Spanning the gap: experimental determination of paratenic host specificity of horsehair worms (Nematomorpha: Gordiida)

Abstract. Details of the life cycle of freshwater nematomorphs (gordiids) remain unclear. Free-living aquatic larval gordiids must make a critical transition from an epibenthic aquatic environment to terrestrial hosts. In order to identify potential hosts capable of bridging this ecological gap, the specificity of paratenic hosts of three common species of North American gordiids was investigated. All three species were characterized by an identical infection pattern: low host specificity. Gordiids were able to encyst within annelids, mollusks, crustaceans, insects and a vertebrate. Three species of putative host (a turbellarian, a water mite, and a mosquito larva) were not infected with any of the gordiid species. Internal defense reactions (IDR) and feeding behaviors are implicated as preventing infection in these species. Several of the other host species produced either an IDR or an immune reaction to the cysts, although reactions to the cysts were highly variable between species. In most species, IDR did not cause noticeable harm to the encysted larvae. It is proposed that although many species are easily infected with gordiid cysts, most do not act as natural paratenic hosts. For some of these host groups, especially snails, a role as reservoir host is suggested. Of all hosts included in this study, aquatic insects were identified as the hosts likely responsible for spanning the ecological gap and acting as true hosts for gordiids.     

Life cycle and paratenesis of American gordiids (Nematomorpha: Gordiida)

To complete their life cycle, gordiids must make a transition from aquatic to terrestrial environments. However, epibenthic aquatic larvae and their terrestrial definitive hosts do not overlap in habitat. This has led many investigators to suggest that infections are acquired through the ingestion of insects, which become infected as aquatic larvae with gordiid cysts and subsequently carry gordiids to land. This proposed life cycle was experimentally tested using 3 common American species of gordiids: Gordius robustus, Paragordius varius, and Chordodes morgani. Cysts of all 3 species survived the metamorphosis of Tanytarsus sp., a midge. Subsequent infection trials of definitive hosts with cysts from imagos show that cysts surviving the metamorphosis of insects remained viable and free of host internal defense reaction. Data from naturally infected mayflies, Callibaetus sp., show that encystment and survival of gordiids within aquatic insects occur in nature. Paratenesis between paratenic hosts was also shown to be possible in these 3 species. This latter finding appears to indicate that cysts formed in spurious paratenic hosts may not be lost but may eventually transfer to normal paratenic hosts.     

Hyperparasitism by Paragordius varius (Nematomorpha: Gordiida) larva of Monostome redia (Trematoda: Digenea)

Gordiid larvae enter and encyst within a large variety of aquatic vertebrates and invertebrates. Cysts of a single species of gordiid have been found in such diverse hosts as insect larvae, snails, crustaceans, fish, and many others. One particularly surprising host report was made nearly 100 yr ago, i.e., cysts within adult trematodes. The origin of these cysts remained unclear, but it was suggested that the gordiid larvae gained entry into the adult flukes via their definitive, vertebrate host. In the present study, the finding is reported of gordiid cysts within monostome redia within a Physa gyrina snail. This is the first time gordiid cysts have been reported within redia, and this provides an alternative explanation for the presence of cysts within adult trematodes.     

Parasitic mites influence fitness components of their host, the land snail Arianta arbustorum

Abstract. Parasites can influence the population dynamics of their hosts by affecting life-history strategies and behavior. The hematophageous mite Riccardoella limacum lives in the lung cavity of terrestrial gastropods. We used correlational and experimental approaches to investigate the influence of parasite infection on the behavior and life-history traits of the simultaneously hermaphroditic land snail Arianta arbustorum , a common host of R. limacum. Naturally infected individuals of A. arbustorum , collected in the wild, showed a decreased activity compared with uninfected snails. The reproductive output, expressed as the number of eggs deposited in a reproductive season, was reduced in mite-infected hosts. However, the hatching success of the eggs laid by parasitized snails was slightly higher than that of uninfected individuals. We also examined winter survival in 361 adults of A. arbustorum collected from four natural populations. The prevalence of mite infection ranged from 44.8% to 70.1% in three populations (snails in the fourth population were not infected). Winter survival was reduced in infected snails in two out of three populations. Furthermore, experimentally infected snails from an uninfected population showed a reduced winter survival compared with control snails. Our results indicate that parasite pressure imposed by members of R. limacum may influence life history in A. arbustorum.     

Field prevalence and laboratory susceptibility of southern Australian land snails to Brachylaima cribbi sporocyst infection

Brachylaima cribbi is a terrestrial trematode of birds and mammals with helicid and hygromiid land snails reported as first and second intermediate hosts. However, reports describing the first intermediate host range of B. cribbi have been limited to those snail species present in a small number of geographical locations in South Australia. The natural first intermediate host range, distribution and prevalence of B. cribbi in land snails in southern Australia were determined. A total of 6,432 introduced and native land snails were collected from eight geographical districts across 3,000 km of southern Australia and examined microscopically for B. cribbi sporocysts. Four introduced European snails, Theba pisana, Cernuella virgata, Cochlicella acuta and Cochlicella barbara were natural first intermediate hosts. Sporocyst-infected snails were detected in all districts from Victoria to the west coast of South Australia, a distance of over 1,300 km. Natural sporocyst infection was not observed in introduced European snails Microxeromagna armillata and Helix aspersa or in native Australian land snails Succinea australis and Strangesta gawleri. Egg feeding experiments in the laboratory with B. cribbi confirmed the susceptibility of those species of snails found to be natural first intermediate hosts. Of those species not found to be infected in nature, only M. armillata could be infected in the laboratory. Although this study has shown that five different species of European land snails are suitable first intermediate hosts for B. cribbi there are as yet no reports of B. cribbi from these snails in Europe or from other countries where they have been introduced. Further investigations are needed in Europe to clarify the origins of this parasite.     

Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea.

An important component of the parasite fauna of seabirds in arctic regions are the flukes (Digena). Different species of digeneans have life cycles which may consist of 1 intermediate host and no free-living larval stages, 2 intermediate hosts and 1 free-living stage, or 2 intermediate hosts and 2 free-living larval stages. This study examined the distribution of such parasites in the intertidal zones of the southern coast of the Barents Sea (northwestern Russia and northern Norway) by investigating 2 species of periwinkles (Littorina saxatilis and L. obtusata) which are intermediate hosts of many species of digeneans. A total of 26,020 snails from 134 sampling stations were collected. The study area was divided into 5 regions, and the number of species, frequency of occurrence and prevalence of different digenean species and groups of species (depending on life cycle complexity) were compared among these regions, statistically controlling for environmental exposure. We found 14 species of digeneans, of which 13 have marine birds as final hosts. The number of species per sampling station increased westwards, and was higher on the Norwegian coast than on the Russian coast. The frequency of occurrence of digeneans with more than 1 intermediate host increased westwards, making up a larger proportion of the digeneans among infected snails. This was significant in L. saxatilis. The prevalence of different species showed the same pattern, and significantly more snails of both species were infected with digeneans with complicated life cycles in the western regions. In L. saxatilis, environmental exposure had a statistically significant effect on the distribution of the most common digenean species. This was less obvious in L. obtusata. The causes of changing species composition between regions are probably (1) the harsh climate in the eastern part of the study area reducing the probability of successful transmission of digeneans with complicated life cycles, and (2) the distribution of different final hosts.     

Larval trematode infections and spatial distributions of snails

Abstract. The hypothesis that infecting trematodes influence the spatial distribution of the estuarine snail Ilyanassa obsoleta was tested. This work was conducted in the Savages Ditch habitat, Rehoboth Bay, DE, USA, which has an essentially flat, sandy-mud bottom bordered by saltmarsh shorelines and many infected snails. In 1996, two groups of snails were individually marked and released from one location after being screened for trematode infections. One group, transplanted from sites where snails tended not to be infected, consisted of snails that tested as uninfected. The other group consisted of snails native to Savages Ditch. Species of trematode carried by each snail was recorded. Marked snails were found and their positions were recorded until 2001. Snails were in five infection categories: (1) not infected, and infected with (2) Himasthla quissetensis , or (3) Lepocreadium setiferoides or (4) Zoogonus rubellus , or (5) with both H. quissetensis and Z. rubellus . The results show that the spatial distributions of snails depended on whether or not they were infected and, if infected, on which trematode species they carried. To complete life cycles, these parasites must accomplish transmission from the first (the snail) to the second intermediate hosts by short-lived, swimming cercariae. These data do not allow resolution of why snails distributed as they did, but sighting distributions of infected snails can be related to distributions of second hosts and it is proposed that parasites engender host snail distributions that improve chances of transmission.     

Host life history and the effect of parasitic castration on growth: A field study of Cerithidea californica Haldeman (Gastropoda : Prosobranchia) and its trematode parasites

The prevalence of parasitic infection by larval digenetic trematodes in natural populations of the mud snail, Cerithidea californica Haldeman, was found to increase with snail length; all snails ≥ 33 mm were infected. Distributions of infections by the seven most common larval trematodes were heterogeneous due to two species being more common than expected in the smaller size classes of snails, two being more common than expected in the larger size-classes of snails and three species being most prevalent in snails of intermediate length. The relative abundances of trematodes in different size-classes reflected these distributional patterns.A mark-recapture field study of snail growth rates failed to demonstrate that parasitic infection causes gigantism in Cerithidea. Parasitism tended to stunt the growth of juvenile snails and to a lesser degree, that of adult snails. The effects of trematodes on snail growth was shown to be species specific. This finding contrasts with those of earlier studies in which gigantic growth was observed in infected snails. This discrepancy is attributed to differences in the life histories of the host snails. It is predicted that gigantism will occur commonly in short-lived or semelparous species of snails but rarely, if ever, in long-lived iteroparous species which are predominately marine.     

Endemic echinostome infections of candidate hosts

Wild Lymnaea tomentosa snails, recovered from Lake Wanaka, New Zealand, were established in the laboratory. Wild snails, naturally infected with echinostomes, provided metacercariae for infection of laboratory maintained snails. Metacercarial cysts from wild and laboratory snails were then used to attempt infection of definitive host candidates. Laboratory snails provided convenient packaging of known numbers of cysts. Metacercariae excysted in the small intestines of ducklings to mature in 6 days. Worms were expelled as they became gravid. Attempts to establish infections in experimental hosts other than ducklings were not successful. No worms were recovered from mice, white rats, guinea pigs, hamsters or immunosuppressed white rats.     

In vitro and in vivo encystment of the cercariae of Echinostoma caproni

In vitro and in vivo studies were conducted on the cercariae of Echinostoma caproni. Of the 15 media tried, 2 resulted in effective in vitro encystment in petri dish cultures maintained at 23 +/- 1 C. They were a Locke's--artificial springwater (ASW) (1:1) medium (67% encystment) and a Biomphalaria glabrata embryonic cell line medium (23% encystment). To obtain large numbers of in vitro--formed cysts, finger bowl cultures containing 40 ml of the Locke's-ASW (1:1) medium were used at 23 +/- 1 C. Of 3,000 cercariae tested, 1,890 (63%) were encysted in this medium by 48 hr. Most of these cysts looked similar to those formed in vivo, although some showed abnormalities in the outer cyst wall and other malformations. A total of 200 in vitro-formed cysts treated in an alkaline trypsin-bile salts (TB) medium for 2 hr at 41 C showed 94% excystation. In vitro-formed cysts fed to mice produced ovigerous adults within 2 wk postinfection (PI). Eggs from these worms gave rise to miracidia that produced patent intramolluscan infections in B. glabrata snails. In vivo encystment was studied in lab-raised juvenile Helisoma trivolvis (Colorado strain) snails, 1-3 mm in shell diameter. From 6 to 24 hr PI, 93-100% of the cercariae were recovered as metacercarial cysts in the snail tissue. Treatment of these cysts in the TB medium resulted in 96% excystation within 2 hr at 41 C.     

Life history and identification of Philophthalmus lucipetus from Israel

A Philophthalmus species whose larval stages have been isolated from Melanopsis praemorsa snails collected in Israel and formerly identified as probably belonging to Philophthalmus palpebrarum has now been reevaluated as belonging to Philophthalmus lucipetus. The present determination is based on a detailed study of all the stages of the parasite's life cycle--eggs, intramolluscan stages, cercariae, and adults. They were compared to the original species P. lucipetus, recently reexamined and redescribed from source material in Vienna, Austria. The identity of the eyefluke from Israel and P. lucipetus was further confirmed by successful cross-infections employing miracidia of the Israeli isolate in European (Bulgarian) Fagotia acicularis acicularis snails on the one hand and miracidia of P. lucipetus from Bulgaria in Israeli Melanopsis praemorsa on the other hand, but none infected Melano?des tuberculata snails from Israel.     

The influence of habitat on the distribution and abundance of metacercariae of Macravestibulum obtusicaudum (Pronocephalidae) in a small Indiana stream

Snails (Elimia livescens) from a central Indiana stream were examined for encysted metacercariae of Macravestibulum obtusicaudum (Pronocephalide) to determine the distribution and abundance of this parasite on its second intermediate host. Five samples of snails were collected, with 2 samples being restricted to high-flow (riffle) or low-flow (pool) areas of the stream. Snails (n = 386) were measured for shell length; the shell and the inner and outer surfaces of the operculum (in most samples) were examined for metacercariae. Seventy-five percent of snails (overall) had encysted metacercariae (range, 52-97%), primarily on the opercula. A significantly lower proportion of snails from riffles were infected, and these snails had significantly fewer cysts as well. Snails collected from pools showed up to 10 times as many metacercariae than those from riffles, although there was no significant difference in the proportion of snails with intramolluscan infections of M. obtusicaudum. The inner opercular surface appeared to be the preferred site of encystment in both flow regimes. Differences in microhabitats, in terms of both snails in the stream and metacercariae on the snails, clearly must be considered when evaluating the infection patterns of this trematode.     

Age/size- and time-specific effects of Schistosoma mansoni on energy allocation patterns of its snail host Biomphalaria glabrata

Snail hosts of different ages constitute different resource environments for larval trematodes because each individual has a particular energy budget and energy allocation pattern at the time of infection. Effects of monomiracidial trematode infections on shell growth, body dry weight and reproductive effort of the snail host were compared between controls and infected juvenile and adult snails during the prepatent and patent periods. The results demonstrate phenotypic plasticity in the host response. There is an age/size-specific effect characterized by limitation of growth rate when snails are infected as juveniles and reduction of reproductive effort when snails are infected as adults, and a time-specific effect with early enhancement of growth rate and reproductive effort for infected juvenile and adult snails respectively during prepatency, before reduction and cessation during patency. The parasite is considered as a generalist in its energy exploitation strategy of the snail host, but taking into account the differential host responses observed relative to the host age, the possibility of a host preference for juvenile or adult snails is discussed. Received: 4 February 1997 / Accepted: 14 July 1997     

Host quality and spatial patterning in infections of the Eastern mudsnail (Ilyanassa obsoleta) by two trematodes (Himasthla quissetensis and Zoogonus rubellus)

Several studies have suggested that the fitness of a parasite can be directly impacted by the quality of its host. In such cases, selective pressures could act to funnel parasites towards the highest-quality hosts in a population. The results of this study demonstrate that snail host quality is strongly correlated with spatial patterning in trematode infections and that habitat type is the underlying driver for both of these variables. Two trematodes (Himasthla quissetensis and Zoogonus rubellus) with very different life cycles assume the same spatial infection pattern in populations of the first intermediate host (Ilyanassa obsoleta) in coastal marsh habitats. Infected snails are disproportionately recovered from intertidal panne habitats, which offer more hospitable environs for snails than do adjacent habitats (intertidal creeks, coastal flats, and subtidal creeks), in terms of protection from turbulence and wave action, as well as the availability of food stuffs. Snails in intertidal panne habitats are of higher quality when assessed in terms of average size-specific mass, growth rate, and fecundity. In mark-recapture experiments, snails frequently dispersed into intertidal pannes but were never observed leaving them. In addition, field experiments demonstrate that snails confined to intertidal panne habitats are disproportionately infected by both trematode species, relative to conspecifics confined to adjacent habitats. Laboratory experiments show that infected snails suffer significant energetic losses and consume more than uninfected conspecifics, suggesting that infected snails in intertidal pannes may survive better than in adjacent habitats. We speculate that 1 possible mechanism for the observed patterns is that the life cycles of both trematode species allows them to contact the highest-quality snails in this marsh ecosystem.     

Segmentina hemisphaerula: a new molluscan intermediate host for Echinostoma cinetorchis in Korea.

Three species of Planorbidae have been reported from Korea, e.g., Gyraulus convexiusculus, Hippeutis (Helicorbis) cantori, and Segmentina (Polypylis) hemisphaerula. Of these, only H. cantori was reported as the first and second intermediate host for Echinostoma cinetorchis, an important human intestinal parasite in Korea. Segmentina hemisphaerula has also been found to be an intermediate host. In field-collected planorbids, only S. hemisphaerula was found shedding echinostome cercariae and infected with metacercariae of E. cinetorchis, whereas no G. convexiusculus and H. cantori were found to be infected. In experiments with laboratory-bred snails, G. convexiusculus and S. hemisphaerula were susceptible to infection by miracidia of E. cinetorchis, but H. cantori could not be infected. Tadpoles of Rana nigromaculata and laboratory-bred snails of the 3 planorbid species were exposed to E. cinetorchis cercariae shed from field-collected S. hemisphaerula. All tadpoles, S. hemisphaerula, and G. convexiusculus became infected, but no H. cantori were infected. Metacercariae from tadpoles, S. hemisphaerula, and G. convexiusculus were fed to rats per os, and eggs of E. cinetorchis were detected in the rat feces 1 wk later. The rats were killed, and adult E. cinetorchis were recovered from the small intestines. This is the first report of G. convexiusculus as a potential first and second intermediate host and of S. hemisphaerula as a new first and second intermediate host for E. cinetorchis in Korea.     

Effects of Schistosoma mansoni infection on inorganic elements in the snail Biomphalaria glabrata

Inductively coupled plasma atomic emission spectrometry (ICP-AES) was used to study element ions in whole bodies of uninfected Biomphalaria glabrata snails and those experimentally infected with larval Schistosoma mansoni trematodes. Infected snails were analysed 8 weeks post-infection. Cohort snails that were left uninfected were analysed at the same time as the infected snails. Sixteen elements (aluminum, boron, barium, calcium, cadmium, copper, iron, potassium, magnesium, manganese, sodium, nickel, lead, selenium, tin and zinc) were found to be present in infected and uninfected whole bodies at concentrations above the detection limit of the ICP-AES analysis. Of these, calcium, cadmium, manganese and sodium were present in significantly higher amounts (Student's t-test, P<0.05) in whole infected versus whole uninfected snails. Variations in the present results compared with other studies reflect intrinsic differences in the larval trematode-snail systems used.     

Distributional ecology of snails (Gastropoda: Mollusca) in seasonal ponds of Tamil Nadu,South India

The present study was focused to examine diversity and distributional pattern of freshwater snails and to identify the schistosome infected snails in ten different ponds of Madurai district, Tamil Nadu, South India. Snails were collected from native substrates in ponds using dip net from Madurai North, Tamil Nadu province of south India and microscopic examination for detecting cercariae larvae in snails were assessed. In total, 1250 individuals belonging to six species under five families of freshwater snails were collected. The alpha and beta diversity analyses were calculated for estimating the diversity of snails. The cercariae infection was observed in four collected freshwater snail species. Of four infected snails, Lymnaea luteola had the highest percentage of cercariae infection. Statistical tests showed that the environmental factors of total dissolved solids, pH and salinity were significantly related with snail distribution and cercariae infection rather than spatial factor. The study demonstrated that the salinity, conductivity and total dissolved solids of pond water play a key factor for the distribution of snails and cercariae infection. The findings of our study will improve the understanding of the dynamics of schistosomiasis transmission and would ease the implementation of integrated disease control measures based on ecological knowledge of schistosomiasis vector in Madurai and Tamil Nadu zones.     

Effects of snail size and diet on encystment of Echinostoma caproni cercariae in juvenile Helisoma trivolvis (Colorado strain) and observations on survival of infected snails

The effects of snail size and diet on encystment of Echinostoma caproni cercariae in juvenile Helisoma trivolvis (Colorado strain) snails were studied. Encystment in neonatal (<1-mm shell diameter) and juvenile (2- to 3-mm shell diameter) snails was compared 24 hr postinfection (PI) after individual exposure of snails of each size to 1, 5, 10, 25, or 50 cercariae. Significantly more cysts were recovered from juvenile snails exposed to 10, 25, or 50 cercariae than from neonatals with comparable exposure. The maximum number of cysts recovered from juveniles exposed to 50 cercariae was 42, compared with a maximum of 15 cysts in neonatals comparably exposed. Size of H. trivolvis was a major factor in determining cyst burden in this planorbid. A diet of either Romaine lettuce leaf or hen's egg yolk did not have a significant effect on the number of cysts recovered at 24 hr PI from juvenile snails exposed to 25 or 75 cercariae. Survival of infected versus uninfected neonatals was also examined for 7 days. Neonatals exposed to 10 cercariae showed a significant decrease in survival at 6 and 7 days PI when compared with uninfected controls.     

Confirmation and identification of parasitic stages of obligate endobionts (Harpellales) in blackflies (Simuliidae) by means of rRNA sequence data

Over the last 35 y, the life cycle of endosymbiotic gut fungi (Harpellales) has been expanded to include cyst stages associated with the developing ovaries. Ovarian cysts (chlamydospore stages) have been identified after germination and production of asexual trichospores in vitro, but germination is not always successful, and spores exhibit morphological variation. Sequence data (for partial 18S and 28S rRNA genes) were generated for these putative stages of Harpellales using ungerminated cysts from adult blackflies and germinated cysts associated with field-collected blackfly egg masses. Cladistic analyses of the 18S and 28S rRNA sequences confirmed that ovarian cysts are stages in the life cycle of Harpellales. Ungerminated cysts, from a blackfly collected from New York state were identified as Pennella simulii and two samples from Newfoundland Prosimulium mixtum adults were identified as Harpella melusinae. Cysts with bipolar germ tubes, associated with field-collected Simulium egg masses from Newfoundland, were also identified as H. melusinae. Two other samples of cysts could not be matched with available sequences of gut fungi from larval hosts. The potential use of this approach to identify pathogenic stages associated with adult ovaries or field-collected egg masses among other host groups is highlighted and promoted as a tool to test the hypothesis that ovarian cysts are a dispersal stage common to all genera of Harpellales.     

Transplantation of Schistosoma japonicum daughter sporocysts in Oncomelania hupensis

Schistosoma japonicum daughter sporocysts obtained from infected Oncomelania hupensis hupensis were successfully transplanted to parasite-free O. hupensis hupensis. Survival and infection rates of recipient snails were 80% and 75% respectively. Intramolluscan development of transplanted daughter sporocysts in recipient snails appears to proceed in a similar manner as those reported for transplanted S. mansoni and S. haematobium in their respective snail intermediate hosts. Complete colonization of the digestive gland of recipient snails by sporocysts was observed 80 days after transplantation. Cercarial production during a 10-day observation from recipient snails was characterized by periods of high and low and irregular daily emissions. The average daily cercarial production was 150 per snail. Cercariae produced by recipient snails were infective to mice. Of those cercariae exposed to mice, approximately 30% developed to adult schistosomes. These results have definitive utility in the maintenance of S. japonicum in the laboratory.