Acanthocephalan Parasite Pomphorhynchus Laevis Research Articles

Increased temperature has no consequence for behavioral manipulation despite effects on both partners in the interaction between a crustacean host and a manipulative parasite

Parasites alter many traits of their hosts. In particular, parasites known as “manipulative” may increase their probability of transmission by inducing phenotypic alterations in their intermediate hosts. Although parasitic-induced alterations can modify species’ ecological roles, the proximate factors modulating this phenomenon remain poorly known. As temperature is known to affect host–parasite associations, understanding its precise impact has become a major challenge in a context of global warming. Gammarids are ecologically important freshwater crustaceans and serve as intermediate hosts for several acanthocephalan species. These parasites induce multiple effects on gammarids, including alterations of their behavior, ultimately leading to modifications in their functional role. Here, experimental infections were used to assess the effect of two temperatures on several traits of the association between Gammarus pulex and its acanthocephalan parasite Pomphorhynchus laevis. Elevated temperature affected hosts and parasites in multiple ways (decreased host survival, increased gammarids activity, faster parasites development and proboscis eversion). However, behavioral manipulation was unaffected by temperature. These results suggest that predicted change in temperature may have little consequences on the trophic transmission of parasites through changes in manipulation, although it may modify it through increased infection success and faster parasites development.

Parasite-induced colour alteration of intermediate hosts increases ingestion by suitable final host species

Abstract Parasites with complex life cycles often alter the phenotypic appearance of their intermediate hosts in order to facilitate ingestion by the final host. However, such manipulation can be costly as it might increase ingestion by less suitable or dead-end hosts as well. Species-specific parasitic manipulation is a way to enhance the transmission to suitable final hosts. Here, we experimentally show that the altered body colouration of the intermediate host Gammarus pulex caused by its acanthocephalan parasite Pomphorhynchus laevis differently affects predation by different fish species (barbel, perch, ruffe, brown trout and two populations of three-spined stickleback) depending on their suitability to act as final host. Species that were responsive to colour manipulation in a predation experiment were more susceptible to infection with P. laevis than unresponsive species. Furthermore, three-spined stickleback from different populations responded to parasite manipulation in opposite directions. Such increased ingestion of the intermediate host by preferred and suitable hosts suggests fine-tuned adaptive parasitic manipulation and sheds light on the ongoing evolutionary arms race between hosts and manipulative parasites.

First evidence for a possible invasional meltdown among invasive fish parasites

Biological invasions are frequently studied topics in ecological research. Unfortunately, within invasion ecology parasite-associated aspects such as parasite impacts on new environments and on local host populations are less well-studied. Round gobies migrating from the Ponto-Caspian region into the Rhine River system are heavily infested with the Ponto-Caspian acanthocephalan parasite Pomphorhynchus laevis. As shown by experimental infestations the acanthocephalans occur as pre-adults in host-encapsulated cysts within the internal organs of the migrating gobies, but remain infective for their definitive host chub. Recently, we described the occurrence of larvae of another parasite, the invasive eel swim bladder nematode Anguillicola crassus, in these Pomphorhynchus cysts. In the present study, we could prove the infectivity of the nematode larvae for European eels for the first time. After experimental inoculation of Pomphorhynchus cysts occasionally infested with A. crassus larvae, the nematodes grow to maturity and reproduce whereas all P. laevis were unviable. We therefore postulate that the nematode larvae behave like immunological hitchhikers that follow a “Trojan horse strategy” in order to avoid the paratenic host’s immune response. Accordingly, the interaction between both invasive parasites gives first evidence that the invasional meltdown hypothesis may also apply to parasites.

Parasite-induced alteration of plastic response to predation threat: increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis

Larvae of many trophically-transmitted parasites alter the behaviour of their intermediate host in ways that increase their probability of transmission to the next host in their life cycle. Before reaching a stage that is infective to the next host, parasite larvae may develop through several larval stages in the intermediate host that are not infective to the definitive host. Early predation at these stages results in parasite death, and it has recently been shown that non-infective larvae of some helminths decrease such risk by enhancing the anti-predator defences of the host, including decreased activity and increased sheltering. However, these behavioural changes may divert infected hosts from an optimal balance between survival and foraging (either seeking food or a mate). In this study, this hypothesis was tested using the intermediate host of the acanthocephalan parasite Pomphorhynchus laevis, the freshwater amphipod Gammarus pulex. We compared activity, refuge use, food foraging and food intake of hosts experimentally infected with the non-infective stage (acanthella), with that of uninfected gammarids. Behavioural assays were conducted in four situations varying in predation risk and in food accessibility. Acanthella-infected amphipods showed an increase in refuge use and a general reduction in activity and food intake. There was no effect of parasite intensity on these traits. Uninfected individuals showed plastic responses to water-borne cues from fish by adjusting refuge use, activity and food intake. They also foraged more when the food was placed outside the refuge. At the intra-individual level, refuge use and food intake were positively correlated in infected gammarids only. Overall, our findings suggest that uninfected gammarids exhibit risk-sensitive behaviour including increased food intake under predation risk, whereas gammarids infected with the non-infective larvae of P. laevis exhibit a lower motivation to feed, irrespective of predation risk and food accessibility.

PROTECTION FIRST THEN FACILITATION: A MANIPULATIVE PARASITE MODULATES THE VULNERABILITY TO PREDATION OF ITS INTERMEDIATE HOST ACCORDING TO ITS OWN DEVELOPMENTAL STAGE

Many trophically transmitted parasites with complex life cycles manipulate their intermediate host behavior in ways facilitating their transmission to final host by predation. This facilitation generally results from lowering host's antipredatory defenses when the parasite is infective to the final host. However, a recent theoretical model predicts that an optimal parasitic strategy would be to protect the intermediate host from predation when noninfective, before switching to facilitation when the infective stage is reached. We tested this hypothesis in the fish acanthocephalan parasite Pomphorhynchus laevis using the amphipod Gammarus pulex as intermediate host. Gammarids parasitized by noninfective stage of P. laevis (acanthella) hid significantly more under refuges than uninfected ones. In addition, acanthella-infected gammarids were less predated upon by trout than uninfected ones. As predicted, a switch toward decreased antipredatory behavior of G. pulex and enhanced vulnerability to predation was found when P. laevis reached the stage infective to its final host. The parasites appear to be able to exploit plasticity in host antipredatory responses, and shift the host optimal response toward their own optimal balance.

Intraspecific conflict over host manipulation between different larval stages of an acanthocephalan parasite

Competitive interactions between coinfecting parasites are expected to be strong when they affect transmission success. When transmission is enhanced by altering host behaviour, intraspecific conflict can lead to 'coinfection exclusion' by the first-in parasite or to a 'sabotage' of behavioural manipulation by the youngest noninfective parasite. We tested these hypotheses in the acanthocephalan parasite Pomphorhynchus laevis, reversing phototaxis in its intermediate host Gammarus pulex. No evidence was found for coinfection exclusion in gammarids sequentially exposed to infection. Behavioural manipulation was slightly weakened but not cancelled in gammarids infected with mixed larval stages. Therefore, coinfecting infective and noninfective larvae both suffered competition, potentially resulting in delayed transmission and increased risk of mortality, respectively. Consequently, noninfective larva is not just a 'passive passenger' in the manipulated host, which raises interesting questions about the selective pressures at play and the mechanisms underlying manipulation.

VARIATION BETWEEN POPULATIONS AND LOCAL ADAPTATION IN ACANTHOCEPHALAN-INDUCED PARASITE MANIPULATION

Many trophically transmitted parasites manipulate their intermediate host phenotype, resulting in higher transmission to the final host. However, it is not known if manipulation is a fixed adaptation of the parasite or a dynamic process upon which selection still acts. In particular, local adaptation has never been tested in manipulating parasites. In this study, using experimental infections between six populations of the acanthocephalan parasite Pomphorhynchus laevis and its amphipod host Gammarus pulex, we investigated whether a manipulative parasite may be locally adapted to its host. We compared adaptation patterns for infectivity and manipulative ability. We first found a negative effect of all parasite infections on host survival. Both parasite and host origins influenced infection success. We found a tendency for higher infectivity in sympatric versus allopatric combinations, but detailed analyses revealed significant differences for two populations only. Conversely, no pattern of local adaptation was found for behavioral manipulation, but manipulation ability varied among parasite origins. This suggests that parasites may adapt their investment in behavioral manipulation according to some of their host's characteristics. In addition, all naturally infected host populations were less sensitive to parasite manipulation compared to a naive host population, suggesting that hosts may evolve a general resistance to manipulation.

MODIFICATION OF HOSTS' BEHAVIOR BY A PARASITE: FIELD EVIDENCE FOR ADAPTIVE MANIPULATION

Parasites relying on trophic transmission to complete their life cycles often induce modifications of their host's behavior in ways that may increase their susceptibility to predation by final hosts. These modifications have often been interpreted as parasite adaptations, but very few studies have demonstrated that host manipulation has fitness benefits for the parasite. The aim of the present study was to address the adaptive significance of parasite manipulation by coupling observations of behavioral manipulation to estimates of trophic transmission to the definitive host in the natural environment. We show that the acanthocephalan parasite Pomphorhynchus laevis manipulates the drifting behavior of one of its intermediate hosts, the amphipod Gammarus pulex, but not of a sympatric host, the introduced amphipod Gammarus roeseli. We found a 26.3-28.3 times higher proportion of infected G. pulex in the stomach content of one of the definitive hosts of P. laevis, the bullhead Cottus gobio, than in the benthos. No such trend was observed for G. roeseli. The bell-shaped curve of mean parasite abundance (MPA) relative to host size observed in G. pulex also supported an increased predation mortality of P. laevis-infected individuals compared to uninfected amphipods. Again, no such pattern was observed in G. roeseli. Furthermore, our results indicate that the modifications induced by P. laevis are specific to the definitive host and do not increase the risk of predation by inappropriate hosts, here the adult edible frog Rana esculenta. Overall, our study is original in that it establishes, under field conditions, a direct link between parasitic manipulation and increased transmission to the definitive host, and more importantly, identifies the specificity of the manipulation both in the intermediate host species and toward the definitive host.

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.

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.

The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead ( 210Pb) in its fish host chub ( Leuciscus cephalus)

Uninfected chub as well as fish experimentally infected with the acanthocephalan parasite Pomphorhynchus laevis were exposed to 210Pb 2+ for up to 38 days and the uptake and distribution of lead within different fish organs and the parasites was determined at various time points. Highest metal concentrations were detected in the acanthocephalans, followed by intestine, bile, liver, gill and muscle of the fish host. Infected chub had significantly lower 210Pb levels in the gills on day 17 ( P≤0.01), in the bile on day 24 ( P≤0.05) and in the gills as well as in the intestine on day 38 compared with uninfected fish. A subsequent polynomial regression revealed that lead levels for the infected fish ranged below the levels determined for uninfected fish during most of the exposure period. This is the first proof that P. laevis reduces lead levels in the bile thereby diminishing or even impeding the hepatic intestinal cycling of lead, which may reduce the amount of metals available for the fish organs. This is especially important for ecotoxicological research. For example, organisms used as accumulation indicators may erroneously indicate low levels of pollution if they are infected with parasites which alter their pollutant uptake mechanisms. Additionally, the results gave further experimental evidence for acanthocephalans as accumulation indicators for metals.

Activity levels and predator detection by amphipods infected with an acanthocephalan parasite, Pomphorhynchus laevis.

The acanthocephalan parasite Pomphorhynchus laevis (Müller, 1776) uses freshwater amphipods as its intermediate host. In order to complete the life cycle, the infected amphipod must be consumed by a fish, where the acanthocephalan will mature and reproduce. Parasite transmission, and therefore fitness, could be enhanced if infected amphipods fail to detect or avoid predatory fish. We compared the activity levels of infected and non-infected amphipods, Echinogammarus stammeri (Karaman, 1931), in both the presence and absence of odours from its natural, definitive host, the fish Leuciscus cephalus (L.). Throughout the experiment, infected amphipods were more active than were non-infected individuals. The non-infected amphipods reduced their activity after the addition of fish odours, but the infected amphipods failed to show a significant decrease. The failure of infected amphipods to reduce activity levels in the presence of fish odour may reflect a parasite strategy to increase its chances of transmission by making its amphipod host more vulnerable to predation by fish.

A predator's dilemma: prey choice and parasite susceptibility in three-spined sticklebacks.

The acanthocephalan parasite Pomphorhynchus laevis is transmitted by a suitable intermediate host such as the amphipod Gammarus pulex to its definitive fish host. Parasite-induced alterations in both appearance and behaviour concur to render infected gammarids more vulnerable to predation, thus promoting parasite transmission. Experimental infection of laboratory bred full- and half-sib groups of three-spined sticklebacks (Gasterosteus aculeatus) provided evidence that the parasite imposes a survival cost proportional to the severity of infection on its final host. Variation among sibships in the susceptibility to infection was consistent. When given a choice, fish consumed significantly more infected than uninfected prey. Overall, more resistant fish did not prey upon infected gammarids more often than did relatively susceptible fish. Only fish with a relatively high physical condition properly adjusted prey selection to the extent of their parasite susceptibility, thus exploiting the enhanced profitability of infected prey.

Pomphorhynchuslaevis (Palaeacanthocephala) in the intestine of chub ( Leuciscuscephalus) as an indicator of metal pollution

Chub experimentally infected with the acanthocephalan parasite Pomphorhynchus laevis were exposed to 0.01 mg l −1 Pb 2+ over 5 weeks. Lead was rapidly accumulated in the intestinal worms reaching a steady-state concentration after 4 weeks. This concentration was significantly greater than in the host muscle, liver and intestine and more than 9,000 times higher than the exposure concentration. Lead accumulation in P. laevis increased at a higher exposure concentration but was not correlated with either parasite intensity or with pooled or individual worm weight. The highest lead concentrations were recorded in those specimen of P. laevis that were attached in the posterior intestine. Interestingly, parasitised chub accumulated less lead in their own tissues than uninfected conspecifics. A mechanism of lead uptake by P. laevis and the application of acanthocephalans as accumulation indicators of metal pollution is discussed.

The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex

Besides conspicuous changes in behaviour, manipulative parasites may also induce subtle physiological effects in the host that may also be favourable to the parasite. In particular, parasites may be able to influence the re-allocation of resources in their own favour. We studied the association between the presence of the acanthocephalan parasite, Pomphorhynchus laevis, and inter-individual variation in the lipid and glycogen content of its crustacean host, Gammarus pulex (Amphipoda). Infected gravid females had significantly lower lipid contents than uninfected females, but there was no difference in the lipid contents of non-gravid females and males that were infected with P. laevis. In contrast, we found that all individuals that were parasitised by P. laevis had significantly increased glycogen contents, independent of their sex and reproductive status. We discuss our results in relation to sex-related reproductive strategies of hosts, and the influence they may have on the level of conflict over energy allocation between the host and the parasite.

Parasite-Altered Behavior in a Crustacean Intermediate Host: Field and Laboratory Studies

The effects of the acanthocephalan parasite Pomphorhynchus laevis on the behavior of its crustacean intermediate host, the amphipod Echinogammarus stammeri, were studied. A drift study revealed that infected amphipods were disproportionately represented in drift samples taken throughout a 24-hr period; infection with more than 1 parasite enhanced this effect. Infection also interacted with the daily timing of drift, with parasitized amphipods beginning to drift earlier in the evening. Two distinct behaviors quantified in laboratory settings may play a role in this increased drifting behavior: parasitized amphipods showed (1) an increased preference for an illuminated environment and (2) increased activity in comparison to nonparasitized conspecifics. These results are consistent with previous studies on the effects of P. laevis on another amphipod host, Gammarus pulex, and provide new data on the activity level of P. laevis-infected amphipods.

Decreased enterochromaffin-like cell and parietal cell densities in hyperplastic oxyntic mucosa of hypergastrinemic rats infected with Taenia taeniaeformis

Chub experimentally infected with the acanthocephalan parasite Pomphorhynchus laevis were exposed to 0.01 mg l−1 Pb2+ over 5 weeks. Lead was rapidly accumulated in the intestinal worms reaching a steady-state concentration after 4 weeks. This concentration was significantly greater than in the host muscle, liver and intestine and more than 9,000 times higher than the exposure concentration. Lead accumulation in P. laevis increased at a higher exposure concentration but was not correlated with either parasite intensity or with pooled or individual worm weight. The highest lead concentrations were recorded in those specimen of P. laevis that were attached in the posterior intestine. Interestingly, parasitised chub accumulated less lead in their own tissues than uninfected conspecifics. A mechanism of lead uptake by P. laevis and the application of acanthocephalans as accumulation indicators of metal pollution is discussed.

The cement apparatus of larval and adult Pomphorhynchus laevis (Acanthocephala: Palaeacanthocephala).

Light and electron microscopy were used to study the ultrastructure of the cement apparatus, namely cement glands and cement ducts of mature specimens of the acanthocephalan parasite Pomphorhynchus laevis Müller, 1776, recovered from the digestive tracts of fish Leuciscus cephalus Risso, 1826. In addition, the cement glands of immature P. laevis found within the body cavity of the fish Alburnus alburnus alborella De Filippi, 1844 were examined. In a mature male of P. laevis the 6 cement glands are rounded to oval in shape and each of them has an outer cytoplasmic layer containing nuclei and surrounding a space for storage of the cement material within the gland. The nuclei have an irregular outline and the cytoplasm of the cells contains round, membrane-bound secretory granules approximately 1 micron in diameter. Nuclei surrounded by secretory granules were present inside the gland lumen. Within the gland ducts of mature males, granules were present within the wall thickness and, inside the luminal area, mitochondria were encountered. In contrast, within the cement glands of immature P. laevis there were no secretory granules and the chromatin of the nuclei appeared condensed. The nature of the secretory product of the cement glands was investigated with histological and electrophoretic methods. A protein with molecular weight of 23 kDa was recorded as a major component of cement.

PARASITE-INDUCED CHANGES IN BEHAVIOR AND COLOR MAKEGAMMARUS PULEXMORE PRONE TO FISH PREDATION

The acanthocephalan parasite Pomphorhynchus laevis is transmitted by crustaceans such as Gammarus pulex to its paratenic or final hosts, fish. The conspicuous orange-yellow parasite is visible through the transparent cuticle of G. pulex. Infected gammarids are significantly less photophobic than uninfected ones. When hungry three-spined sticklebacks (Gasterosteus aculeatus), one of the hosts of this parasite, were offered equal numbers of uninfected and infected prey, G. pulex infected with P. laevis were eaten significantly more often. We tested experimentally whether parasite color and parasite-induced changes in host behavior affected the predation rate of G. pulex. Color effects were tested with uninfected G. pulex by painting an orange spot on their cuticle that simulated infection. Behavioral effects were tested with infected G. pulex by covering the place through which the orange parasite was visible with inconspicuous brown paint. We showed for the first time that both parasite color and changed intermediate host behavior promote the transmission of P. laevis to its next host. The evolution of orange parasite color, and why sticklebacks do not avoid infected prey, are discussed.

The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex)

SUMMARY 1. The drift of Gammarus pulex in a population in which approximately 20% of adults are infected with the acanthocephalan parasite Pomphorhynchus laevis was monitored at margin and mid‐river sites in the River Teme, England over a 24‐h period in mid‐summer.2. Drift densities showed a diurnal pattern with a large increase at night, independent of parasite burden.3. There was no significant effect of site (margin or mid‐river) on the proportion of parasitized and unparasitized G. pulex found in the drift or the benthos.4. The drift of parasitized G. pulex was significantly greater than unparasitized animals. Gammarids harbouring only one parasite were found in significantly higher proportions in the drift than those with two or more parasites.5. At both sites (margin and mid‐river) the proportion of unparasitized adult G. pulex in the drift was significantly lower than that in the benthos. However, there was a significantly higher proportion of parasitized animals in the drift than in the benthos.