Uninfected Gammarids Research Articles

Infection with an acanthocephalan helminth reduces anxiety-like behaviour in crustacean host

Trophically transmitted heteroxenous parasites of diverse clades can decrease or reverse antipredator behaviours in their intermediate hosts, thereby increasing their chances of reaching their final hosts. Such behavioural alterations could result from compromised cognitive abilities affecting fear- or more generally stress-related neurophysiological pathways. We tested this hypothesis in a key model system in the study of parasitic manipulation, the fish acanthocephalan parasite Pomphorhynchus tereticollis and its intermediate crustacean host Gammarus fossarum, using the ‘threat of electric shock’ paradigm. We exposed uninfected and infected G. fossarum to chronic and/or acute electric shock programs at two different intensities (voltage), and then quantified their sheltering behaviour as a proxy for anxiety-like state. Infected gammarids did not express anxiety-like response to electric shocks, while uninfected gammarids hid more when exposed to acute treatments, and when exposed to the high intensity chronic treatment. Interestingly, the lack of response in infected gammarids depended on parasite developmental stage. Our results support the hypothesis that this acanthocephalan parasite impacts the general anxiety-like circuitry of their intermediate host. Further studies are needed to investigate whether it involves inappropriate processing of information, impaired integration, or altered activation of downstream pathways initiating behavioural action.

Effects of parasites upon non-host predator avoidance behaviour in native and invasive gammarids.

The acanthocephalan parasite, Polymorphus minutus, manipulates its intermediate hosts' (gammarids) behaviour, presumably to facilitate its transmission to the definitive hosts. A fundamental question is whether this capability has evolved to target gammarids in general, or specifically sympatric gammarids. We assessed the responses to chemical cues from a non-host predator (the three-spined sticklebacks Gasterosteus aculeatus) in infected and non-infected gammarids; two native (Gammarus pulex and Gammarus fossarum), and one invasive (Echinogammarus berilloni) species, all sampled in the Paderborn Plateau (Germany). The level of predator avoidance was assessed by subjecting gammarids to choice experiments with the presence or absence of predator chemical cues. We did not detect any behavioural differences between uninfected and infected G. pulex and E. berilloni, but an elevated degree of predator avoidance in infected G. fossarum. Avoiding non-host predators may ultimately increase the probability of P. minutus' of predation by the definitive host. Our results suggested that P. minutus' ability to alter the host's behaviour may have evolved to specifically target sympatric gammarid host species. Uninfected gammarids did not appear to avoid the non-host predator chemical cues. Overall the results also opened the possibility that parasites may play a critical role in the success or failure of invasive species.

Pomphorhynchus laevis manipulates Gammarus pulex behaviour despite salt pollution

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

High food quality increases infection of Gammarus pulex (Crustacea: Amphipoda) by the acanthocephalan parasite Pomphorhynchus laevis

Parasitism is an important process in ecosystems, but has been largely neglected in ecosystem research. However, parasites are involved in most trophic links in food webs with, in turn, a major role in community structure and ecosystem processes. Several studies have shown that higher nutrient availability in ecosystems tends to increase the prevalence of parasites. Yet, most of these studies focused on resource availability, whereas studies investigating resource quality remain scarce. In this study, we tested the impact of the quality of host food resources on infection by parasites, as well as on the consequences for the host. Three resources were used to individually feed Gammarus pulex (Crustacea: Amphipoda) experimentally infected or not infected with the acanthocephalan species Pomphorhynchus laevis: microbially conditioned leaf litter without phosphorus input (standard resource); microbially conditioned leaf litter enriched in phosphorus; and microbially conditioned leaf litter without phosphorus input but complemented with additional inputs of benthic diatoms rich in both phosphorus and eicosapentaenoic acid. During the 110 day experiment, infection rate, parasite load, host survival, and parasite-mediated behavioral traits implicated in trophic transmission were measured (refuge use, geotaxis and locomotor activity). The resources of higher quality, regardless of the infection status, reduced gammarid mortality and increased gammarid growth. In addition, higher quality resources increased the proportion of infected gammarids, and led to more cases of multi-infections. While slightly modifying the geotaxis behavior of uninfected gammarids, resource quality did not modulate the impact of parasites on host behavior. Finally, for most parameters, consumption of algal resources had a greater impact than did phosphorus-enriched leaf litter. Therefore, manipulation of resource quality significantly affected host–parasite relationships, which stressed the need for future research to investigate in natura the relationships between resource availability, resource quality and parasite prevalence.

Inter-population variation in the intensity of host manipulation by the fish acanthocephalan Pomphorhynchus tereticollis: are differences driven by predation risk?

Many trophically-transmitted parasites induce behavioural alteration in their intermediate hosts that tend to increase host vulnerability to predation. Inter-population variability in parasite-induced alterations is expected to arise from variable local opportunities for trophic transmission. Yet, this hypothesis has not been investigated so far. We addressed the issue in four populations of the fish parasite Pomphorhynchus tereticollis (Acanthocephala), using variable fish biomass density as a proxy for transmission opportunities. We found variation in the intensity of parasite-induced changes in phototaxis and refuge use among populations. Two of the populations with the lowest predator biomass exhibited the highest levels of behavioural manipulation and prevalence, as expected at low transmission opportunities. They also exhibited micro-habitat segregation between infected and uninfected gammarids in the field. In addition, infection had variable effects on two physiological defence systems, immunity and antioxidant capacity, and on total protein content. Overall, our study brings partial support to the prediction that host manipulation and prevalence should be higher at low predator biomass. Although stronger evidence should be sought by increasing population replicates, our study points to the importance of the ecological context, specifically transmission opportunities brought about by predation pressure, for the evolution of parasite manipulation in trophically-transmitted parasites.

Activity level and aggregation behavior in the crustacean gammarid Gammarus insensibilis parasitized by the manipulative trematode Microphallus papillorobustus

Hosts manipulated by parasites are profoundly altered organisms exhibiting a broad range of potential modifications. Exploring this multidimensionality is an emerging field. Previous studies have shown that the bird trematode Microphallus papillorobustus induces several behavioural changes in the gammarid Gammarus insensibilis. Knowing that aggregation behaviour and reduced activity levels are strategies that limit predation in other species of amphipods, we explored in this study these behavioural responses for infected and uninfected G. insensibilis in the presence of host and non-host predator olfactory cues (bird faeces and fish mucus). While uninfected individuals reduced their activity level in the presence of predator cues, infected individuals did not change their activity level in presence of aquatic bird faeces. We also studied the gammarid aggregation behaviour. Uninfected gammarids in clean water spent significantly more time in aggregates than did infected individuals. Among the uninfected individuals, the aggregation level tended to increase when bird faeces and fish mucus were added, but the difference was not significant. Among infected individuals, the level of aggregation was significantly increased only with the bird faeces. We discussed our results in the context of the literature on multidimensional manipulations, acknowledging that subtle differences between unparasitized and parasitized gammarids can also be by-products of manipulation on other traits.

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.

Does the carotenoid-based colouration of Polymorphus minutus facilitate its trophic transmission to definitive hosts?

Freshwater gammarids infected with the acanthocephalan parasite Polymorphus minutus show behavioural alterations but also differ from uninfected individuals in their appearance because of the carotenoid-based colouration of the parasite visible through the cuticle. However, it's not clear whether this phenotypic alteration is an adaptation favouring parasite transmission to the definitive host. To test this hypothesis, we investigated the selective preference of mallard towards two prey types: uninfected gammarids on which we applied a dot of inconspicuous brown paint, and uninfected gammarids on which we applied a dot of bright orange paint to mimic the change in appearance due to P. minutus without changes in host behaviour. Mallards showed a significant preference for orange-painted gammarids regardless of how gammarids were distributed (isolated or aggregated). This suggests that parasite's colouration may play a role in enhanced transmission to definitive avian hosts. The role of P. minutus' colouration in the conspicuousness of gammarids has however to be balanced by the extent to which mallards use visual cues to forage in the field. From the perspective of a multidimensional manipulation, this study suggests that the change in appearance may act synergistically with the changes in behaviour to promote transmission to waterbirds.

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.

Impact of olfactory non-host predator cues on aggregation behaviour and activity in Polymorphus minutus infected Gammarus pulex

Parasites with a complex life cycle are supposed to influence the behaviour of their intermediate host in such a way that the transmission to the final host is enhanced, but reduced to non-hosts. Here, we examined whether the trophically transmitted bird parasite Polymorphus minutus increases the antipredator response of its intermediate host, the freshwater amphipod Gammarus pulex to fish cues, i.e. non-host cues (‘increased host abilities hypothesis’). Aggregation behaviour and reduced activity are assumed to decrease the predation risk of gammarids by fishes. Uninfected G. pulex are known to aggregate in the presence of a fish predator. In the present study, gammarids were allowed to choose either to join a group of conspecifics or to stay solitary (experiment 1) or between two groups differing in infection status (experiment 2), both in the presence or absence of fish odour. The perception of the groups was limited to mainly olfactory cues. Contrary to the ‘increased host abilities hypothesis’, in infected gammarids of experiment 1, fish cues induced similar aggregation behaviour as in their uninfected conspecifics. In experiment 2, uninfected as well as infected gammarids did not significantly discriminate between infected and uninfected groups. Although only uninfected gammarids reduced their activity in the presence of predator cues, infected G. pulex were generally less active than uninfected conspecifics. This might suggest that P. minutus manipulates rather the general anti-predator behaviour than the plastic response to predation risk.

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.

Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host

Fish acanthocephalans can modify the antipredator behaviour of their intermediate hosts in response to cues from fish predators. However, it is still unclear whether such behavioural changes are adaptive, or are just the consequence of infection. We addressed this question through studying two acanthocephalans, Pomphorhynchus laevis and Polymorphus minutus, and their intermediate host, the amphipod Gammarus pulex. Pomphorhynchus laevis completes its cycle in a freshwater fish, whereas P. minutus exploits waterbirds as final hosts. We first assessed vulnerability of infected and uninfected gammarids to predation by bullheads, Cottus gobio. Pomphorhynchus laevis-infected gammarids were more susceptible to predation than uninfected ones when a refuge was available, whereas no selective predation on P. minutus-infected individuals was recorded, independently of refuge availability. We then quantified refuge use when a bullhead was present in an enclosure or when the enclosure was empty. Individuals of each group significantly increased refuge use in the presence of a bullhead. However, a larger proportion of P. laevis-infected gammarids remained out of the refuge in the presence of a predator, compared with uninfected controls, whereas no such effect was observed in P. minutus-infected ones. Finally, we assessed reaction to bullhead olfactory cues, using a Y-maze apparatus. Pomphorhynchus laevis-infected gammarids spent significantly more time in the predator-scented arm, whereas the reverse was observed in uninfected ones. Polymorphus minutus-infected individuals, however, did not differ from uninfected controls. We discuss our results in relation with the adaptiveness of host manipulation by parasites.

Pollution-induced heat shock protein expression in the amphipod Gammarus roeseli is affected by larvae of Polymorphus minutus (Acanthocephala)

The relationship between the exposure of organisms to chemicals and subsequent alterations in various biochemical processes (commonly referred to as biomarkers) is of growing importance in environmental and ecotoxicological research. However, parasites which also affect the physiological homeostasis of their hosts, and thus may alter biomarker reactions, are usually ignored in environmental research. To address this deficit, we have used the host-parasite system Gammarus roeseli naturally infected with cystacanths of the acanthocephalan Polymorphus minutus to investigate whether infection of gammarids with parasites alters their heat shock protein response following exposure to palladium (Pd). After 24 days of metal exposure relative levels of heat shock protein hsp70 were analysed in the tissues of parasites and intermediate hosts. Simultaneously, the metal accumulation in gammarids and parasites was determined. As none of the infected gammarids showed hsp70 levels at the end of the Pd exposure (either exposed or not), infected and unparasitized G. roeseli were exposed to heat. Again, only uninfected gammarids showed a temperature-dependent increase in hsp70 levels. Interestingly, although the intermediate hosts showed no hsp70 response, exposure to Pd and heat results in increasing hsp70 in the parasites within in the haemocoel of G. roeseli. Heat experiments with isolated cystacanths also showed increasing hsp70 levels in P. minutus with temperature. Concerning uninfected G. roeseli, exposure to Pd and heat causes a hsp70 response. Pd concentrations were found to be higher in the larval parasites than in the gammarids. This result clearly contradicts previous results, as high metal accumulation was so far only described from adult acanthocephalans. Our findings provide experimental evidence that parasites alter the biomarker responses of their host and that the infection status of test animals is extremely important for ecotoxicological studies.

An acanthocephalan parasite increases the salinity tolerance of the freshwater amphipod Gammarus roeseli (Crustacea: Gammaridae)

Studies of the influence of parasites on host fitness generally conclude that parasites have a strong negative effect on their hosts. In this study, we have investigated experimentally the role of Polymorphus minutus, an acanthocephalan parasite, on the salinity tolerance of the freshwater amphipod Gammarus roeseli, one of its intermediate hosts. Unexpectedly, P. minutus-infected gammarids were more tolerant to salinity stress than uninfected ones. The mean lethal salt concentrations for 50% mortality of hosts tested were 17.3 (infected) and 9.7 g/L (uninfected). The parasitic load (one or two parasites per host) did not affect the result. The size of hosts had no significant influence on the salinity tolerance of either infected or uninfected gammarids. The mobility of all types of gammarid decreased when the salinity exceeded 9.0 g/L, but there was no significant difference between infected and uninfected gammarids. We discuss the higher salinity tolerance of infected amphipods in relation to O(2) consumption and osmoregulation. Finally, we demonstrate that the salinity tolerance is enhanced in the parasitized amphipod but without a significant change in behavior or an osmoregulatory adjustment.

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.

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 effects of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on pairing success in male Gammarus pulex (Crustacea: Amphipoda)

Parasites can decrease male mating success in host species in various ways, in particular by affecting male competitive ability for access to females. However, male-male competition can take different forms (i.e. interference vs exploitation competition) and which type of competition is most affected by parasites is not always clear. We investigated the influence of two acanthocephalan parasites Pomphorhynchus laevis and Polymorphus minutus on the pairing success of their intermediate host, Gammarus pulex, using field-based studies and complementary laboratory-based studies. We first studied male pairing success in the field using four large samples of paired and unpaired individuals collected at different dates. In three of the samples, the effects of size and parasite infection were significant, whereas for one sample only male size had a significant effect. There was no difference in size distributions between infected and uninfected gammarids. Large males were paired more often than smaller males, and uninfected males were paired more frequently than infected males, the pairing success of P. minutus-infected males being more severely affected than that of P. laevis-infected males. We then experimentally tested the ability to enter into precopula with a receptive female in the presence or absence of competitors. In competitive situations, the pairing success of P. laevis- and P. minutus-infected males was significantly lower than that of uninfected males, with pairing success being more affected in P. laevis-infected than in P. minutus-infected males. In the absence of competition, males infected with P. laevis were significantly less likely to enter into precopula compared with uninfected males and P. minutus-infected males, whereas there was no difference between uninfected and P. minutus-infected males in their inclination to pair with a receptive female. However, for both parasites, latency time to pair formation was significantly shorter for uninfected than for infected males. In a third experiment, we tested for a potential effect of vertical segregation on the pairing success of infected and uninfected males, but found no evidence for it. We conclude that infected males may be less competitive than uninfected males in competition by exploitation between males for females.

Depressed Protein and Copper Content of the Midgut Gland in an Intermediate Host, Gammarus pulex (Crustacea), Infected with Cystacanths of Pomphorhynchus laevis (Acanthocephala)

It had previously been shown that hemolymph protein titers (especially hemocyanin) in Gammarus pulex infected with the cystacanth of Pomphorhynchus laevis were significantly elevated above levels in uninfected animals (Bentley and Hurd, 1993). In this study, the protein and copper contents of midgut glands (thought to be hemopoietic tissue) were investigated to determine whether these were affected by infection. The volume of midgut glands from infected gammarids did not differ from uninfected gammarids of the same total wet weight. However, midgut glands from infected gammarids showed a significant depression in total protein concentration (52.33 μg mm -3 ± 5.16 infected versus 82.23 μg mm -3 ± 10.22 uninfected; P < 0.05 Chow test) and gland copper concentration (6.73 mmol mm -3 ± 0.67 infected versus 10.94 mmol mm -3 ± 1.35 uninfected; P < 0.05, Chow test). The possibility that infection induces a shift in resources from the storage organ to the hemolymph is discussed.

Serotonin, octopamine, and the clinging behavior induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea)

Gammarus lacustris infected with cystacanths of Polymorphus paradoxus display an abnormal behavior. They respond to disturbance by swimming to the surface and clinging to a solid object (W. M. Bethel and J. C. Holmes. 1973. J. Parasitol. 59: 945–956). Uninfected gammarids injected with serotonin (1–20 μg/50 mg) but not other neurotransmitters also responded to mechanical stimulation by clinging, but the response lasted for a shorter time than in infected gammarids. Octopamine suppressed the clinging response in infected gammarids for several hours. The results suggest that cystacanths of P. paradoxus modulate the behavior of gammarids through the alteration of neural activity in some serotonin-sensitive or serotonergic central pathway, probably one involved in precopulatory clinging in male amphipods.

Parasite manipulation of host behaviour: acanthocephalans and shrimps in the laboratory

Many parasites, dependent on more than one host to complete their life cycle, can manipulate the appearance and/or behaviour of their intermediate host to facilitate transmission to the definitive host. The acanthocephalan parasite Pomphorhynchus laevis renders its intermediate host, the shrimp Gammarus pulex, more vulnerable to predation by fish. We describe three experiments designed to illustrate this. Experiments 1 and 2 look at the effects of light and habitat on the behaviour of infected and uninfected gammarids. Experiment 3 examines the effectiveness of altered host behaviour and appearance in facilitating predation by the parasite's definitive hosts. Together, the experiments provide undergraduates with an opportunity to study a fascinating and currently popular area of biology embracing both parasitology and ethology.