Infected Amphipods Research Articles

The effect of waterfowl signals and Pseudocorynosoma enrietti infection on the behaviour of the amphipod Hyalella patagonica.

In the present study, we sought to determine whether i) a waterfowl signal induces avoidance behaviour of the amphipod Hyalella patagonica, ii) infection by the acanthocephalan Pseudocorynosoma enrietti affects the behaviour of the amphipod, and iii) the parasite interferes with the amphipod response to waterfowl. We evaluated amphipod behaviour experimentally by measuring activity levels, phototaxis, geotaxis, and clinging behaviour. The main findings of this study indicate that uninfected amphipods show avoidance behaviour by reducing their activity in the presence of a predator signal. Secondly, infected amphipods show altered behaviour, such as swimming in bright areas near the water surface, which makes them more visible to predators in nature. Lastly, the presence of predatory cues causes infected amphipods to drop to the bottom, which increases their visibility to predators. The present research allows us to perceive the intricate interplay among predators, parasites, and their intermediate hosts and advance our understanding of these complex ecological dynamics.

Are amphipodsOrchestia grillus(Bosc, 1802) (Amphipoda: Talitridae) infected with the trematodeLevinseniella byrdi(Heard, 1968) drawn to the light?

AbstractA parasite can change its host’s behavior in spectacular ways. When the saltmarsh amphipod Orchestia grillus (Bosc, 1802) is infected with the trematode Levinseniella byrdi (Heard, 1968) it is bright orange and is found in the open unlike uninfected individuals. I tested the hypothesis that infected amphipods are found in the open because L. byrdi reverses their innate photophobia. During daytime treatments and when placed in a dark chamber, 0% of the uninfected and 20% of the infected amphipods, on average, moved to the light chamber after 30 minutes. When placed in a light chamber, 91% of the uninfected and 53% of the infected amphipods, on average, went to the dark side after 30 minutes. These results clearly indicate that O. grillus is normally photophobic, but not drawn to light when infected with L. byrdi. Instead, L. byrdi appears to neutralize the amphipod’s photophobia. Uninfected O. grillus are typically found under vegetation. I hypothesize that O. grillus with L. byrdi infections wander into open, unvegetated habitats randomly. In addition, 94% of infected amphipods could be touched by a finger in the field suggesting they can be easily caught by predators. Levinseniella byrdi infects at least three other amphipod hosts, Chelorchestia forceps (Smith & Heard, 2001), Uhlorchestia spartinophila (Bousfield & Heard, 1986), and U. uhleri (Shoemaker, 1930). The parasite-manipulation hypothesis suggests that the parasite-induced changes (conspicuous body color and neutralized light response) are adaptive for L. byrdi to make amphipod hosts more susceptible to bird predators, the definitive hosts. This hypothesis remains to be tested.

Pseudocorynosoma enrietti (Molfi & Freitas Fernandes, 1953) (Acanthocephala: Polymorphidae) from Patagonia (Argentina): life cycle, localities, and new host records.

All Pseudocorynosoma species inhabit freshwater environments of the American continent, but little is known about their life cycles. We report Pseudocorynosoma enrietti (Molfi & Freitas Fernandes, 1953) from natural and experimental specimens in Patagonia and identify the intermediate and definitive hosts of its life cycle for the first time in South America. Adult worms were recovered from Anas platyrhynchos (Linnaeus) and from a new definitive host, Coscoroba coscoroba Molina. Naturally infected amphipods, Hyalella patagonica Ortmann, were collected to obtain cystacanths that were fed to Gallus gallus domesticus (Linnaeus) and Anas platyrhynchos. Specimens of P. enrietti are described in detail using light and scanning electron microscopy. A key to species of the genus Pseudocorynosoma is included. Worms are characterized in both sexes by fore-trunk spines, and genital spines in an isolated field. The proboscis has 19-20 hook rows; males have 9-11 (10) hooks per row and females 7-9 (8). Males with four cement glands similar in size. Eggs elongated, with filaments. Experimental male and female worms were recovered from A. platyrhynchos at seven and 14 days, post-infection.

What doesn’t kill you doesn’t make you stronger: Parasites modify interference competition between two invasive amphipods

We used a freshwater amphipod-microsporidian model (Ponto-Caspian hosts: Dikerogammarus villosus and D. haemobaphes, parasite: Cucumispora dikerogammari) to check whether parasites affect biological invasions by modulating behaviour and intra- and interspecific interactions between the invaders. We tested competition for shelter in conspecific and heterospecific male pairs (one or both individuals infected or non-infected). In general, amphipods of both species increased their shelter occupancy time when accompanied by infected rather than non-infected conspecifics and heterospecifics. Infected amphipods faced lower aggression from non-infected conspecifics. Moreover, D. villosus was more aggressive than D. haemobaphes and more aggressive towards conspecifics vs. heterospecifics. In summary, infection reduced the intra- and interspecific competitivity of amphipods, which became less capable of defending their shelters, despite their unchanged need for shelter occupancy. Dikerogammarus haemobaphes, commonly considered as a weaker competitor, displaced by D. villosus from co-occupied locations, was able to compete efficiently for the shelter with D. villosus when microsporidian infections appeared on the scene. This suggests that parasites may be important mediators of biological invasions, facilitating the existence of large intra- and interspecific assemblages of invasive alien amphipods.

Ultrastructure, phylogeny and histopathology of two novel haplosporidians parasitising amphipods, and importance of crustaceans as hosts.

This study provides morphological, ultrastructural and phylogenetic characterization of 2 novel species of Haplosporidia (Haplosporidium echinogammari n. sp. and H. orchestiae n. sp.) infecting amphipods of the genera Echinogammarus and Orchestia collected in southwestern England. Both parasites infect the connective tissues associated with the digestive gland and the tegument, and eventually infect other organs causing disruption of host tissues with associated motor impairment and fitness reduction. Prevalence of infection varied with host species, provenance and season, being as high as 75% for individuals of E. marinus infected with H. echinogammari in June (n = 50). Although no spores were found in any of the infected amphipods examined (n = 82), the morphology of monokaryotic and dikaryotic unicellular stages of the parasites enabled differentiation between the 2 new species. Phylogenetic analysis of the new species based on the small subunit (SSU) rDNA gene placed H. echinogammari close to H. diporeiae in haplosporidian lineage C, and H. orchestiae in a novel branch within Haplosporidium. Genetic diversity of the haplosporidians infecting these and other amphipod species was evaluated and compared to morphological and ultrastructural changes to host tissues. The phylogenetic relationship of haplosporidian infections in other crustacean hosts is discussed after inclusion into the analysis of 25 novel SSU rDNA sequences obtained from crabs, isopods and crayfish.

Bottom‐up control of parasites

AbstractParasitism is a fundamental ecological interaction. Yet we understand relatively little about the ecological role of parasites compared to the role of free‐living organisms. Bottom‐up theory predicts that resource enhancement will increase the abundance and biomass of free‐living organisms. Similarly, parasite abundance and biomass should increase in an ecosystem with resource enhancement. We tested this hypothesis in a landscape‐level experiment in which salt marshes (60,000 m2 each) received elevated nutrient concentrations via flooding tidal waters for 11 yr to mimic eutrophication. Nutrient enrichment elevated the densities of the talitrid amphipod, Orchestia grillus, and the density and biomass of its trematode parasite, Levinseniella byrdi. Strikingly, L. byrdi prevalence increased over time, up to 13 times higher in nutrient‐enriched marshes (30%) relative to the mean prevalence in reference marshes (2.4%). The biomass density of infected amphipods was, on average, 11 times higher in nutrient‐enriched marshes (1.1 kg/ha) than in reference marshes (0.1 kg/ha), when pooling across all years. Orchestia grillus biomass comprises 67% of the arthropod community biomass; thus, nutrient enrichment elicits a substantial surge in parasitized biomass in the arthropod community. If our results are typical, they suggest that eutrophication can increase parasite abundance and biomass with chronic resource enhancement. Therefore, minimizing aquatic nutrient pollution may prevent outbreaks of parasites with aquatic hosts.

Parasite-induced alteration of odour responses in an amphipod–acanthocephalan system

Odour-related behaviours in aquatic invertebrates are important and effective anti-predator behaviours. Parasites often alter invertebrate host behaviours to increase transmission to hosts. This study investigated the responses of the amphipod Hyalella azteca when presented with two predator chemical cues: (i) alarm pheromones produced by conspecifics and (ii) kairomones produced by a predatory Green Sunfish (Lepomis cyanellus). We compared the responses of amphipods uninfected and infected with the acanthocepalan parasite Leptorhynchiodes thecatus. Uninfected amphipods reduced activity and increased refuge use after detecting both the alarm pheromones and predator kairomones. Infected amphipods spent significantly more time being active and less time on the refuge than uninfected amphipods, and behaved as if they had not detected the chemical stimulus. Therefore, L. thecatus infections disrupt the amphipods’ anti-predator behaviours and likely make their hosts more susceptible to predation.

Variable effects of increased temperature on a trematode parasite and its intertidal hosts

Climate change has the potential to influence host–parasite interactions. In this study, we tested how an increase in temperature outside of the common range (12–17°C) in the Upper Bay of Fundy affected the infection success and impact of a marine parasite (the trematode Gynaecotyla adunca) to its second intermediate host, the intertidal amphipod Corophium volutator. We measured the emergence of G. adunca infectious stages (cercariae) from the first intermediate host, the mud snail Ilyanassa obsoleta, over short (24h) and long (34days) time periods, the condition of infected snails, the success of cercariae in penetrating amphipod hosts (infectivity), and the survivorship of infected amphipods. The greatest number of cercariae emerged at 22°C after 24h; however, after an initial peak, few cercariae emerged over the longer observation period and there were no consistent temperature effects. Infected snails remained in good condition at the highest temperature (22°C), as evidenced by their high survivorship and ability to upright themselves. Amphipod host infection (prevalence and intensity) was not affected by temperature. The highest temperature negatively affected amphipod survival, but this did not differ between infected and uninfected hosts. We suggest that increased temperature by itself appears not to result in greater amphipod susceptibility to infection by trematodes or reduced host condition/survival if it is within a naturally-experienced range. While our study indicates no clear and consistent effects of a moderate temperature increase alone on the infection success and impacts of G. adunca in the Upper Bay of Fundy, further studies employing a greater range of temperature extremes and additional abiotic and biotic factors will be needed in order to better understand how climate change may impact the keystone amphipods in nature.

Parasite-induced suppression of aggregation under predation risk in a freshwater amphipod: Sociality of infected amphipods

Recent findings suggest that grouping with conspecifics is part of the behavioural defences developed by amphipod crustaceans to face predation risk by fish. Amphipods commonly serve as intermediate hosts for trophically transmitted parasites. These parasites are known for their ability to alter intermediate host phenotype in a way that promotes predation by definitive hosts, where they reproduce. If aggregation in amphipods dilutes the risk to be preyed on by fish, then it may dilute the probability of transmission for the parasite using fish as definitive hosts. Using experimental infections, we tested whether infection with the fish acanthocephalan Pomphorhynchus laevis alters attraction to conspecifics in the amphipod intermediate host Gammarus pulex. We also measured G. pulex's activity and reaction to light to detect potential links between changes in aggregation and changes in other behaviours. The attraction to conspecifics in the presence of predator cue, a behaviour found in uninfected gammarids, was cancelled by the infection, while phototaxis was reversed and activity unchanged. We found no correlation between the three behaviours in infected amphipods, while activity and aggregation were negatively correlated in uninfected individuals after the detection of predation cue. The physiological causes and the adaptive value of aggregation suppression are discussed in the context of a multidimensional manipulation.

Host manipulation revisited: no evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with acanthocephalans

Summary1.Many parasites with complex life cycles critically rely on trophic transmission to pass from an intermediate host to a final host. Parasite‐induced behavioural alterations in intermediate hosts are often supposed to be adaptive through increasing the susceptibility of intermediate hosts to predation by final hosts. However, the evidence is so far only correlational, and direct evidence for a causal link between one single behavioural alteration and increased trophic transmission is still missing.2.Here, we addressed, for the first time, the relationship between increased vulnerability to fish predation and altered photophobia in an amphipod, Gammarus pulex, infected with a fish acanthocephalan, Pomphorhynchus tereticollis.3.In microcosms, naturally‐infected amphipods were significantly more vulnerable to fish predation than uninfected ones at two different light intensities. However, although variation in illumination significantly affected the extent of difference in photophobia between infected and uninfected individuals, it had no effect on predation bias towards infected amphipods.4.In addition, although an injection of a mixture of serotonin and fluoxetine in uninfected amphipods mimicked the parasite‐induced decreased photophobia, injected individuals were not more vulnerable to fish predation that uninfected ones injected with a control solution.5.Overall, our results indicate that the decreased photophobia in infected intermediate hosts does not play in itself a causal role in the trophic transmission of the parasite to its final host. The actual role a parasite‐induced behavioural alteration plays in trophic transmission should be carefully assessed before an adaptive interpretation is given.

Paramyxean–microsporidian co-infection in amphipods: Is the consensus that Microsporidia can feminise their hosts presumptive?

The current consensus is that Microsporidia belong to a select group of parasites capable of causing both intersexuality and complete sex reversal in their hosts. Indeed, species such as Nosema granulosis and Dictyocoela duebenum, which infect amphipod crustaceans, are regularly referred to as ‘feminising microsporidians’. This categorisation is based on a combination of findings: that these species are vertically transmitted and occur at a high prevalence of infection in intersex and female amphipods, that infected amphipod populations are female-biased, and that infected females have significantly female-biased broods with no concurrent increase in mortality. In this study, we report on a population of the amphipod Echinogammarus marinus presenting both female bias and high levels of intersexuality, which are infected with D. deubenum. In keeping with its feminising classification, infection is prevalent in animals presenting female and intersex phenotypes. However, a further screen revealed the presence of a previously unknown paramyxean parasite related to organisms of the genus Marteilia, a group known to cause catastrophic sexual dysfunction in bivalves. We found that the paramyxean parasite was also vertically transmitted, with infections being more prevalent in females and intersex animals. Critically, every animal infected with D. deubenum was also co-infected with the paramyxean, with few animals presenting an independent paramyxean infection. In contrast, co-infection of E. marinus with a paramyxean and the non-feminising microsporidian Dictyocoela berillonum rarely occurred. These observations raise a new hypothesis, namely, that D. duebenum and other feminising microsporidians are not actually capable of host feminisation but instead ‘hitch-hike’ together with a feminising paramyxean parasite.

Effects of salinity on an intertidal host–parasite system: Is the parasite more sensitive than its host?

Intertidal habitats are characterised by highly fluctuating environmental conditions including varying salinity regimes. Changes in salinity may be gradual or abrupt; for example, heavy rainfall or evaporation during warm periods can either decrease or increase salinity. Trematodes are the most common parasites in intertidal ecosystems and their transmission is known to be highly influenced by environmental conditions. However, effects of salinity on the transmission of intertidal trematodes are not well studied. Here, we investigated the effects of long-term (i.e. several weeks) exposure to different salinities (25, 30, 35 and 40 psu) on the transmission of Maritrema novaezealandensis from its first intermediate snail host ( Zeacumantus subcarinatus) to a second intermediate amphipod host ( Paracalliope novizealandiae), in order to evaluate overall net effects. The following steps were assessed: output of parasite transmission stages (cercariae) from infected snail hosts, survival and infectivity of cercariae, susceptibility of amphipod hosts to infection and survival of amphipod hosts including parasite development within amphipod hosts. Output and survival of cercariae increased with increasing salinity whilst infectivity of cercariae and susceptibility of amphipods to infection were not clearly affected. Survival of amphipods was significantly longer at lower salinities and parasite development in infected amphipods was concomitantly more advanced. Overall, the results suggest that the parasite and the amphipods are differentially affected, and that under normal to increased salinities conditions are more favourable for the parasite than for the amphipod host.

Development of Ascarophis SP. (Nematoda: Cystidicolidae) to Maturity In Gammarus deubeni (Amphipoda)

Experimentally transmitted Ascarophis sp. (Spirurida) developed to adult worms in the invertebrate host, Gammarus deubeni (Amphipoda), collected in the intertidal zone in Passamaquoddy Bay, New Brunswick, Canada. The morphological development and growth of larval stages is very similar to other cystidicolids, which are found as adults in fish. Unlike virtually all other Spirurida, which require a vertebrate definitive host, infective larvae of Ascarophis sp. migrate from the invertebrate host musculature into the hemocoel where they molt twice to become adults. Gravid females appear at 80 days and 69 days post-infection at 10-12 C and 18-20 C, respectively. While there is little evident host reaction to the parasite within the muscle tissue, within the hemocoel there is hemocytic reaction to shed nematode cuticles, released eggs, and sometimes the worm itself, including some melanization. The worms are morphologically similar to Ascarophis sp. from G. oceanicus in the Baltic and White seas and among Ascarophis species from fish is most similar to A. arctica. It is suggested that Ascarophis sp. no longer requires a vertebrate host and is transmitted between amphipods either through death and disintegration of infected amphipods and dispersal of the nematode eggs, or more likely through cannibalism or necrophagy.

Introduced brown trout alter native acanthocephalan infections in native fish

1. Native parasite acquisition provides introduced species with the potential to modify native host-parasite dynamics by acting as parasite reservoirs (with the 'spillback' of infection increasing the parasite burdens of native hosts) or sinks (with the 'dilution' of infection decreasing the parasite burdens of native hosts) of infection. 2. In New Zealand, negative correlations between the presence of introduced brown trout (Salmo trutta) and native parasite burdens of the native roundhead galaxias (Galaxias anomalus) have been observed, suggesting that parasite dilution is occurring. 3. We used a multiple-scale approach combining field observations, experimental infections and dynamic population modelling to investigate whether native Acanthocephalus galaxii acquisition by brown trout alters host-parasite dynamics in native roundhead galaxias. 4. Field observations demonstrated higher infection intensity in introduced trout than in native galaxias, but only small, immature A. galaxii were present in trout. Experimental infections also demonstrated that A. galaxii does not mature in trout, although parasite establishment and initial growth were similar in the two hosts. Taken together, these results support the hypothesis that trout may serve as an infection sink for the native parasite. 5. However, dynamic population modelling predicts that A. galaxii infections in native galaxias should at most only be slightly reduced by dilution in the presence of trout. Rather, model exploration indicates parasite densities in galaxias are highly sensitive to galaxias predation on infected amphipods, and to relative abundances of galaxias and trout. Hence, trout presence may instead reduce parasite burdens in galaxias by either reducing galaxias density or by altering galaxias foraging behaviour.

The consequences of parasitic infections for host behavioural correlations and repeatability

Summary The lifecycles of parasites are often complex, with multiple successive hosts. Many parasites have evolved the ability to modify the behaviour of their present host to increase the chance of transmission to the next host. Few studies to date have considered how a suite of related behavioural traits in the host can be affected by parasitic manipulations. The present study investigated the effect of two trematode parasites, Coitocaecum parvum and Microphallus sp., on the behaviour of their amphipod host (Paracalliope fluviatilis) in a behavioural syndrome framework. This framework focused on the correlations between, and repeatabilities within suites of behavioural traits. Three activity-related behavioural tests were conducted: phototaxis (response to light), horizontal activity, and vertical distribution. Infection by C. parvum did not have any significant effect on any of the behavioural traits investigated. However, amphipods infected by Microphallus sp. spent less time in the light. Surprisingly, amphipods harbouring Microphallus sp. also showed stronger behavioural correlations in general, compared to those of uninfected hosts. Furthermore, the repeatability of the phototaxis test for infected amphipods was lower than that of uninfected amphipods. Given these results, we encourage future studies to use this behavioural syndrome framework.

A manipulative parasite increasing an antipredator response decreases its vulnerability to a nonhost predator

Trophically transmitted parasites have to deal with the antipredator adaptations of their intermediate hosts. Some of these parasites induce behavioural changes in their intermediate hosts that make them more vulnerable to predation by definitive hosts. However, the adaptiveness of behavioural manipulation also depends on the probability of being eaten by a nonhost predator. Parasites might therefore try to use specific antipredator responses of intermediate hosts to avoid this dead end. We tested this hypothesis using the acanthocephalan Polymorphus minutus and its intermediate amphipod host, Gammarus roeseli. In their natural habitat, uninfected G. roeseli shelter near the river bottom while infected gammarids tend to cling onto floating materials. In microcosm experiments, infected amphipods were preyed upon by sticklebacks (nonhost predators) less than uninfected individuals when refuges were provided near the water surface. Regardless of their infection status, G. roeseli reacted to olfactory cues of predation by spending more time on refuges and near the surface. However, these behaviours were increased in infected gammarids. These results suggest that, in addition to specific induced behaviours, parasites may also enhance an existing antipredator behaviour to increase their own survival.

Haplosporidian parasite in Diporeia spp. amphipods from the Great Lakes region, USA

Light microscope observations of a haplosporidian in Diporeia spp. amphipods from Lakes Michigan and Huron, USA, found that the parasite spore is operculate and measures 8.1 microm in length and 6.1 microm in width. Round to amorphous sporocysts averaging 23.6 microm were present throughout hemal sinuses of infected amphipods. The number of developing spores within a sporocyst was highly variable and spores were observed in various stages of development. Electron microscopy revealed a lid over the operculum of developing spores and documented spores with fairly large and extensive ornamentation. This is the first haplosporidian reported in Diporeia spp. amphipods and only the second haplosporidian from freshwater species.

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.

The Effect of Echinorhynchus borealis (Acanthocephala) Infection on the Anti-Predator Behavior of a Benthic Amphipod

In benthic habitats, predators can generally not be detected visually, so olfaction may be particularly important for inducing anti-predation behaviors in prey organisms. Manipulative parasites infecting benthic hosts could suppress these responses so as to increase the probability of predation and thus trophic transmission. We studied how infection with the acanthocephalan Echinorhynchus borealis affects the response of the benthic amphipod Pallasea quadrispinosa to water conditioned by burbot (Lota lota), the parasite's definitive host. In normal lake water, refuge use by infected and uninfected amphipods was similar, but when exposed to burbot-conditioned water, uninfected amphipods spent much more time hiding than infected amphipods. Thus, rather than affecting ambient hiding behavior, E. borealis infection seems to alter host response to a predator. A group of amphipods sampled from a postglacial spring that is devoid of fish predators exhibited only a weak response to burbot-conditioned water, perhaps suggesting these anti-predator behaviors are costly to maintain. The hiding behavior of spring and infected amphipods was very similar. If the reduced refuge use by the spring amphipods reflects adaptation to a predator-free environment, this indicates that E. borealis severely weakens its host's anti-predator behavior. Presumably this increases the likelihood of parasite transmission.

Crustacean-acanthocephalan interaction and host cell-mediated immunity: parasite encapsulation and melanization

Host-parasite interactions of Pomphorhynchus laevis (Müller, 1776) in naturally infected amphipod, Echinogammarus stammeri (Karaman), from the Brenta River (northern Italy) are described. A fully developed acanthocephalan larva occupies a large portion of an amphipod's haemocoelic space; thus, the parasite frequently induces displacement of host digestive tract and other internal organs. However, no apparent damage to the host's internal structures was observed. Within the haemocoel of E. stammeri, each larva of P. laevis is surrounded with a membranous layer, formed by microvilli, which maintains intimate contact with the amphipod's internal organs and haemocytes. Three types of circulatory haemocytes were identified based upon their distinct appearance: hyaline cell, semi-granular cell and granular cell. Echinogammarus stammeri haemocytes surrounded acanthocephalan larvae and in some instances a partially and/or totally melanized P. laevis larva was noticed. Interestingly, no melanized larvae were found in E. stammeri parasitized with other acanthocephalans namely Echinorhynchus truttae (Schrank, 1788), Polymorphus minutus (Goeze, 1782) and Acanthocephalus clavula (Dujardin, 1845).