Infected Amphipods Research Articles

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.

Diversity of trematode genetic clones within amphipods and the timing of same-clone infections

The genetic diversity of trematodes within second intermediate hosts has important implications for the evolution of trematode populations as these hosts are utilized after the parasites reproduce asexually within first intermediate hosts and before sexual reproduction within definitive hosts. We characterised the genetic clonal diversity of the marine trematode Maritrema novaezealandensis within amphipod ( Paracalliope novizealandiae) second intermediate hosts using four to six microsatellite loci to determine if multiple copies of identical trematode clones existed within naturally infected amphipods. To determine the relative timing of infections by identical clones within hosts, trematode metacercariae were assigned to six developmental stages and the stages of identical clones were compared. The genotypes of 306 trematodes were determined from 44 amphipods each containing more than one trematode. Six pairs of identical trematode clones were recovered in total (representing five amphipods: 11% of amphipods with greater than one trematode) and all pairs of clones belonged to the same developmental stage. This suggests that identical clone infections are effectively synchronous. A general decrease in the number of metacercariae recovered, prevalence, and mean intensity of infection for each subsequent developmental stage coupled with large numbers of metacercariae (>9) only being recovered from recent infections, supports the occurrence of post-infection amphipod mortality and/or within-host trematode mortality. Taken together, our results indicate that natural infections are characterised by high genetic diversity, but that amphipods also periodically encounter “batches” of genetically identical clones, potentially setting the stage for interactions within and between clonal groups inside the host.

Effects of the trematode Maritrema novaezealandensis on the behaviour of its amphipod host: adaptive or not?

There are many recorded cases of parasites that are capable of altering the behaviour of their host to enhance their transmission efficiency. However, not all of these cases are necessarily the results of the parasites actively manipulating host behaviour; they may rather be the 'by-products' of pathology caused by the parasite's presence. This study investigates the effect of the microphallid trematode Maritrema novaezealandensis on the behaviour of one of its crustacean intermediate hosts, the amphipod Paracalliope novizealandiae. Uninfected amphipods were experimentally infected by exposure to M. novaezealandensis cercariae. The activity level and vertical position of experimentally infected amphipods were compared with uninfected amphipods at 2 weeks and 6 weeks post-infection, i.e. both before and after the parasite achieved infectivity to its definitive host. Infected amphipods were found to exhibit significantly lower levels of activity and to occur significantly lower in the water column than uninfected controls during both periods. Based on the timing of the change in behaviour exhibited by infected amphipods, the results suggest that the altered behaviour exhibited by P. novizealandiae infected with M. novaezealandensis is most likely due to pathology caused by the parasite rather than a case of active, and adaptive, behavioural manipulation.

Host manipulation of a freshwater crustacean ( Gammarus roeseli) by an acanthocephalan parasite ( Polymorphus minutus) in a biological invasion context

Several gammarid species serve as intermediate hosts for the acanthocephalan parasite Polymorphus minutus. This parasite influences gammarid behaviour in order to favour transmission to its ultimate host, generally a bird. We investigated this host manipulation in Gammarus roeseli, a gammarid species introduced in France 150 years ago which now coexists with several exotic species from different origins. In the field, vertical distribution of G. roeseli revealed a higher proportion of infected individuals close to the water’s surface and the size distribution of infected gammarids revealed predation pressure on infected individuals. However, under laboratory conditions both infected and non-infected individuals remained benthic. The addition of a second gammarid, Dikerogammarus villosus, to the experimental device involved a vertical displacement of infected G. roeseli towards the water’s surface. Dikerogammarus villosus, originating from the Ponto-Caspian basin, can be considered as an aggressive predator. The substitution of D. villosus with Atyaephyra desmarestii, a planktivore decapod, did not alter the gammarids’ distribution, with both infected and uninfected G. roeseli staying benthic. Thus, biotic interactions between D. villosus and G. roeseli represent selective pressure encouraging the expression of manipulated behaviour in infected amphipods. Through manipulation, P. minutus was found to increase the survival of infected G. roeseli when faced with non-host predators and to make it more vulnerable to predation by the parasite’s definitive host.

VIRULENCE OF CORYNOSOMA CONSTRICTUM (ACANTHOCEPHALA: POLYMORPHIDAE) IN HYALELLA AZTECA (AMPHIPODA) THROUGHOUT PARASITE ONTOGENY

Development and growth of parasites depend on resources provided by the host and the parasite's ability to use them. Identifying specific costs incurred by the host provides insight for assessment of parasite energy budgets, which differ among taxa and ontogenetic stages. Data from this study were analyzed using an accelerated failure-time model with intensity as a covariate. Results indicated significantly reduced survival of amphipods, Hyalella azteca, infected with the acanthocephalan Corynosoma constrictum compared with uninfected controls. Male and female amphipod survivorship and infection intensity did not differ; however, amphipods with high-intensity infections (> 16 larvae) died earlier compared with amphipods with low-intensity infections (< 3 larvae). The majority of infected amphipods died between 12 and 24 days postexposure, a period of rapid larval development. It is hypothesized that host death may be due either to an increase in overall larval nutritional demands or to parasite-mediated depletion of a specific host substance. Results from this study suggest that developing C. constrictum satisfies energy requirements by depriving amphipod hosts of resources normally used for somatic growth and maintenance.

Pathogenicity of the hymenolepidid cestodeMicrosomacanthus hopkinsiin its intermediate host,Hyalella azteca: implications for transmission, host fitness, and host populations

Infection by larval parasites can have severe consequences on intermediate hosts that affect transmission, fecundity and fitness of the host, and host population structure. This study examines the pathogenic effects of cysticercoid larvae of the hymenolepidid cestode Microsomacanthus hopkinsi (Schiller, 1951) on its amphipod intermediate host, Hyalella azteca Saussure, 1858. There was a significant, positive relationship between oncosphere consumption, cysticercoid burden, and age in short-term experiments in which groups of H. azteca were exposed individually to single egg packets of M. hopkinsi during instars 1, 2, 3, 4, 6, 8, and 9; however, there was no correlation between oncosphere consumption and the intensity of infection in the amphipod hosts within each instar. The mean number of moults over a 14 day experimental period was significantly less in infected amphipods than in their respective controls. In short-term experiments, the greatest mortality appeared to be limited to amphipods exposed during the earliest instars; little mortality was observed in amphipods exposed during instar 4 or later. Long-term experiments revealed a significant negative effect of infection on the overall life span of both male and female H. azteca exposed individually to a single egg packet during instar 4. Of 72 females infected during instar 4 and provided with mates during instar 6, only 1 and 4 produced broods in instars 8 and 9, respectively, compared with 58 and 57 of 72 control females. Broods produced by infected females were significantly smaller than those of control females. Infected individuals were less likely to mate successfully. The results are discussed in terms of their consequences for transmission, host fitness, and potential effects on host populations.

THE BEHAVIORAL RESPONSE OF AMPHIPODS HARBORING CORYNOSOMA CONSTRICTUM (ACANTHOCEPHALA) TO VARIOUS COMPONENTS OF LIGHT

Many studies have shown that photic behavior of amphipods is subject to parasitic manipulation. However, all these investigations have focused on but one property of light (i.e., intensity). This study investigated the possibility that variable wavelength sensitivity, as a potentially important component of amphipod ecology, is subject to parasitic manipulation. The photic behavior of freshwater amphipods Hyalella azteca, infected with the duck acanthocephalan Corynosoma constrictum, was tested. The phototactic responses of infected and uninfected amphipods to various wavelengths in the visible spectrum were compared, and to delineate the effects of intensity and wavelength on behavior, the preferences of amphipods for environments characterized by various combinations of light intensity and wavelength were determined. Response to blue light (400-450 nm) was little affected by infection. Amphipod response to higher red region wavelengths (600-700 nm) was altered by infection. Infected amphipods were significantly less responsive to green region light (500-550 nm), which could lead to increased wandering throughout the water column, thereby facilitating increased parasite transmission through increased predation risk. This study reinforces the subtlety with which parasites can alter their host's behavior, presumably resulting in an increased probability of being transmitted from the intermediate host to a definitive host.

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.

Effect of cystacanth body size on adult success.

Laboratory-reared cystacanths of Leptorhynchoides thecatus (Acanthocephala: Rhadinorhynchidae) were used to study the effect of cystacanth size on adult success and the factors that influence cystacanth size within the intermediate host. To assess how host size and intensity of infection influence cystacanth size, infected amphipods (Hyalella azteca) were measured, and sex, length, and width of cystacanths were determined. After a subset of cystacanths was measured, small- and large-size classes of cystacanths were designated. To determine how cystacanth size relates to adult size, green sunfish (Lepomis cyanellus) were fed 10 large or small cystacanths. Fish were dissected 6 wk after infection, and worms were removed. After adult worms were permanently mounted on slides, their length and width were measured. Intensity of infection and amphipod size significantly influenced cystacanth size in that large amphipods harbored larger cystacanths than did small amphipods and heavy infections produced smaller cystacanths than did light infections. Adult worms from the small and large cystacanth-size classes showed no significant difference in size; however, large cystacanths had a significantly higher establishment and survival than did small cystacanths: 40% of large worms and 14% of small worms were recovered. The results of this study indicate that host size and host sharing influence cystacanth size and that cystacanth size is an important factor in determining adult success.

A parasite spatially structures its host population

Acanthocephalan parasites are capable of altering the behavior of their intermediate amphipod hosts by inducing hyperactivity and increasing downstream drift. We used a laboratory and field study to investigate how Echinogammarus stammerii amphipods infected by the acanthocephalan Pomphorhychus laevis compensated for downstream displacement and responded to a fish extract predator cue. Experiments conducted in laboratory streams showed infected amphipods drifted more and compensated for drift less than non‐infected individuals. When fish extract was added to the channels, non‐infected individuals decreased their activity while infected individuals did not. A field study examined the up‐ and down‐stream movements of a population of E. stammerii infected with P. laevis in the River Brenta, Italy. Drift by E. stammerii was positively influenced by acanthocephalan infection. Infected amphipods made up 40% of the drift but accounted for just 5% of the E. stammerii population. Infected individuals, however, were under‐represented among upstream‐moving amphipods collected from the main river channel and a near‐shore migration column, comprising only 3% of sampled individuals. These data suggest that infected individuals may be effectively displaced downstream, creating a mechanism for spatial separation of the non‐infected and infected sub‐populations.

Inequalities in size and intensity-dependent growth in a mermithid nematode parasitic in beach hoppers.

Inequality in body sizes is a common feature in populations of helminth parasites, with potential consequences for egg production and population genetics. Inequalities in body lengths and the effects of intraspecific competition on worm length were studied in a species of mermithid nematode parasitic in the crustacean Talorchestia quoyana (Amphipoda: Talitridae). The majority of the 753 worms recovered were relatively small, and an analysis using a Lorenz curve and Gini coefficient suggested that there were no marked inequalities in body lengths among the worms. Total worm length in the 356 infected amphipods (i.e. the sum of the lengths of all the worms in a host) increased steadily as a function of the number of worms per amphipod, whereas the length of the longest worm per amphipod peaked in amphipods harbouring intermediate numbers of worms. This last result was not significantly accounted for by the observed increase in host size with increasing intensity of infection, but resulted from a correlation between worm length and host size. As the number of worms per amphipod increased, the relative sizes of the second-, third-, and fourth-longest worms per host increased markedly. This means that relative inequalities in sizes become less pronounced, i.e. subordinate worms get closer in size to the longest worm, as the number of worms per host increases. The main consequence of this phenomenon is that worm sizes in the mermithid population are more homogeneous than they would be if intraspecific competition had stronger effects on worm growth.

Parasitism and the burrowing depth of the beach hopper Talorchestia quoyana (Amphipoda: Talitridae)

Talitrid amphipods spend their days burrowed in sand to avoid predators as well as desiccation and heat stress, although other factors may influence burrowing depth. We investigated the potential role of mermithid nematode parasites in determining burrowing depth in the amphipod Talorchestia quoyana. Mermithids grow as parasites inside amphipods until they reach adulthood, when they must emerge from their host into moist sand to complete their life cycle and reproduce. When allowed to burrow to a depth of their choice in experimental situations, large amphipods burrowed deeper than small ones. In addition, deep-burrowing amphipods were more likely to be infected by mermithid nematodes, and harboured longer worms, on average, than amphipods that burrowed close to the sand surface. This last result is not an artefact of the larger size of deep-burrowing amphipods: the increase in worm length with increasing depth was found after statistical correction for host size. In other words, amphipods that burrowed deeper harboured longer worms than expected based on their body size, whereas those that stayed near the surface of the sand column harboured worms shorter than one would expect based on host size. This implies that the greater burrowing depth of infected amphipods is a consequence, and not a cause, of infection. These results emphasize the importance of parasitism as a determinant of the small-scale spatial distribution of their hosts.

Conflict of interest between a nematode and a trematode in an amphipod host: test of the "sabotage" hypothesis

Microphallus papillorobustus is a manipulative trematode that induces strong behavioural alterations in the gamaridean amphipod Gammarus insensibilis, making the amphipod more vulnerable to predation by aquatic birds (definitive hosts). Conversely, the sympatric nematode Gammarinema gammari uses Gammarus insensibilis as a habitat and a source of nutrition. We investigated the conflict of interest between these two parasite species by studying the consequences of mixed infection on amphipod behaviour associated with the trematode. In the field, some amphipods infected by the trematode did not display the altered behaviour. These normal amphipods also had more nematodes, suggesting that the nematode overpowered the manipulation of the trematode, a strategy that would prolong the nematode's life. We hypothesize that sabotage of the trematode by the nematode would be an adaptive strategy for the nematode consistent with recent speculation about co-operation and conflict in manipulative parasites. A behavioural test conducted in the laboratory from naturally infected amphipods yielded the same result. However, exposing amphipods to nematodes did not negate or decrease the manipulation exerted by the trematode. Similarly, experimental elimination of nematodes from amphipods did not permit trematodes to manipulate behaviour. These experimental data do not support the hypothesis that the negative association between nematodes and manipulation by the trematode is a result of the "sabotage" hypothesis.

Review of experimental and natural invertebrate hosts of sealworm (&lt;i&gt;Pseudoterranova decipiens&lt;/i&gt;) and its distribution and abundance in macroinvertebrates in eastern Canada

Experimental and natural invertebrate intermediate hosts of sealworm (Pseudoterranova decipiens) as well as transmission experiments of sealworm from invertebrates to fish are reviewed and summarized. Experimental hosts include copepods, mysids, cumaceans, isopods, amphipods, decapods, annelids, and molluscs. Invertebrates collected from eastern Canada between 1989 and 1995 were checked for nematode infections by microscopic examination of dissected animals or enzymatic digestion of bulk samples. Third-stage larval sealworm were found in mysids (Neomysis americana, Mysis stenolepis) from Passamaquoddy Bay, the Bras d’Or Lakes, inshore Cape Breton, Sable Island and Sable Island Bank. Infected amphipods (Amphiporeia virginiana, Americorchestia megalophthalma, Gammarus spp.) were found only on Sable Island. Typical infection rates in macroinvertebrates were 1-4/1000. No sealworm infections were found in approximately 18,000 amphipods examined from Sable Island Bank, the site of the most heavily infected fishes in eastern Canada. In Wallace Lake, a brackish pond on Sable Island, infection rates were much higher in mysids than in amphipods. Estimates of rates of transmission of sealworm from invertebrates to fish were derived from infection levels in Wallace Lake and feeding experiments involving sticklebacks and invertebrate prey. It is concluded that mysids may be much more important than amphipods in transmitting sealworm to fish hosts.

AN EMPIRICAL MODEL OF THE OPTIMAL TIMING OF REPRODUCTION FOR FEMALE AMPHIPODS INFECTED BY TREMATODES

Life-history theory predicts that hosts should reproduce when first infected by parasites if hosts are capable and if parasites have a lower cost on current than on future reproduction of hosts. We constructed an empirical model to explore fitness of females of the intertidal amphipod Corophium volutator that reproduced soon versus long after infection by the trematode Gynaecotyla adunca. For uninfected females, the optimal time to reproduce was at their maximum body length. However, for females infected by low or high intensities of trematode metacercariae, reproductive potential (realized fecundity) was highest for females that mated immediately after becoming infected. Even after removing a high cost of delaying reproduction for infected amphipods (high likelihood of depredation by sandpipers, which are final hosts of G. adunca), realized fecundity remained highest if reproduction occurred immediately following infection by trematodes. Results from our model support the view that early reproduction of female amphipods following infection by G. adunca is an adaptive life-history response to parasitism.

Species associations among larval helminths in an amphipod intermediate host

Larval helminths that share the same intermediate host may or may not also share the same definitive hosts. If one or more of these helminth species can manipulate the phenotype of the intermediate host, there can be great advantages or severe costs for other helminths resulting from co-occurring with a manipulator, depending on whether they have the same definitive host or not. Among 2372 specimens of the amphipod Echinogammarus stammeri collected from the river Brenta, northern Italy, there was a positive association between two acanthocephalan species with the same fish definitive hosts, the relatively common Pomphorhynchus laevis and the much less prevalent Acanthocephalus clavula.The number of cystacanths of P. laevis per infected amphipod, which ranged from one to five, did not influence the likelihood that the amphipod would also host A. clavula. A third acanthocephalan species, Polymorphus minutus,which matures in birds, showed no association with either of the two other species. These results show that associations among helminth species in intermediate hosts are not random, and are instead the product of selection favouring certain pathways of transmission.

Male amphipods increase their mating effort before behavioural manipulation by trematodes

Certain parasites appear to alter the behaviour of intermediate hosts, making them more susceptible to predation by final hosts (adaptive parasite manipulation). In some cases, however, hosts are expected to respond by increasing their reproductive effort when first parasitized (adaptive host response). We tested predictions of these two hypotheses for males of the amphipod Corophium volutator (Pallas). Consistent with adaptive parasite manipulation, males infected by the trematode Gynaecotyla adunca (Linton) were likely to crawl on the surface of a mud flat, but only when visual predation by the final host, semipalmated sandpipers, Calidris pusilla L., was likely (during the day), and after trematodes had developed to their infective stage. Males appeared to compensate for parasitism by being more likely to mate, and perhaps by increasing ejaculate size. However, parasitized males that mated when first infected were less likely to mate again once their parasites reached their infective stage, despite their increased crawling at that time, which is associated with mate searching. We did not find that trematodes reduced host survival, apart from expected increases in predation rate on amphipods; in fact, highly infected amphipods actually lived longer than lightly infected ones. Taken together, our results suggest that adaptive host responses can occur before parasite manipulation is realized.

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.

Uptake of lead by Pomphorhynchus laevis cystacanths in Gammarus pulex and immature worms in chub (Leuciscus cephalus).

The uptake of lead by cystacanths of the acanthocephalan Pomphorhynchus laevis in naturally infected amphipods, Gammarus pulex, and by immature parasites in experimentally infected fish, Leuciscus cephalus, was examined following 3-week experimental exposures (0.01 and 0.1 mg l(-1) Pb2+). Both G. pulex and the cystacanths of P. laevis accumulated lead but concentrations in the parasites were lower than in the host tissues at the low lead dose and significantly lower at the high dose. P. laevis from chub exposed to 0.01 mg l(-1) lead contained significantly more of the metal than the tissues of their host. Interestingly, there was an increase in the mean lead levels in the parasites from the control chubs which was concurrent with a decrease in host tissue concentrations. The results of this experimental study therefore confirm previous suggestions that heavy metals are predominantly accumulated by acanthocephalans inside the fish definitive host and not by cystacanths in the haemocoel of the amphipod intermediate host. The microhabitat of the parasite is therefore of primary importance rather than its developmental stage. Furthermore, metal concentrations in adult acanthocephalans will respond rapidly to changes in environmental exposure of their hosts.

Transmission of the sealworm, Pseudoterranova decipiens (Krabbe), from invertebrates to fish in an enclosed brackish pond

The life cycle and transmission dynamics of sealworm, Pseudoterranova decipiens (Krabbe), were studied in Wallace Lake, an enclosed brackish pond on Sable Island, Nova Scotia. Abundance of larval sealworm was determined in amphipods ( Gammarus spp. ), mysids ( Neomysis americana S.L. Smith), and threespine ( Gasterosteus aculeatus Linnaeus) and fourspine ( Apeltes quadracus Mitchill) sticklebacks. Sealworm larvae were more numerous in mysids (0.001–0.004 worms/host) than in amphipods (0–0.0005 worms/host), and P. decipiens abundance in mysids and fourspine stickleback was positively correlated. Amphipods outnumbered mysids in three depth zones in the lake, but density of infected mysids (1.43/m 2) was much higher than that of infected amphipods (0.22/m 2) in the vegetated zone where fish were found. Threespine and fourspine stickleback fed mainly on copepods (98% and 57% of diets, respectively), and less frequently on amphipods (1% and 23% of diets, respectively) and mysids (1% and 19% of diets, respectively). Both sticklebacks fed preferentially on mysids (Murdoch's index of preference=1.49) over amphipods (Murdoch's index=0.67). In separate feeding experiments, fourspine stickleback ingested 1.3 (±1.2) amphipods or 7.7 (±2.0) mysids per day. Calculated transmission rates suggest that these fish acquire sealworm from eating infected mysids at a rate of about 1 per month, compared to 1 every 8 yr from amphipods. Abundance of larval sealworm in N. americana on Sable Island Bank (0.002 worms/host) in January 1995 was similar to that in Wallace Lake. Results of this study demonstrate that mysids are more important than amphipods in transmission of sealworm to small benthophagous fishes in an isolated, landlocked brackish-water environment.