Transmammary infection of paratenic and definitive hosts with Alaria marcianae (trematoda) mesocercariae

Transmammary infection with Alaria marcianae mesocercariae was demonstrated using mice as model, paratenic hosts. Prenatal transmission was ruled out because neonates removed immediately postpartum from infected dams were never infected. Mesocercarial distribution in virgin females and in females examined immediately postpartum showed no marked preference for the mammary glands. In contrast, infection of neonates that were allowed to suckle on infected dams was absolute, and the number of mesocercariae in the mammary glands of postparturient dams that suckled their young was increased significantly. These experimental observations were coupled with other observations on paratenic hosts to outline the pathways open to mesocercariae in gravid hosts. The term amphiparatenic host is coined for those host species that are paratenic hosts as adults, but as juveniles can serve as definitive hosts.     

Transmission of Ancylostoma caninum and Alaria marcianae in coyotes (Canis latrans)

One of seven female coyotes (Canis latrans) captured in Webb County, Texas during September 1986 and confined and mated in holding facilities at Millville, Utah whelped the following spring. The maternal female (greater than 5-yr-old) and her five neonates were killed at 22 days postparturition. All were infected with adult Ancylostoma caninum and were passing eggs in their feces. Also, the neonates and maternal female were infected with immature and adult Alaria marcianae, respectively. These findings suggested that the transmammary route is an important transmission mechanism for acquisition of these species of helminths in coyotes. The lack of overdispersion in the frequency distribution of these parasites and infection of the entire litter indicated that transmission from the infected female was nonselective among the pups.     

Transmammary transmission of mesocercariae of Alaria marcianae (Trematoda) in experimentally infected primates

A lactating primate, Callithrix jacchus, was infected experimentally with 600 mesocercariae of Alaria marcianae 10 days after parturition to determine if she would transmit the mesocercariae to her offspring. Her twin infants were examined 4 wk postinoculation and 16 mesocercariae were found in their tissues. The female was mated again and gave birth to a litter of triplets. She was not given additional mesocercariae. One infant died within hours of birth without suckling and was found negative for any stage of A. marcianae. The other 2 were allowed to nurse for 5 wk, examined and found to be infected with a total of 115 mesocercariae in various tissues, 1 metacercaria in the lungs, and 1 immature and 2 fully formed ovigerous adults in the small intestines. The female was examined at the same time and 246 mesocercariae were recovered. No other stage was found. Histological examination of her mammary glands revealed numerous mesocercariae in the milk-laden alveoli.     

Common sculpin Cottus gobio as a natural paratenic host of Proteocephalus longicollis (Cestoda: Proteocephalidae), a parasite of salmonids, in Europe.

Common sculpins Cottus gobio L. (Pisces: Cottidae), from the Mlynsky Brook near Ceské Zleby in the Sumava National Park, southwestern Bohemia, Czech Republic, were found to harbour in their intestines juvenile cestodes Proteocephalus longicollis (Zeder, 1800), a common parasite of holarctic salmonids, with a prevalence of 60% and intensity of 1 to 11 (mean 5) parasites per fish; undoubtedly, these prey fish serve as paratenic hosts. In this locality, the definitive host of P. longicollis is the brown trout Salmo trutta m. fario L., large specimens of which apparently acquire infection of this parasite by feeding on infected sculpins. C. gobio is the first known natural paratenic host of P. longicollis in Europe.     

Transmammary infection of free-ranging Florida panther neonates by Alaria marcianae (Trematoda: Diplostomatidae)

Two freshly-dead female Florida panther (FP) neonates, Puma concolor couguar (=Puma concolor coryi), an 11-day-old and a 17-day-old, were collected in the Florida Panther National Wildlife Refuge (26 degrees 14'N, 81 degrees 36'W), Collier County, Florida. The 2 neonates were siblings and had presumably fed only on milk from the dam since birth. A 12-day-old female FP neonate was collected in the Big Cypress National Preserve (26 degrees 05'N, 81 degrees 15'W), Collier County, Florida and had also fed only on milk from the dam since birth. Milk was the only food item found in the gastrointestinal tract of these neonates. Mesocercariae and diplostomula of Alaria marcianae were collected from the lungs of the 3 neonates, indicating a transmammary route of infection. No mesocercariae, diplostomula, or mature A. marcianae were seen in the stomach or small intestine. The probable paratenic host for the A. marcianae infection in the adult Florida panther is the raccoon (Procyon lotor).     

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Intraspecific competition between co-infecting parasites can influence the amount of virulence, or damage, they do to their host. Kin selection theory dictates that infections with related parasite individuals should have lower virulence than infections with unrelated individuals, because they benefit from inclusive fitness and increased host longevity. These predictions have been tested in a variety of microparasite systems, and in larval stage macroparasites within intermediate hosts, but the influence of adult macroparasite relatedness on virulence has not been investigated in definitive hosts. This study used the human parasite Schistosoma mansoni to determine whether definitive hosts infected with related parasites experience lower virulence than hosts infected with unrelated parasites, and to compare the results from intermediate host studies in this system. The presence of unrelated parasites in an infection decreased parasite infectivity, the ability of a parasite to infect a definitive host, and total worm establishment in hosts, impacting the less virulent parasite strain more severely. Unrelated parasite co-infections had similar virulence to the more virulent of the two parasite strains. We combine these findings with complementary studies of the intermediate snail host and describe trade-offs in virulence and selection within the life cycle. Damage to the host by the dominant strain was muted by the presence of a competitor in the intermediate host, but was largely unaffected in the definitive host. Our results in this host–parasite system suggest that unrelated infections may select for higher virulence in definitive hosts while selecting for lower virulence in intermediate hosts.     

Nematode transmission patterns

The transmission of nematode parasites of vertebrates is reviewed with special reference to the phenomena of monoxeny, heteroxeny, paratenesis, and precocity. Monoxeny is divided into 2 types. Primary monoxeny assumes that there was never an intermediate host in the transmission. Secondary monoxeny assumes the loss of an intermediate host during the course of evolution and its replacement by a tissue phase in the final host. Heteroxeny, or the use of intermediate hosts, is a common feature of many nematode groups. The Spirurida utilize arthropods, the Metastrongyloidea molluscs, and Ascaridida arthropods and vertebrates. Paratenesis, or the use of transport hosts, is a common feature of the transmission of nematode parasites of carnivores. It is postulated that in some instances paratenic hosts have become intermediate hosts and replaced the original intermediate host. Precocity in the development of nematodes in intermediate hosts (including what may have been paratenic hosts) is defined as growth and/or development beyond the expected. Its occurrence among the nematode parasites of vertebrates is reviewed. It is regarded as a transmission strategy which accelerates gamete production in the final host. Precocity could also provide the mechanism for the transfer of a parasite from a predator final host to a prey final host.     

Conflict between parasites with different transmission strategies infecting an amphipod host

Competition between parasites within a host can influence the evolution of parasite virulence and host resistance, but few studies examine the effects of unrelated parasites with conflicting transmission strategies infecting the same host. Vertically transmitted (VT) parasites, transmitted from mother to offspring, are in conflict with virulent, horizontally transmitted (HT) parasites, because healthy hosts are necessary to maximize VT parasite fitness. Resolution of the conflict between these parasites should lead to the evolution of one of two strategies: avoidance, or sabotage of HT parasite virulence by the VT parasite. We investigated two co-infecting parasites in the amphipod host, Gammarus roeseli: VT microsporidia have little effect on host fitness, but acanthocephala modify host behaviour, increasing the probability that the amphipod is predated by the acanthocephalan's definitive host. We found evidence for sabotage: the behavioural manipulation induced by the Acanthocephala Polymorphus minutus was weaker in hosts also infected by the microsporidia Dictyocoela sp. (roeselum) compared to hosts infected by P. minutus alone. Such conflicts may explain a significant portion of the variation generally observed in behavioural measures, and since VT parasites are ubiquitous in invertebrates, often passing undetected, conflict via transmission may be of great importance in the study of host-parasite relationships.     

Manipulation of host-resource dynamics impacts transmission of trophic parasites

Many complex life cycle parasites rely on predator–prey interactions for transmission, whereby definitive hosts become infected via the consumption of an infected intermediate host. As such, these trophic parasites are embedded in the larger community food web. We postulated that exposure to infection and, hence, parasite transmission are inherently linked to host foraging ecology, and that perturbation of the host-resource dynamic will impact parasite transmission dynamics. We employed a field manipulation experiment in which natural populations of the eastern chipmunk (Tamias striatus) were provisioned with a readily available food resource in clumped or uniform spatial distributions. Using replicated longitudinal capture-mark-recapture techniques, replicated supplemented and unsupplemented control sites were monitored before and after treatment for changes in infection levels with three gastro-intestinal helminth parasites. We predicted that definitive hosts subject to food supplementation would experience lower rates of exposure to infective intermediate hosts, presumably because they shifted their diet away from the intermediate host towards the more readily available resource (sunflower seeds). As predicted, prevalence of infection by the trophically transmitted parasite decreased in response to supplemental food treatment, but no such change in infection prevalence was detected for the two directly transmitted parasites in the system. The fact that food supplementation only had an impact on the transmission of the trophically transmitted parasite, and not the directly transmitted parasites, supports our hypothesis that host foraging ecology directly affects exposure to parasites that rely on the ingestion of intermediate hosts for transmission. We concluded that the relative availability of different food resources has important consequences for the transmission of parasites and, more specifically, parasites that are embedded in the food web. The broader implications of these findings for food web dynamics and disease ecology are discussed.     

Infectivity of two nematode parasites, Camallanus lacustris and Anguillicola crassus, in a paratenic host, the three-spined stickleback Gasterosteus aculeatus

Three-spined sticklebacks Gasterosteus aculeatus are frequent paratenic hosts of the nematode parasites Anguillicola crassus and Camallanus lacustris. As paratenic hosts, sticklebacks could spread infection by carrying high numbers of infective stages. In contrast, low infective ability of either parasite for the paratenic host could hinder the spread of infection. In the present study, G. aculeatus was, for the first time, infected under controlled laboratory conditions with defined doses of the parasites. Sticklebacks were exposed to 6, 12, 18 and 24 parasite larvae to determine the infective ability of the 2 nematode species. There were significantly higher infection rates for C. lacustris (18 to 49%) than for A. crassus (4 to 14%) at each exposure dose. In C. lacustris-infected sticklebacks, infection rates tended to be highest after exposure to 12 C. lacustris larvae and lowest after exposure to 24 parasites. In A. crassus-infected sticklebacks, no effect of parasite exposure dose on infection rates was observed. Immunity parameters such as respiratory burst activity and lymphocyte proliferation of head kidney leukocytes recorded 18 wk post exposure were not significantly affected by either parasite or exposure dose. Granulocyte:lymphocyte ratios were elevated only within the stickleback group showing the highest infection intensity of C. lacustris, i.e. to those exposed 18 parasites.     

Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni

For parasites that require multiple hosts to complete their development, genetic interplay with one host may impact parasite transmission and establishment in subsequent hosts. In this study, we used microsatellite loci to address whether the genetic background of snail intermediate hosts influences life-history traits and transmission patterns of dioecious trematode parasites in their definitive hosts. We performed experimental Schistosoma mansoni infections utilizing two allopatric populations of Biomphalaria glabrata snails and assessed intensities and sex ratios of adult parasites in mouse definitive hosts. Our results suggest that the genetic background of hosts at one point in a parasite’s life cycle can influence the intensities and sex ratios of worms in subsequent hosts.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Interspecific associations among larval helminths in fish

Various processes can generate associations between the larvae of different helminth species in their fish intermediate or paratenic host. We investigated the pairwise associations among larval helminth species in eight different fish populations, using two different coefficients of associations, in order to determine in what situations they are strongest. All helminth species included use the fish studied as either their second intermediate host or their paratenic host, and are acquired by the fish when it ingests an infected first intermediate host. The intensity of infection correlated positively with fish length for most helminth species. Pairs of species which both exhibited positive correlations with fish length tended to be more strongly associated with one another, although this tendency was not pronounced. Similarity in life cycle had a more important influence on pairwise associations. Among the 62 pairwise associations that could be computed, pairs of helminth species that shared both first intermediate hosts and definitive hosts were the most strongly associated, followed by pairs that shared only one other host, and finally by pairs that did not share other hosts. The results suggest that assemblages of larval helminth parasites in fish are not random collections of locally available species, but rather structured packets of larval parasites that travel together along common transmission routes.     

New data in France on the trematode Alaria alata (Goeze, 1792) obtained during Trichinella inspections

The trematode Alaria alata is a cosmopolite parasite found in red foxes (Vulpes vulpes), the main definitive host in Europe. In contrast only few data are reported in wild boars (Sus scrofa), a paratenic host. The aim of this paper is to describe the importance and distribution of Alaria alata mesocercariae in wild boars, information is given by findings of these larvae during Trichinella mandatory meat inspection on wild boars' carcasses aimed for human consumption. More than a hundred cases of mesocercariae positive animals are found every year in the East of France. First investigations on the parasite's resistance to deep-freezing in meat are presented in this work.     

Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites?

Density-dependent effects on parasite fitness have been documented from adult helminths in their definitive hosts. There have, however, been no studies on the cost of sharing an intermediate host with other parasites in terms of reduced adult parasite fecundity. Even if larval parasites suffer a reduction in size, caused by crowding, virtually nothing is known about longer-lasting effects after transmission to the definitive host. This study is the first to use in vitro cultivation with feeding of adult trematodes to investigate how numbers of parasites in the intermediate host affect the size and fecundity of adult parasites. For this purpose, we examined two different infracommunities of parasites in crustacean hosts. Firstly, we used experimental infections of Maritrema novaezealandensis in the amphipod, Paracalliope novizealandiae, to investigate potential density-dependent effects in single-species infections. Secondly, we used the crab, Macrophthalmus hirtipes (Ocypodidae), naturally infected by the trematodes, M. novaezealandensis and Levinseniella sp., the acanthocephalan, Profilicollis spp., and an acuariid nematode. These four helminths all develop and grow in their crustacean host before transmission to their bird definitive host by predation. In experimental infections, we found an intensity-dependent establishment success, with a decrease in the success rate of cercariae developing into infective metacercariae with an increasing dose of cercariae applied to each amphipod. In natural infections, we found that M. novaezealandensis-metacercariae achieved a smaller volume, on average, when infrapopulations of this parasite were large. Small metacercariae produced small in vitro-adult worms, which in turn produced fewer eggs. Crowding effects in the intermediate host thus were expressed at the adult stage in spite of the worms being cultured in a nutrient-rich medium. Furthermore, excystment success and egg-production in M. novaezealandensis in naturally infected crabs were influenced by the number of co-occurring Profilicollis cystacanths, indicating interspecific interactions between the two species. Our results thus indicate that the infracommunity of larval helminths in their intermediate host is interactive and that any density-dependent effect in the intermediate host may have lasting effects on individual parasite fitness.     

Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation

Little is known about actual mating systems in natural populations of parasites or about what constitutes the limits of a parasite deme. These parameters are interesting because they affect levels of genetic diversity, opportunities for local adaptation, and other evolutionary processes. We expect that transmission dynamics and the distribution of parasites among hosts should have a large effect on mating systems and demic structure, but currently we have mostly speculation and very few data. For example, infrapopulations (all the parasites in a single host) should behave as demes if parasite offspring are transmitted as a clump from host to host over several generations. However, if offspring are well mixed, then the parasite component population (all the parasites among a host population) would function as the deme. Similarly, low mean intensities or a high proportion of worms in single infections should increase the selfing rate. For species having an asexual amplification stage, transmission between intermediate and definitive (final) hosts will control the variance in clonal reproductive success, which in turn could have a large influence on effective sizes and rates of inbreeding. We examined demic structure, selfing rates, and the variance in clonal reproductive success in natural populations of Plagioporus shawi, a hermaphroditic trematode that parasitizes salmon. Overall levels of genetic diversity were very high. An a posteriori inference of population structure overwhelmingly supports the component population as the deme, rather than individual infrapopulations. Only a single pair of 597 adult individuals was identified as clones. Thus, the variance in clonal reproductive success was almost zero. Despite being hermaphroditic, P. shawi appears to be almost entirely outcrossing. Genetic estimates of selfing (<5%) were in accordance with the proportion of parasites from single infections. Thus, it appears that individual flukes outcross whenever possible and only resort to selfing when alone. Finally, our data support the hypothesis that aquatic transmission and the use of several intermediate hosts promotes high genetic diversity and well-mixed infrapopulations.     

The role of the European bitterling (<Emphasis Type="Italic">Rhodeus amarus,</Emphasis> Cyprinidae) in parasite accumulation and transmission in riverine ecosystems

In aquatic ecosystems, fish play a key role in parasite accumulation and transmission to predacious animals. In the present study, realized on seven populations of a small cyprinid fish species, the European bitterling Rhodeus amarus, we investigated (1) the role of the European bitterling as a potential intermediate or paratenic host, (2) the ability of the fish to accumulate parasites with similar final host group, and (3) its significance as a potential source of parasite infection in the ecosystem in respect to habitat characteristics. A total of 36 parasite species were recorded; 31 species (90% of all parasite specimens) were classified as endoparasites. Most of the endoparasites were found in the larval life stage, using bitterling as an intermediate or paratenic host. In particular, parasite community structure showed significantly higher proportions of allogenic parasites in comparison with autogenic. The supposed co-occurrence of parasite species with identical final host groups showed only a weak association. The adjacent reservoir areas were a significant determinant of both the total and infracommunity parasite species richness and for the mean parasite abundance. No relationship between the distance of sampling site from the adjacent reservoir and parasite community characteristics was found. As a small-sized fish with a wide distribution range and high local abundances, the European bitterling can represent a natural prey for a wide range of piscivorous predators. Due to its susceptibility to the number of larval endoparasites, this fish species may therefore fulfill the role as important transmitter of parasites to their final hosts.     

Characterization and localization of Paragonimus westermani antigen stimulating antibody formation in both the infected cat and rat

Applicability of the adult Paragonimus westermani antigen for detection of anti-immature P. westermani antibodies in experimentally infected rats, a paratenic host of this lung fluke, was examined. The serum antibodies of the cats and rats infected with P. westermani metacercariae were detected by enzyme-linked immunosorbent assay (ELISA) with the adult-fluke antigen. The ELISA titers of serum samples of the rats infected with only immature flukes were as high as those of the cats infected with adult flukes. Sodium dodecyl sulfate polyacrylamide gel electrophoresis and the immunoblotting technique showed that a major protein band of 27,000 daltons was recognized in the sera of the infected cats and rats. Immunoperoxidase staining applied on the sectioned flukes provided evidence showing that the antigenic substance was located on the surface of the gut epithelium and in the luminal contents in both adult and immature flukes. The adult-fluke antigen containing the 27,000-dalton substance is applicable as a standard antigen for diagnosis of paragonimiasis westermani in not only definitive hosts but also in paratenic hosts.     

Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite

An investigation of a parasite species that is broadly host- and habitat-specific and exhibits alternative transmission strategies was undertaken to examine intraspecific variability and if it can be attributed to cryptic speciation or environmentally induced plasticity. Specimens of an acanthocephalan parasite, Leptorhynchoides thecatus, collected throughout North America were analysed phylogenetically using sequences of the cytochrome oxidase I gene and the internal transcribed spacer region. Variation in host use, habitat use, and transmission were examined in a phylogenetic context to determine if they were more likely phylogenetically based or due to environmental influences. Results indicated that most of the variation detected can be explained by the presence of cryptic species. The majority of these species have narrow host and microhabitat specificities although one species, which also may comprise a complex of species, exhibits broad host and habitat specificity. Alternate transmission pathways only occurred in two of the cryptic species and correlate with host use patterns. Taxa that mature in piscivorous piscine hosts use a paratenic fish host to bridge the trophic gap between their amphipod intermediate host and piscivorous definitive host. One potential example of environmentally induced variation was identified in three populations of these parasites, which differ on their abilities to infect different host species.