Development of Fasciola hepatica in Lymnaea columella infected with miracidia derived from cattle and marmoset infections

The development of Fasciola hepatica from two species of definitive hosts, i.e. cattle (Bos taurus) and a marmoset (Callithrix penicillata) in the snail Lymnaea columella was determined based on the production of rediae and cercariae and snail survival rate. More rediae and cercariae at 60-74 days post-infection were produced by snails infected by cattle-derived miracidia (cattle group) than by those infected by marmoset-derived miracidia (marmoset group). Among the L. columella parasitized by the marmoset group, the survival rate and the percentage of positive snails were higher than among those parasitized by the cattle group. Eggs of F. hepatica released in cattle faeces were significantly bigger than those released in marmoset faeces. Miracidia originating from parasites that completed their development in cattle were more efficient in infecting the intermediate host. These results suggest that vertebrate-host origin influences the eggs produced by the parasite and the infection rates in the snail host L. columella.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

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.     

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.     

Life cycle and identification of an eyefluke from Israel transmitted by Melanoides tuberculata (Müller, 1774)

A philophthalmid species from Israel using the freshwater snail Melanoides tuberculata as intermediate host was studied. The biological and morphological characteristics of all developmental stages of the life cycle of this philophthalmid were described, and compared to those of Philophthalmus lucipetus Rudolphi, 1819 from Israel, Philophthalmus gralli Mathis and Leger, 1910 from Jordan, Philophthalmus palpebrarum Looss, 1899, Philophthalmus nocturnus Looss, 1907, Cercaria distomatosa Looss 1896 from Egypt, and Philophthalmus lucknowensis Baugh, 1962 from India. The possible identity with 1 of these species is discussed. On the basis of comparative analysis of the data for all parasite stages in the life cycle, geographical distribution, snail hosts, and snail host specificity, we propose to designate the Israeli Melanoides tuberculata-transmitted eye fluke to Philophthalmus distomatosa n. comb. (Looss, 1896), (Digenea: Philophthalmidae).     

Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario

Agricultural activity and landscape features have previously been associated with diversity and prevalence of trematode species in amphibian second intermediate hosts. In this study, the density, diversity, and size of snail first intermediate hosts, and the diversity and prevalence of their trematode species, were assessed in 2 types of ponds, i.e., those adjacent to cornfields and those from the same region in southwestern Ontario that were adjacent to nonagricultural settings. Species of trematodes included, but were not restricted to, those that are known parasites of larval and adult frogs. We also assessed landscape factors likely to influence use by definitive hosts. Presence of the herbicide atrazine in ponds was measured to check that ponds adjacent to agriculture had potential to be affected by agricultural runoff. Both snail size and the proportion of snails releasing cercariae were greater in nonagricultural ponds, contrasting with a previous finding of lower trematode infection in tadpoles from nonagricultural ponds. Percentage of forest cover was associated with prevalence of certain trematode species, but not with estimates of combined prevalence. Absence of relations of trematode prevalence to measures of road density also contrasted with previous studies. We interpret our results in light of how agricultural activity might influence trematode viability, snail growth, and use by wildlife definitive hosts, independently of landscape factors.     

The life cycle of Brachylaima ruminae n. sp. (Trematoda: Brachylaimidae), a parasite of rodents

The life cycle of Brachylaima ruminae n.sp. (Trematoda: Brachylaimidae), a duodenal parasite of rodents on the Mediterranean island of Formentera (Spain) is elucidated. The new species follows a terrestrial triheteroxenous life cycle. Eggs passed in the faeces of the definitive host must be ingested by a specific first intermediate host, the land snail Rumina decollata. Branched cercariogenous sporocysts develop in the digestive gland. Microcercous cercariae come out through the terminal birth pores of the branches. Cercariae shed by the snail are terrestrial, crawling on humid substratum. They contact the second intermediate host, another land snail, principally the species R. decollata and less frequently slugs and Helicids. Cercariae enter via the excretory pore and kidney duct to their specific final location, the kidney. Unencysted metacercariae develop in the kidney (also, less frequently, in the pedal glands) to the mature, infective stage. Infective metacercariae infest the definitive host when ingested together with the snail.     

Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites

The comparative genetic structure of hosts and their parasites has important implications for their coevolution, but has been investigated in relatively few systems. In this study, we analysed the genetic structure and diversity of the New Zealand intertidal snail Zeacumantus subcarinatus ( n  =   330) and two of its trematode parasites, Maritrema novaezealandensis ( n  =   269) and Philophthalmus sp. ( n  =   246), using cytochrome c oxidase subunit I gene ( COI ) sequences. Snails and trematodes were examined from 11 collection sites representing three regions on the South Island of New Zealand. Zeacumantus subcarinatus displayed low genetic diversity per geographic locality, strong genetic structure following an isolation by distance pattern, and low migration rates at the scale of the study. In contrast, M. novaezealandensis possessed high genetic diversity, genetic homogeneity among collection sites and high migration rates. Genetic diversity and migration rates were typically lower for Philophthalmus sp. compared to M. novaezealandensis and it displayed weak to moderate genetic structure. The observed patterns likely result from the limited dispersal ability of the direct developing snail and the utilization of bird definitive hosts by the trematodes. In addition, snails may occasionally experience long-distance dispersal. Discrepancies between trematode species may result from differences in their effective population sizes and/or life history traits.     

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.     

Do Parasitic Trematode Cercariae Demonstrate a Preference for Susceptible Host Species?

Many parasites are motile and exhibit behavioural preferences for certain host species. Because hosts can vary in their susceptibility to infections, parasites might benefit from preferentially detecting and infecting the most susceptible host, but this mechanistic hypothesis for host-choice has rarely been tested. We evaluated whether cercariae (larval trematode parasites) prefer the most susceptible host species by simultaneously presenting cercariae with four species of tadpole hosts. Cercariae consistently preferred hosts in the following order: Anaxyrus ( = Bufo) terrestris (southern toad), Hyla squirella (squirrel tree frog), Lithobates ( = Rana) sphenocephala (southern leopard frog), and Osteopilus septentrionalis (Cuban tree frog). These host species varied in susceptibility to cercariae in an order similar to their attractiveness with a correlation that approached significance. Host attractiveness to parasites also varied consistently and significantly among individuals within a host species. If heritable, this individual-level host variation would represent the raw material upon which selection could act, which could promote a Red Queen “arms race” between host cues and parasite detection of those cues. If, in general, motile parasites prefer to infect the most susceptible host species, this phenomenon could explain aggregated distributions of parasites among hosts and contribute to parasite transmission rates and the evolution of virulence. Parasite preferences for hosts belie the common assumption of disease models that parasites seek and infect hosts at random.     

Effects of ultraviolet radiation on the transmission process of an intertidal trematode parasite

The transmission of parasites takes place under exposure to a range of fluctuating environmental factors, one being the changing levels of solar ultraviolet radiation (UVR). Here, we investigated the effects of ecologically relevant levels of UVR on the transmission of the intertidal trematode Maritrema novaezealandensis from its first intermediate snail host (Zeacumantus subcarinatus) to its second intermediate amphipod host (Paracalliope novizealandiae). We assessed the output of parasite transmission stages (cercariae) from infected snail hosts, the survival and infectivity of cercariae, the susceptibility of amphipod hosts to infection (laboratory experiments) and the survival of infected and uninfected amphipod hosts (outdoor experiment) when exposed to photo-synthetically active radiation only (PAR, 400-700 nm; no UV), PAR+UVA (320-700 nm) or PAR+UVA+UVB (280-700 nm). Survival of cercariae and susceptibility of amphipods to infection were the only two steps significantly affected by UVR. Survival of cercariae decreased strongly in a dose-dependent manner, while susceptibility of amphipods increased after exposure to UVR for a prolonged period. Exposure to UVR thus negatively affects both the parasite and its amphipod host, and should therefore be considered an influential component in parasite transmission and host-parasite interactions in intertidal ecosystems.     

Effects of trematode double infection on the shell size and distribution of snail hosts

Infection with larval trematodes sometimes alters the phenotypes of their snail hosts. While some trematode species have distinct effects on host phenotypes, it is still unclear how snail phenotypes are altered when they are parasitized with multiple trematode species. Here, we report that double infection with trematode species averages the effects of parasitic alteration on host phenotype. We found that snail hosts Batillaria attramentaria (Batillariidae) infected with Cercaria batillariae (Heterophyidae) have abnormally large shells and distribute in lower areas of the intertidal zone. Snails with another dominant trematode species, the renicolid cercaria I (Renicolidae), have slightly larger shells and distribute in upper areas of the intertidal zone. A number of double infections with both trematodes was observed in this study. Snails infected with both trematode species exhibited an intermediate size and inhabited a depth between those of snails solely infected with either trematode species, suggesting that the two trematodes simultaneously affected the snail phenotypes. Because altered host phenotypes are frequently beneficial to parasites, two trematode species may compete for successful transmission through alteration of host phenotypes.     

Bird schistosomes: do they die in mammalian skin?

The cercariae of bird schistosomes, released from the intermediate water snail host, actively penetrate the skin of both birds and mammals. Whereas in birds the infection leads to worm maturation and egg production, in the mammalian hosts skin invasion is accompanied by cercarial dermatitis (swimmer's itch, clam-digger's disease) and the fate of the parasites is not clear. Here, we review bird schistosomes as causative agents of cercarial dermatitis, underline adaptations of bird schistosomes to their life in vertebrate hosts, and discuss potential risks caused by the parasites migrating in humans.     

Toxic effects of cadmium and zinc on the transmission of Echinoparyphium recurvatum cercariae

The toxicity of cadmium, zinc and Cd/Zn mixtures to the transmission of Echinoparyphium recurvatum (Digenea: Echinostomatidae) cercariae into the snail second intermediate hosts was investigated at concentrations ranging from 100 microg l-1 to 10 000 microg l-1 in both soft and hard water. A differential response in the infectivity of metal-exposed cercariae into Lymnaea peregra and Physa fontinalis was demonstrated which was dependent on the snail species being infected. Exposure of L. peregra, P. fontinalis, and L. stagnalis to heavy metals caused a differing susceptibility to E. recurvatum cercariae depending on the snail species being exposed. The mechanism and effects of metal toxicity, together with the importance of the parasite/host strain on cercarial transmission are discussed.     

Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae)

Marine bivalves harbour a diversity of trematode parasites affecting population and community dynamics of their hosts. Although ecologically and economically important, factors influencing transmission between first (snail) and second (bivalve) intermediate hosts have rarely been studied in marine systems. In laboratory experiments, the effect of temperature (10, 15, 20, 25 degrees C) was investigated on (1) emergence from snails, (2) survival outside hosts and (3) infectivity in second intermediate hosts of cercariae of the trematode Renicola roscovita (Digenea: Renicolidae), a major parasite in North Sea bivalves. Emergence of cercariae peaked at 20 degrees C (2609 +/- 478 cercariae snail(-1) 120 h(-1)) and was considerably lower at 10 degrees C (80 +/- 79), 15 degrees C (747 +/- 384) and 25 degrees C (1141 +/- 334). Survival time decreased with increasing temperature, resulting in 50% mortality of the cercariae after 32.8 +/- 0.6 h (10 degrees C), 26.8 +/- 0.8 h (15 degrees C), 20.2 +/- 0.5 h (20 degrees C) and 16.6 +/- 0.3 h (25 degrees C ). Infectivity of R. roscovita cercariae in cockles Cerastoderma edule increased with increasing temperature and was highest at 25 degrees C (42.6 +/- 3.9%). However, mesocosm experiments with infected snails and cockle hosts in small aquaria, integrating cercarial emergence, survival and infectivity, showed highest infection of cockles at 20 degrees C (415 +/- 115 metacercariae host(-1)), indicating 20 degrees C to be the optimum temperature for transmission of this species. A field experiment showed metacercariae of R. roscovita to appear in C. edule with rising water temperature in April; highest infection rates were in August, when the water temperature reached 20 degrees C. Since another trematode species (Himasthla elongata; Digenea: Echinostomatidae) occurring at the experimental site showed a similar temporal pattern, trematode transmission to second intermediate bivalve hosts may peak during especially warm (> or = 20 degrees C) summers in the variable climate regime of the North Sea.     

Internal movement of estuarine digenetic trematodes through their intermediate snail host Cerithidea californica

The ability of free-swimming larval parasites to control emergence from their hosts can be critical in increasing the chances of successful infection transmission. For a group of estuarine trematodes, emergence of cercariae from their snail hosts is known to match favorable temperature, tidal activity, and light intensity. How the larvae time this behavior is not well understood, but the pathway that the larvae take through their host may play a role. Through video and histological analysis, we were able to identify the snail's anus as the emergence point and the peri-intestinal sinus dorsal to the intestines as the route by which they reach that point. By moving through this open sinus, the larvae have an energetically efficient pathway to reach their emergence point while minimizing damage to the host. Most importantly, it allows control over emergence to be maintained by the parasite, not the host, thus increasing the chances of the larva successfully reaching its intended destination.     

Clone-specific immune reactions in a trematode-crustacean system

Variability of immune responses is an essential aspect of ecological immunology, yet how much of this variability is due to differences among parasite genotypes remains unknown. Here, variation in immune response of the crab, Macrophthalmus hirtipes, is examined as a function of experimental exposure to 10 clonal cercarial lineages of the trematode Maritrema novaezealandensis. Our goals were (1) to assess the variability of the host immune reaction elicited by 10 parasite clones, (2) to test if the heterozygosity-fitness correlation, whereby organisms with higher heterozygosities achieve a higher fitness than those with lower heterozygosities, applies to heterozygous parasites eliciting weak immune responses, and (3) to see how concomitant infections by other macroparasites influence the crab's immune response to cercariae. Parasite clones were distinguished and heterozygosities calculated using 20 microsatellite markers. We found that exposure to cercariae resulted in increased haemocyte counts, and that although interclonal differences in immune response elicited were detected, parasite heterozygosity did not correlate with host immune response. Additionally, the presence of other pre-existing parasites in hosts did not influence their immune response following experimental exposure to cercariae. Overall, the existence of variability in immune response elicited by different parasite clones is promising for future ecological immunology studies using this system.     

Bioenergetic theory predicts infection dynamics of human schistosomes in intermediate host snails across ecological gradients

Epidemiological dynamics depend on the traits of hosts and parasites, but hosts and parasites are heterogeneous entities that exist in dynamic environments. Resource availability is a particularly dynamic and potent environmental driver of within‐host infection dynamics (temporal patterns of growth, reproduction, parasite production and survival). We developed, parameterised and validated a model for resource‐explicit infection dynamics by incorporating a parasitism module into dynamic energy budget theory. The model mechanistically explained the dynamic multivariate responses of the human parasite Schistosoma mansoni and its intermediate host snail to variation in resources and host density. At the population level, feedbacks mediated by resource competition could create a unimodal relationship between snail density and human risk of exposure to schistosomes. Consequently, weak snail control could backfire if reductions in snail density release remaining hosts from resource competition. If resource competition is strong and relevant to schistosome production in nature, it could inform control strategies.     

Effects of ultraviolet radiation on an intertidal trematode parasite: an assessment of damage and protection

Trematode parasites are integral components of intertidal ecosystems which experience high levels of ultraviolet radiation. Although these parasites mostly live within hosts, their life cycle involves free-living larval transmission stages such as cercariae which are directly exposed to ambient conditions. UV has previously been shown to considerably reduce the survival of cercariae. Here, we investigated potential mechanisms of protection and damage related to UV in the intertidal trematode Maritrema novaezealandensis. Firstly, the presence of sunscreen compounds (i.e. mycosporine-like amino acids) was quantified in the parasite tissue producing cercariae within a snail host, as well as in the free-swimming cercariae themselves. Secondly, levels of oxidative stress in cercariae after exposure to UV were investigated (i.e.protein carbonyls, catalase and superoxide dismutase). Thirdly, the DNA damage (i.e. cyclobutane–pyrimidine dimers) was compared between cercariae exposed and not exposed to UV. Lastly, functional aspects(survival and infectivity) of cercariae were assessed, comparing cercariae under light conditions versus dark after exposure to UV. We confirmed the presence of my cosporine-like amino acids in cercariae-producing tissue from within snail hosts, but were unable to do so in cercariae directly. Results further suggested that exposure to UV induced high levels of oxidative stress in cercariae which was accompanied by a reduction in the levels of protective antioxidant enzymes present. We also identified higher levels of DNA damage in cercariae exposed to UV, compared with those not exposed. Moreover, no clear effect of light condition was found on survival and infectivity of cercariae after exposure to UV. We concluded that cercariae are highly susceptible to UV damage and that they have very little scope for protection against or repair of UV-induced damage.     

Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages

The transmission stages of parasites are key determinants of parasite fitness, but they also incur huge mortality. Yet the selective forces shaping the sizes of transmission stages remain poorly understood. We ran a comparative analysis of interspecific variation in the size of transmission stages among 404 species of parasitic trematodes. There are two transmission steps requiring infective stages in the life cycle of trematodes: transmission from the definitive to the first intermediate (snail) host is achieved by eggs and/or the miracidia hatched from those eggs, and transmission from the first to the second intermediate host is achieved by free-swimming cercariae. The sizes of these stages are under strong phylogenetic constraints. Our results show that taxonomy explains >50% of the unaccounted variance in linear mixed models, with most of the variance occurring at the superfamily level. The models also demonstrated that mollusc size is positively associated with egg volume, miracidial volume and cercarial body volume, but not with the relative size of the cercarial tail. In species where they encyst on substrates, cercariae have significantly larger bodies than in species penetrating chordates, although the relative size of the cercarial tail of species using chordates as second intermediate hosts was larger than in other trematode species. Habitat also matters, with larger cercarial tails seen in freshwater trematodes than in marine ones, and larger miracidial volumes in freshwater species than in marine ones. Finally, the latitude (proxy for local temperature) at which the trematode species were collected had no effect on the sizes of transmission stages. We propose that resource availability within the snail host, the probability of contacting a host, and the density and viscosity of the water medium combine to select for different transmission stage sizes.