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.     

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.     

Non-native parasite enhances susceptibility of host to native predators

Parasites often alter host physiology and behavior, which can enhance predation risk for infected hosts. Higher consumption of parasitized prey can in turn lead to a less parasitized prey population (the healthy herd hypothesis). Loxothylacus panopaei is a non-native castrating barnacle parasite on the mud crab Eurypanopeus depressus along the Atlantic coast. Through prey choice mesocosm experiments and a field tethering experiment, we investigated whether the predatory crab Callinectes sapidus and other predators preferentially feed on E. depressus infected with L. panopaei. We found that C. sapidus preferentially consumed infected E. depressus 3 to 1 over visibly uninfected E. depressus in the mesocosm experiments. Similarly, infected E. depressus were consumed 1.2 to 1 over uninfected conspecifics in field tethering trials. We evaluated a mechanism behind this skewed prey choice, specifically whether L. panopaei affects E. depressus movement, making infected prey more vulnerable to predator attack. Counter to our expectations, infected E. depressus ran faster during laboratory trials than uninfected E. depressus, suggesting that quick movement may not decrease predation risk and seems instead to make the prey more vulnerable. Ultimately, the preferential consumption of L. panopaei-infected prey by C. sapidus highlights how interactions between organisms could affect where novel parasites are able to thrive.     

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.     

Nyctiphanes couchii as intermediate host for the acanthocephalan Bolbosoma balaenae in temperate waters of the NE Atlantic

Cystacanths of the acanthocephalan Bolbosoma balaenae (Gmelin, 1790) were found encapsulated in the cephalothorax of the euphausiid Nyctiphanes couchii (Bell, 1853) from temperate waters in the NE Atlantic Ocean. Euphausiids were caught in locations outside the Ría de Vigo in Galicia, NW Spain, and prevalence of infection was up to 0.1%. The parasite was identified by morphological characters. Cystacanths were 8.09 ± 2.25 mm total length (mean ± SD) and had proboscises that consisted of 22 to 24 longitudinal rows of hooks, each of which had 8 or 9 hooks per row including 2 or 3 rootless ones in the proboscis base and 1 field of small hooks in the prebulbar part. Phylogenetic analyses of 18S rDNA and cytocrome c oxidase subunit I revealed a close relationship with other taxa of the family Polymorphidae (Meyer, 1931). The results extend northwards ot the known distribution of B. balaenae. Taxonomic affiliation of parasites and trophic ecology in the sampling area suggest that N. couchii is the intermediate host for B. balenae, and we suggest that the whales Balaenoptera physalus (Linnaeus, 1758) and B. acutorostrata (Lacepède, 1804) are its definitive hosts. This life cycle is probably completed with or without paratenic hosts.     

Sarcocystis cernae: A parasite increasing the risk of predation of its intermediate host,Microtus arvalis

Summary 1)The transmission dynamics of the protozoan parasite Sarcocystis carnae (erná and Louková 1976) (Apicomplexa, Eimeroidea, Sarcocystidae) in natural populations were studied in the Lauwersmeerpolder in the northern Netherlands. This parasite needs two hosts to complete its life cycle; the common vole (Microtus arvalis) as its intermediate host and the kestrel (Falco tinnunculus) which preys on the vole, as its final host. 2) Seasonal variation in prevalence of infection in snap-trapped common voles was determined in two years, 1984 and 1985. It was found to be lowest in November (6% of the voles infected) and it increased gradually to a peak in May (33%). 3) Data collected in three successive kestrel breeding seasons (1983–85) revealed that voles in the kestrel summer diet are infected twice as frequently as those in snap-trap samples, 21% and 9% respectively. This difference (P<0.05, X²-test) suggests that the parasite influences its intermediate host behaviour in such a way that it enhances the probability of parasite transmission to the final host.     

Effects of the protozoan parasite Sarcocystis rauschorum on open-field behaviour of its intermediate vertebrate host, Dicrostonyx richardsoni

Behaviour and activity levels were measured in varying lemmings experimentally infected with the heteroxenous parasite, Sarcocystis rauschorum to test the hypothesis that the parasite alters behaviour of this intermediate host and thereby increases probability of transmission to the definitive host, the snowy owl (Nyctea scandiaca). Measures of short-term activity levels on a running wheel indicated no effect of the parasite, either directly, or indirectly as a result of illness. We observed behaviour of infected lemmings placed in an "open field" (arena). Lemmings would increase their susceptibility to predators if they spent more time away from cover, used crypsis (stationary postures) less, spent more time exploring (especially in unfamiliar areas), or responded inappropriately to threats from predators. We found that only exploratory activity showed significant change after infection. The frequency of exploratory activity increased and became disassociated from the usual fear response. This may increase the lemmings' susceptibility to aerial predation. The mechanism for this effect is unknown, but neurological lesions have been observed. The examination of the modes of transmission of the S. rauschorum parasite within lemming populations and of a possible fecundity compensation strategy adopted by the lemmings, and their relevance to population control, are suggested as areas for future study.     

Altered dopamine levels induced by the parasite Profilicollis antarcticus on its intermediate host, the crab Hemigrapsus crenulatus

A serotonergic pathway is apparently involved in parasite-host interactions. Previous studies conducted in our laboratory showed increased rates in oxygen consumption and alterations in body posture in the crab Hemigrapsus crenulatus parasitized by the acanthocephalan, Profilicollis antarcticus. Such changes may be related to the functions described for biogenic amines in crustaceans. During the infective stage the acanthocephalans live freely in the hemocelomic cavity, suggesting that the possible alteration induced by biogenic amines may be related to their neurohormonal function in crustaceans. To test whether the presence of P. antarcticus produced neurohormonal changes in its intermediate host, H. crenulatus, we analyzed serotonin and dopamine levels in the host using HPLC with electrochemical detection. Two groups of 11 female crabs were studied; one group was artificially inoculated with two cystacanths while the other was used as the control. Our results show a dramatic increase in hemolymph dopamine, but not serotonin in H. crenulatus parasitized by the acanthocephalan P. antarcticus. Our results, along with those reported by Maynard (1996), suggest a parasite-specific strategy involved in the behavior alteration caused by the acanthocephalans on their intermediate host. The use of a biogenic amine as a mechanism of interaction by the parasites gives them an endless number of alternative potential actions on their intermediate hosts.     

Interactions of the malaria parasite and its mammalian host

A hallmark of Plasmodium development inside its mammalian victim is the remarkable restriction to the host species. Adaptation to an intracellular life style in specific target cells is determined by multiple parasite-host interactions. The first line of crosstalk occurs during intradermal sporozoite injection by an Anopheles mosquito. The following expansion in the liver is highly efficient and leads to successful establishment of the parasite population. During the periodic waves of fevers and chills the parasite destroys and re-infects red blood cells. Recent advances in experimental genetics and imaging techniques begin to expose the complex interactions at the changing parasite-host interfaces. Understanding the cellular and molecular mechanisms of target cell recognition, nutrient acquisition, and hijacking of cellular and immune functions may ultimately explain the elaborate biology of a medically important single cell eukaryote.     

Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: consequences for the risk of super-infection and links with host behavioural manipulation

Parasite survival in hosts mainly depends on the capacity to circumvent the host immune response. Acanthocephalan infections in gammarids are linked with decreased activity of the prophenoloxidase (ProPO) system, suggesting an active immunosuppression process. Nevertheless, experimental evidence for this hypothesis is lacking: whether these parasites affect several immune pathways is unknown and the consequences of such immune change have not been investigated. In particular, the consequences for other pathogens are not known; neither are the links with other parasite-induced manipulations of the host. Firstly, using experimental infections of Pomphorhynchus laevis we confirmed that the lower immune activity in parasitised Gammarus pulex is induced by the parasite infection. Second, using natural infections of three different parasites, P. laevis, Pomphorhynchus tereticollis and Polymorphus minutus, we showed that acanthocephalan infection was associated with reduction of the activity of the ProPO system and the haemocyte concentration (two major parameters of crustacean immunity) suggesting that immune depression is a phenomenon affecting several immunological activities. This was confirmed by the fact that acanthocephalan infection (whatever the parasite species) was linked to a lower efficiency to eliminate a bacterial infection. The result suggests a cost of parasite immune depression. Finally, acanthocephalans are also known to induce behavioural alterations in the intermediate host which favour their transmission to definitive hosts. We did not find any correlation between behavioural and immunological alterations in both experimentally and naturally-infected gammarids. Overall, this study suggests that whilst immune depression might be beneficial to acanthocephalan survival within the intermediate gammarid host, it might also be costly if it increases host mortality to additional infections before transmission of the parasite.     

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.     

Reproductive traits of the acanthocephalan Neoechinorhynchus brentnickoli in the definitive host

The Acanthocephala constitute a group of helminth parasites that, as adults, infect all classes of vertebrates. Adults of Neoechinorhynchus brentnickoli are parasites of Dormitator latifrons, a commercially important fish species in Tres Palos Lagoon, Guerrero, Mexico. The aim of this study was to describe features of the reproductive biology of this acanthocephalan. Fish were collected from Laguna de Tres Palos during February 2012 to February 2013. The number of fish that were examined (n=688) ranged from 35 (June) to 70 (August) in each collection. The prevalence of infection was more than 90% during this period and mean abundance varied significantly from 32.3 worms per fish (July 2012) to 89.3 worms per fish (March 2012). Acanthocephalans were reproductively active during the whole year. The stomach was the region of the digestive tract with the smallest percentage of helminths, and females were more abundant than males in all sections of the intestine. Larger male and female worms were always located in the more posterior sections of the digestive tract. The mean length at which 50% of individuals reached sexual maturity was 2.9 mm for females and 2.3 mm for males. Relative fecundity increased with length in females.     

Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophallus sp

The complex life cycle of digenean trematodes with alternating stages of asexual multiplication and sexual reproduction can generate interesting within-host population genetic patterns. Metacercarial stages found in the second intermediate host are generally accumulated from the environment. Highly mobile second intermediate hosts can sample a broad range of cercarial genotypes and accumulate genetically diverse packets of metacercariae, but it is unclear whether the same would occur in systems where the second intermediate host is relatively immobile and cercarial dispersal is the sole mechanism that can maintain genetic homogeneity at the population level. Here, using polymorphic microsatellite markers, we addressed this issue by genotyping metacercariae of the trematode Gymnophallus sp. from the New Zealand cockle Austrovenus stutchburyi. Despite the relatively sessile nature of the second intermediate host of Gymnophallus, very high genotypic diversity of metacercariae was found within cockles, with only two cockles harbouring multiple copies of a single clonal lineage. There was no evidence of population structuring at the scale of our study, suggesting the existence of a well-mixed population. Our results indicate that (i) even relatively sessile second intermediate hosts can accumulate a high diversity of genotypes and (ii) the dispersal ability of cercariae, whether passive or not, is much greater than expected for such small and short-lived organisms. The results also support the role of the second intermediate host as an accumulator of genetic diversity in the trematode life cycle.     

Advanced phenology of intraguild predators shifts herbivore host plant preference and performance

1. The abundance of insect herbivores is mediated by interactions with higher and lower trophic levels. This research asks (i) how phenological change across trophic levels affects host plant quality and selection for aphids, and (ii) what higher trophic level mechanisms drive aphid abundance. 2. Ligusticum porteri is a perennial host for the sap-feeding aphid Aphis asclepiadis and intraguild mirid predators (chiefly Lygus hesperus) in Colorado. We used long-term observational data to discover that aphids and mirids respond differently to phenological cues. These unique responses can impact aphid abundance through changes to host plant selection and quality. 3. We used behavioural choice assays to assess how advanced mirid phenology influences aphid host plant selection. More alates landed and reproduced on mirid-free control plants relative to host plants with prior mirid feeding. However, this preference did not correlate with aphid performance when we compared aphid relative growth rates between treatments. This suggests that advanced mirid phenology would impact aphid populations more through host plant choice, rather than reductions in host quality. The addition of mirids to experimental aphid colonies also demonstrated reduced aphid colony growth via predation. 4. We measured plant cues involved in host selection and found differences in volatile composition between plants with prior mirid feeding compared to control plants, providing the potential for aphids to detect enemy-free space using volatile cues.     

A parasite reveals cryptic phylogeographic history of its host

This study compares the continental phylogeographic patterns of two wild European species linked by a host-parasite relationship: the field mouse Apodemus sylvaticus and one of its specific parasites, the nematode Heligmosomoides polygyrus. A total of 740 base pairs (bp) of the mitochondrial cytochrome b (cyt b) gene were sequenced in 122 specimens of H. polygyrus and compared with 94 cyt b gene sequences (974 bp) previously acquired for A. sylvaticus. The results reveal partial spatial and temporal congruences in the differentiation of both species' lineages: the parasite and its host present three similar genetic and geographical lineages, i.e. Western European, Italian and Sicilian, and both species recolonized northwestern Europe from the Iberian refuge at the end of the Pleistocene. However, H. polygyrus presents three particular differentiation events. The relative rate of molecular evolution of the cyt b gene was estimated to be 1.5-fold higher in the parasite than in its host. Therefore, the use of H. polygyrus as a biological magnifying glass is discussed as this parasite may highlight previously undetected historical events of its host. The results show how incorporating phylogeographic information of an obligate associate can help to better understand the phylogeographic pattern of its host.     

Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.