. Here we study vertical transmission in two species of feminising microsporidia, Nosema granulosis and Dictyocoela duebenum, infecting a single population of the crustacean host Gammarus duebeni and measure the effect of temperature on parasite transmission and replication. N. granulosis was vertically transmitted to 82% of the host embryos and D. duebenum was transmitted to 72% of host embryos. For both parasites, we report relatively low parasite burdens in developing host embryos. However, the parasites differ in their pattern of replication and burden within developing embryos. Whilst N. granulosis undergoes replication during host development, the burden of D. duebenum declines, leading us to propose that parasite dosage and feminisation efficiency underlie the different parasite frequencies in the field. We also examine the effect of temperature on parasite transmission and replication. Temperature does not affect the percentage of young that inherit the infection. However, low temperatures inhibit parasite replication relative to host cell division, resulting in a reduction in parasite burden in infected embryos. The reduced parasite burden at low temperatures may underpin reduced feminization at low temperatures and so limit the spread of sex ratio distorters through the host population.     

Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.     

Assortative pairing in Gammarus insensibilis (Amphipoda) infected by a trematode parasite

We have investigated the influence of Microphallus papillorobustus (Trematoda) on the reproductive biology and mating patterns of its intermediate host Gammarus insensibilis (Amphipoda). Infected Gammarus species show altered behaviour which renders them more susceptible to predation by Charadriiform birds, the parasite's definitive hosts. In a natural population of G. insensibilis, mean parasite intensity was higher for unpaired individuals than for paired individuals. Fecundity was reduced in infected amphipods. Size-assortative pairing was significant, although infected males were found with smaller females compared to uninfected males of the same size. There was also a positive assortative pairing by parasitic prevalence. Vertical segregation between infected and uninfected individuals, male-male competition for access to uninfected females, and female choice may explain assortative mating for prevalence. This study provides the first empirical evidence that parasites can have a direct effect on patterns of mating in gammarids.     

Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict?

Larval helminths of different species that share the same intermediate host and are transmitted by predation to the same definitive host may cooperate in their attempts to manipulate the behaviour of the intermediate host, while at the same time having conflicts of interests over the use of host resources. A few studies have indicated that intermediate hosts harbouring larval helminths have altered concentrations of neurotransmitters in their nervous system, and thus measuring levels of neurotransmitters in host brains could serve to assess the respective and combined effect of different helminth species on host behaviour. Here, we investigate potential cooperation and conflict among three helminths in two species of crab intermediate hosts. The acanthocephalan Profilicollis spp., the trematode Maritrema sp. and an acuariid nematode, all use Macrophthalmus hirtipes (Ocypodidae) as intermediate host, whereas Profilicollis and Maritrema also use Hemigrapsus crenulatus (Grapsidae). All three helminths mature inside gulls or other shore birds. There was a significant decrease in the mean volume of Profilicollis cystacanths as the intensity of infection by this parasite increased in H. crenulatus, the only host in which this was investigated; however, there was no measurable effect of other helminth species on the size of acanthocephalans, suggesting no interspecific conflict over resource use within crabs. There was, in contrast, evidence of a positive interspecific association between the two most common helminth species: numbers of Profilicollis and Maritrema were positively correlated among crabs, independently of crab size, in M. hirtipes but not H. crenulatus. More importantly, we found that the total number of larval helminths per crab correlated significantly, and negatively, with concentrations of serotonin in crab brains, again only in M. hirtipes; numbers of each parasite species separately did not covary in either crab species with serotonin or dopamine, the other neurotransmitter investigated in this study. The relationship with serotonin appears due mainly to numbers of Profilicollis and Maritrema and not to nematodes. This is the first demonstration of a potentially synergistic manipulation of host behaviour by different helminth species, one that appears host-specific; our results also point toward the neurobiological mechanism underlying this phenomenon.     

Parasite transmission and cannibalism in an amphipod (Crustacea)

In its freshwater amphipod host Gammarus duebeni celticus, the microsporidian parasite Pleistophora mulleri showed 23% transmission efficiency when uninfected individuals were fed infected tissue, but 0% transmission by water-borne and coprophagous routes. Cannibalism between unparasitised and parasitised individuals was significantly in favour of the former (37% compared to 0%). In addition, cannibalism between parasitised individuals was significantly higher than between unparasitised individuals (27% compared to 0%). Thus, parasitised individuals were more likely to be cannibalised by both unparasitised and parasitised individuals. We discuss the conflicting selective forces within this host/parasite relationship, the implications of parasite mediated cannibalism for host population structure and the impacts this may have on the wider aquatic community.     

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

In 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.